Nova-page proof of cassava in Environmental Research Journal(2012)

Environmental Research Journal (2012) ISSN: 1935-3049Volume 6, Number 2, pp. © 2012 Nova Science Publishers, Inc.

ECO-PHYSIOLOGICAL RESEARCH FOR BREEDINGIMPROVED CASSAVA CULTIVARS IN FAVORABLE AND

STRESSFUL ENVIRONMENTS INTROPICAL/SUBTROPICAL BIO-SYSTEMS

Mabrouk A. El-Sharkawy1, Sara M. de Tafur2, and YamelLopez2

1Centro Internacional de Agricultura Tropical (CIAT) International Center for Tropical Agriculture, Cali,

Colombia2Universidad Nacional de Colombia–Palmira, Colombia

ABSTRACTThis chapter highlights eco-physiological, breeding and

agronomical research on the tropical starchy root cropcassava (Manihot esculenta Crantz) conducted at CIAT. Theobjectives were developing improved technologies needed toenhance productivity, root quality for human consumption andother uses, as well as conserving natural resources indifferent tropical/subtropical bio-systems where the crop isgrown. Laboratory and field studies have elucidated severalphysiological/biochemical mechanisms and plant traitsunderlying productivity in favorable conditions andtolerance to stressful environments such as prolonged waterstress and marginal low-fertility soils. Cassava is endowedwith inherent high photosynthetic capacity expressed in nearoptimal environments that correlates with biologicalproductivity and storage root yield across environments and

E-mail [email protected];

Environmental Research Journal (2012) ISSN: 1935-3049Volume 6, Number 2, pp. © 2012 Nova Science Publishers, Inc.

wide range of germplasm. Long leaf life, and hence betterleaf retention, with reasonable photosynthetic rates wasalso associated with high yields, particularly in prolongeddrought conditions. Extensive fine rooting systems capableof exploring deeper wet soils is another mechanism enhancingtolerance to water stress coupled with stomatal sensitivityto both atmospheric humidity and soil water shortages.Cassava leaves possess elevated activities of the C4phosphoenolpyruvate carboxylase ( PEPC) enzyme thatcorrelate with photosynthesis and productivity in field-grown crops, indicating its importance as another selectabletrait particularly for stressful environments. When cassavarecovers from stress, it rapidly forms new leaves withhigher photosynthetic capacity, which compensates for yieldreductions from the previous prolonged stress. Selecting formedium-statured and short cassava instead of tall cassava isadvantageous for saving on nutrient uptake and ensuringhigher nutrient-use efficiency for root production withoutsacrificing potential yield. Germplasm from the corecollection was screened for tolerance of soils low in P andK, resulting in the identification of several accessionswith good levels of tolerance. In cooler zones such ashigher altitudes in the tropics and lowland subtropics,cassava growth is slower and the crop stays in the groundfor longer time to achieve adequate yields. Under theseconditions, leaf formation is slower, leaf photosynthesis ismuch reduced, but leaf life is longer. Wide geneticvariations exist for photosynthesis that may be valuable forselecting and breeding for genotypes that better toleratecool climates. Combining enhanced leaf photosynthesis withthe normally longer leaf life in cool climates may improveproductivity. Results also point to the importance of fieldresearch versus greenhouse or growth-chamber studies that donot calibrate for representative environments to account foracclimation factors. Calibration becomes even more criticalwhen data from indoor-grown plants are used to extrapolateto the field or to develop crop models. Basic research canbe cost-effective, with high returns, even if slower. It canbe especially successful when conducted in collaborationwith multidisciplinary and/or multi-institutional teams thatfollow well-planned strategies and are focused towardsfulfilling a set of high priority goals and objectives. Muchremains to be done to further improve productivity whileconserving dwindling natural resources such as water and

Eco-Physiological Research for Breeding Improved CassavaCultivars …

land in view of the observed global climate changes.Developing countries, in particular, need more support tocontinue with maintenance research, which aims to upgradeprevious findings and technologies; contribute tosustainable agricultural, economic, and social developments;and enhance food supply to meet increasing demands.

INTRODUCTION

Cassava (manioc, yuca, or mandioca; Manihot esculenta Crantz,Euphorbiaceae) is a perennial shrub of the New World andbecame an important both as a cash crop and a subsistence cropof resource-limited farmers in Africa, Asia, and Latin Americaand the Caribbean with world production of more than 200million tons of storage fresh roots annually (El-Sharkawy,1993) (Figure 1).

The plant is outbreeding heterozygous polyploidy speciespossessing 2n =36 chromosomes. The germplasm is geneticallydiverse due to botanical, social and environmental influences.Botanically, the species is monoecious (female and maleflowers are separated on the same branch) that enhancespercentage of natural outcrossing (Jennings and Iglesias,2002).

Socially, man exerted great influence on the diversity ofthe species since its domestication more than 6000 years agoin the Amazonian region of Brazil (Allem, 2002). Women inparticular played a significant role in increasing the geneticdiversity of cassava where it is grown. For example, in Africawhere newly-wed women move to their husbands’ villages aftermarriage, they bring with them planting materials of their-choice of cassava varieties from their home farmingcommunities (Delêtre et al., 2011). Environmentally, naturalhybridization is a dynamic process and an important driver forgenetic diversity where farmers keep mixed cultivars on theirfields that normally results in the appearance of new races,some of which are targets for selection and adoption for theirdesired traits.

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Mabrouk A. El-Sharkawy, Sara M. de Tafur, and Yamel Lopez

The storage roots are used as a source of carbohydrate (eg,80-87% starch of dry matter) as protein is less than 3 percentin dry roots. They are grown mainly for human consumption,either prepared fresh as in the case of sweet cultivars low incyanogenic glucosides, or after processing into dry productssuch as flour, starch and animal feed in the case of bittercultivars high in cyanogenic glucosides (Balagopalan, 2002;Durfour, 1988; Essers, 1995; Westby, 2002; Montagnac et al.,2009a,b).

Figure 1. Clockwise: mature cassava plants, young cassavaplantation, and samples of storage roots. Source: CIAT;

IITA; Wikimedia Commons, David Monniaux.

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Cassava leaves are also consumed and constitute an excellentsource for protein supplement (leaf crude protein contents ona dry basis range among cultivars from 21% to 39%; Yeoh andChew, 1976; Ravindra, 1993), minerals and vitamins for thehuman diet in many African and Asian countries, as well as incertain regions of Brazil (Lancaster and Brooks, 1983;Montagnac et al., 2009b; Djuikwo et al., 2011). Nevertheless,cassava roots and leaves are deficient in sulphur-containingamino acids (eg, methionine and cysteine; Gil and Buitrago,2002, and Table 1).

Its often poorly-processed food products might contain someanti-nutrient elements such as free HCN, phytates andpolyphenols, and particularly acetone cyanohydrin, which iscommonly associated with an upper motor neuron disease knownas ´konzo syndrome´ in some African countries (Cliff et al.,2011; Tylleskar et al., 1992; Tylleskar, 1994). This occursmainly with large intake of inadequately processed bitter-cassava products in areas hit by long drought and withshortages of balanced diets. Table 1. Contents of some amino acids in cassava storage rootsand leaves, based on dry weight and total protein (adapted

with modifications after Gil and Buitrago, 2002).Note the low contents of cysteine and methionine

Amino acid Storage roots % of dry wt.

% of protein

Leaves% ofdry wt. % of

protein

Alanine 0.15 5.70 1.70 6.10ArginineAspartic acidCysteine

0.290.130.01

11.004.900.40

1.482.440.21

5.308.700.70

Glutamic acid 0.15 5.70 1.99 7.10GlycineHistidine

0.010.07

0.40 2.60

1.730.66

6.202.30

Leucine 0.31 11.30 2.72 9.70Lysine Methionine

0.070.03

2.601.00

1.870.36

6.701.30

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PhenylalanineSerine

0.030.04

1.001.50

0.921.68

3.306.00

Threonine 0.03 1.00 1.35 4.80Tyrosine 0.01 0.40 0.89 3.20

Some of those compounds may also act as anti-oxidants andanti-carcinogens, which may result in adverse effects onhealth if ingested in large amounts (Montagnac et al.,2009a,b; Tsumbu et al., 2011).

The crop also has many different alternative uses asprocessed food, animal feed, starch, alcohol and biofuel.Compared to other energy crops, cassava under favorableproduction conditions produces more annual ethanol per unitland area (Jansson et al., 2009; Sierra et al., 2010, Table 2)[but also see other estimates (Johnston et al., 2009; Spiertzand Ewert, 2009) ]. Another value-added potential is thepossibility of genetically engineer cassava toward transferand overexpressing the genes controlling ´human serum albumin´protein (HSA) in cassava storage roots that might lead toeconomic production of highly needed HAS (current demand isabout 500 or more tons annually), an achievement recentlyobtained with rice grains by Chinese researchers (He et al.,2011).

In contrast to water-loving rice, cassava is a versatile andresilient plant that can tolerate and produce reasonably wellin harsh environments under hot weather coupled with prolongeddrought and marginal soils. Water requirements for theproduction of one ton of dry matter in cassava storage rootsand in rice grains are approximately 400-500 and 3500-4000tons, respectively. In view of shortages in irrigation waterresources and/or in rainfall that will probably be furtheraggravated in most tropical/subtropical regions, caused bypredicted Global Climate Change when average temperature ofearth atmosphere reaches probably 2.4-6.5 ºC above current bythe end of this century (El-Sharkawy and De Tafur, 2011), thecomparative advantage would be at the side of cassava.

Table 2. Comparative advantage of cassava as a potentialbiofuel crop versus other energy crops (adapted with

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modifications after Jansson et al., 2009). Yield estimates arebased on favorable production conditions

Crop species

Average yield(Ton ha-1 year-1)

Conversion rate to bioethanol (Liter ton-1)

Bioethanol yield(Liter ha-1 year-1)

Cassava 40 (fresh storage roots) 150 6,000

Sugarcane 70 (stalks) 70 4,900Sweet sorghum 35 (biomass) 80 2,800

Rice 5 (grains) 450 2,250Maize 5 (grains) 410 2,050

Wheat 4 (grains) 390 1,560

As countries develop their demand for these productsincreases dramatically. Under the marginaltropical/subtropical conditions where it is normally grown(with prolonged drought and low-fertility soils), it producesmore energy per unit area than other crops, and is highlycompatible with many types of intercrop. Thus, cassava’sresilience makes it ideal for food security in marginalenvironments where other staple crops such as cereals andgrain legumes might fail to produce. Because of its metabolicefficiency and other traits described below, cassava is anoutstanding starch biosynthesis plant in both lowland subhumidand humid high-productivity environments. It is practicallyaxiomatic that where there’s cassava there’s no famine. It canbe grown with minimal inputs, but gives considerably higheryields with fertilizers and good management.

The crop is flexible as to time of harvest and can be storednaturally for long periods by keeping the plants in the fieldwith the roots in the soil. Cassava roots are highlyperishable once harvested (van Oirschot et al, 2000), androots must be used immediately or processed into dry products,although pruning three weeks before harvest will reducedeterioration. Therefore, cassava needs to be processed near

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production fields, making it an ideal vehicle for ruraldevelopment through creating employment opportunities in theareas where it is grown.

Although cassava presumably originated in hot humid climatesin the Amazonian lax forests (Allem, 2002), it shows a highdegree of tolerance to prolonged drought in areas with low anderratic precipitation of less than 600mm annually, coupledwith dry air and high temperatures (hence, high potentialevapotranspiration), low fertility soils and high pest anddisease pressure such as in Northeastern Brazil, the northerncoast of Colombia, the west coast of Peru, some areas in sub-Saharan African countries, and parts of Thailand (El-Sharkawy,1993). Cassava is widely grown in countries of tropical andsubtropical Africa, Asia and Latin America between latitudes30o N and S, from sea level to above 2000 masl by resource-limited smallholder farmers on marginal and highly-eroded low-fertility acidic soils, virtually without the application ofagrochemicals (El-Sharkawy, 1993, 2004; Ruppenthal et al,1997).

By not having specific water-stress sensitive growth stagesbeyond crop establishment (compared with, e.g., grain crops),cassava can survive and produce under conditions where otherstaple food crops, such as grain cereals and legumes, wouldrarely produce. These inherent characteristics have motivatedthe expansion of the crop into more marginal lands across manyparts of Africa, Asia and Latin America. Notable is its recentexpansion in sub-Saharan Africa (Romanoff and Lynam, 1992)where its tolerance to various edapho-climatic stresses givesan advantage over other staples (Cadavid et al, 1998; De Tafuret al, 1997b; El-Sharkawy, 1993; Flörchinger et al, 2000;Fermont 2009).

Field research (El-Sharkawy, 2004, 2006a,b, 2007,2009, 2010;El-Sharkawy and De Tafur, 2007, El-Sharkawy et al.,1990,1992a,1993, 2008) has elucidated several physiological plantmechanisms underlying cassava’s potentially high productivityunder favourable hot-humid environments in the tropics. Mostsignificant is its inherent capacity to assimilate carbon innear optimum environments, correlating with both biologicalproductivity and storage root yield in a wide range of

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accessions from cassava core germplasm at CIAT grown indiverse environments over years. Cassava leaves possesselevated activity of the C4 phosphoenolpyruvate carboxylase(PEPC) enzyme that correlates with leaf photosynthesis, leafphotosynthetic nitrogen use efficiency (PNUE) and storage rootyield in field-grown plants, indicating the importance ofselection for high photosynthesis. Under certain conditions,leaves exhibit a very interesting photosynthetic C3-C4

intermediate behaviour which may have important implicationsin future selection efforts. In addition to leafphotosynthesis, yield is also correlated with seasonal meanleaf area index (LAI), ie, leaf area duration.

Under prolonged water shortage in seasonally dry and semi-arid zones (El-Sharkawy, 1993, 2006a,b, 2007, 2010; De Tafuret al.1997b) once established, the crop tolerates the stressand produces reasonably well compared to other food crops. Forexample, in environments with less than 700mm of annual rain,with 6 month dryness, improved cassava cultivars can yieldover 3t ha−1 of oven-dried storage roots. The underlyingmechanisms for such tolerance include stomatal sensitivity toatmospheric and edaphic water deficits, coupled with deeperrooting capacities that prevent severe leaf dehydration (ie, astress avoidance mechanism), and reductions in the leaf canopywith reasonable photosynthesis over the leaf lifespan. Anotherstress-mitigating plant trait includes the capacity to recoverfrom stress once water becomes available, by forming newleaves with even higher photosynthetic rates than those ofnon-stressed crops.

Under extended stress (El-Sharkawy and Cock, 1987b; El-Sharkawy and Cadavid, 2002; El-Sharkawy et al., 1992b) thereduction in biomass is greater in the shoot than in thestorage root, resulting in a higher harvest index (HI).Cassava conserves water by slowly depleting available waterfrom deep soil layers, leading to higher water-use efficiency(WUE) and nutrient-use efficiency (NUE). In dry environments,leaf area duration and resistance to pests and diseases arecritical for sustainable yields. Cassava can survive in thesemi-arid zones but a second wet cycle is required to achieve

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higher yields in this situation, where selection and breedingfor early bulking and for medium/short-stemmed cultivars willbe advantageous.

When grown in cooler zones such as in the tropics at highaltitudes and in lowland subtropics, growth is slower and leafphotosynthesis is greatly reduced. Thus, the crop requires alonger period for reasonable productivity. Here, there is aneed to select and breed for more cold-tolerant genotypes.

This chapter reviews and highlights some of theecophysiological research conducted at CIAT, particularlyunder relevant field conditions where most cassava is grown,in relation to breeding improved cultivars for both favorableand stressful environments. The research had laid thefoundations for cassava breeding and selection of adaptablecultivars under both environments.

CASSAVA TOLERANCE TO DROUGHT AND CONTROLLINGPHYSIOLOGICAL MECHANISMS

Responses to Extended Water Deficits in the Field

Inherent plant mechanisms that may underlie tolerance todrought in cassava have been elucidated and described (El-Sharkawy, 1993, 2004, 2006a,b, 2007, 2010; Caýon et al, 1997;De Tafur et al, 1997a,b; El-Sharkawy et al, 1992b). Mostnotable is the striking sensitivity of cassava to both changesin atmospheric humidity and soil water deficits – viapartially closing its stomata and restricting water loss onceexposed to dry air and/or dry soils, thus protecting the leaffrom severe dehydration – coupled with leaf capability topartially retain its photosynthetic capacities under prolongedwater shortages. Compared to several woody and herbaceousspecies, cassava is more sensitive to changes in air humidity(Cock and El-Sharkawy, 1988b; El-Sharkawy and Cock, 1986; El-Sharkawy et al, 1984d, 1985), and the response has beenrelated to stomatal density and maximum leaf conductance (El-Sharkawy and Cock, 1986; El-Sharkawy et al, 1984d,1985).

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Cassava leaves possess large number of stomata on the abaxialepidermis (> 400 stomata mm−2; Connor and Palta, 1981; El-Sharkawy et al, 1984a; Guzman 1989; Pereira, 1977) that mayunderlie the strong response to humidity (El-Sharkawy and Cock1986; El-Sharkawy et al, 1985).

The phenomenon of direct stomatal response to air humiditywas observed as early as the late 19th and early 20th centuriesby botanists (El-Sharkawy and Cock, 1986; Haberlandt, 1914;Thoday, 1938). Numerous more recent reports have shown thatseveral herbaceous and woody plant species tend to close theirstomata in response to dry air, whether observed within theplant community or in attached leaves and isolated epidermalstrips (eg, Aston, 1976; Bongi et al, 1987; Bunce, 1981, 1982,1984; Fanjul and Jones, 1982; Farquhar et al, 1980; Gollan etal, 1985; Hall and Hoffman, 1976; Hall and Schulze, 1980;Held, 1991; Hirasawa et al, 1988; Hoffman and Rawlins, 1971;Hoffman et al, 1971; Jarvis, 1980; Jarvis and McNaughton,1986; Kappen and Haeger, 1991; Kaufmann, 1982; Körner, 1985;Körner and Bannister, 1985; Lange et al, 1971; Leverenz, 1981;Lösch, 1977, 1979; Lösch and Schenk, 1978; Lösch and Tenhunen,1981; Ludlow and Ibaraki, 1979; Meinzer, 1982; Pettigrew etal, 1990; Rawson et al, 1977; Sheriff and Kaye, 1977; Schulze,1986; Schulze and Hall, 1982; Schulze et al, 1972; Tazaki etal, 1980; Tibbitts, 1979; Tinoco-Ojanguren and Pearcy, 1993;Ward and Bunce, 1986). This apparently widespread phenomenonindicates the need for detailed studies and for itsconsideration while modelling plant community/environmentecosystems (Jarvis and McNaughton, 1986).

The adaptive ‘stress avoidance mechanism in cassava’operating via stomatal sensitivity to both edaphic andatmospheric water deficits is of paramount importance for thecrop’s tolerance to prolonged drought (more than three months)combined with hot dry air in seasonally dry and semi-aridzones (De Tafur et al. , 1997a,b; El-Sharkawy, 1993). Coupledwith this mechanism is the deeper rooting system (below twometres soil depth) that allows the crop to extract storagewater when available (Cadavid et al, 1998; CIAT, 1983, 1994;Connor et al, 1981; De Tafur et al, 1997a; El-Sharkawy and

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Cock, 1987b; El-Sharkawy et al, 1992b; Porto, 1983). Althoughcassava has sparse fine root systems compared with other cropssuch as cereals and tropical grasses (Tscherning et al, 1995),it is capable of penetrating into deeper soil layers. Thisenables the plant to endure long periods of drought, onlyslowly depleting deeper stored water, with the end results ofhigher seasonal crop WUE, albeit at reduced productivity(Connor et al, 1981; El-Sharkawy, 1993, 2004; El-Sharkawy andCock, 1986, 1987b; El-Sharkawy et al, 1992b).

Another characteristic of great importance in conservingwater under extended stress is the large reduction in lightinterception (Figure 2; CIAT, 1991, 1992, 1993,1994, 1995)achieved through a reduced leaf canopy due mainly torestricted formation of new leaves, a smaller leaf size, andleaf fall (Connor and Cock, 1981; El-Sharkawy and Cock, 1987b;El-Sharkawy et al, 1992b; Palta, 1984; Porto, 1983). Althougha reduction in leaf area conserves water, it would also leadto a reduction in total biomass and yield ( CIAT, 1991, 1992,1993, 1994,1995; Connor and Cock, 1981; Connor et al, 1981;El-Sharkawy and Cadavid, 2002; El-Sharkawy and Cock, 1987b,El-Sharkawy et al, 1992b, 1998b; Porto, 1983). However,cassava can recover rapidly once released from stress byforming new leaves.

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Figure 2. Light interception in water-stressed and well-watered cassava crops. Measurements were made with light

sensors placed on top of the canopy and at soil level in themiddle of plots. Note the large reductions in light

interception overtime in the stressed crops due to reducedleaf formation, the small size of new leaves and the loss of

old leaves, and the increase in light interception afterrecovery from stress due to the formation of new leaves.

Source: CIAT, 1991; El-Sharkawy, 1993.

These increase light interception and canopy photosynthesis,thus compensating for previous losses in biomass, particularlyroot yield (CIAT 1991, 1992, 1993, 1994, 1995, 1998b; El-Sharkawy, 1993; El-Sharkawy and Cadavid, 2002; El-Sharkawy andCock, 1987b; El-Sharkawy et al, 1992b). Cassava leaves alsoremain reasonably active during water shortages in the field(Figure 3). Stressed leaves are capable of maintainingphotosynthetic rates around 40–60 percent of that of non-stressed leaves during an entire three month stress period.There are differences among cultivars, with the hybridCM 489-1 showing the least reduction.

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Figure 3. Response of cassava leaf photosynthesis toprolonged water stress (120 d), imposed at 60 d after

planting (control, open symbols; stress, solid symbols). From CIAT (1987-1989) Report; El-Sharkawy., 2010.

Upon recovery from stress, the previously stressed leavescan approach the photosynthetic rates of non-stressedcontrols. Furthermore, the newly-formed leaves of thepreviously stressed crop show even higher photosynthetic ratesthan non-stressed plants (Figure 4). These higher

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photosynthesis rates coincide with higher stomatal conductanceto water vapor, higher mesophyll conductance to CO2 diffusionand higher levels of nitrogen, phosphorus, calcium andmagnesium in leaves compared with controls (Cayón et al, 1997;CIAT, 1990; El-Sharkawy, 1993). Moreover, Cayón et al (1997)reported greater mobilization of potassium out of newlydeveloped leaves, with new leaves in previously stressed cropsconsistently containing an average of 0.79 percent potassiumcompared with 0.96 percent in non-stressed ones. This suggestsa higher demand for assimilates in storage roots, sincepotassium is normally translocated along with sugars to sinks(Giaquinta, 1983).

Figure 4. Response of field-grown cassava to prolongedmidseason water stress. Cassava plants were deprived of

water by covering the soil surface with white plastic sheetsfor three months, commencing 90 d after planting. Plants

recovered from stress (see arrows in A and B) under rainfalland supplemental irrigation for the rest of the growthcycle. The control plants received normal rainfall plussupplemental irrigation. Leaf gas exchange was monitored

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with a portable infrared gas analyzer throughout the stressand recovery periods. A. Leaf photosynthesis during stressand recovery for leaves developed under stress. B. Stomatal

conductance. C. and D. Photosynthesis and stomatalconductance for new leaves developed after stress was

terminated. From CIAT, Cassava Physiology Section database(1991) Annual Report; El-Sharkawy, 1993.

Accordingly, leaf photosynthesis is also controlled in thiscase by sink demand and strength (Burt, 1964; El-Sharkawy,2004; Herold, 1980; Ho, 1988; Humphries, 1967; Nösberger andHumphries, 1965; Pellet and El-Sharkawy, 1994; Thorne andEvans, 1964; Wardlaw, 1990), suggesting that the dynamics ofpotassium in leaves of field-grown cassava might be used as anindicator of root sink strength and source-sink relationships.

Lack of Osmoregulation in Cassava under Extended Water Stress

In the same studies, predawn leaf water potential (Figure 5A,CIAT, 1992) remained around -0.5MPa for all cultivarsthroughout most of the stress period of three months, withvirtually no differences between the stressed and unstressedcrops. Midday leaf water potential (Figure 5 B) in allcultivars in both stressed and unstressed crops oscillatedbetween −0.6 MPa (when presumably a lower leaf-to-air vaporpressure deficit (VPD) during a wet period coincided with thetime of measurement) and −1.6 MPa (at a much higher VPD duringdry/sunny periods), with slight reductions often observed inthe stressed crops. These values are within the rangespreviously reported for cassava under extended periods of soilwater shortages in the field (Caýon et al, 1997; Cock et al,1985; Connor and Palta, 1981; De Tafur et al, 1997a; El-Sharkawy et al, 1992b; Porto, 1983). They are higher thanthose normally observed in other field crops under stress,indicating that cassava conserves water and prevents extremeleaf dehydration due to its stomatal sensitivity to stress(ie, stress avoidance mechanism).

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It appears, therefore, that the phenomenon of osmoticadjustment (OA) in mature leaves developed under water stressand other edaphic stresses, as observed in several other fieldcrops (Ackerson and Hebert, 1981; Hsiao, 1973; Hsiao, et al1976; Jones and Turner, 1978; Morgan, 1984; Turner et al 1978)is not operating in field-grown cassava, since predawn andmidday bulk leaf water potential always remained above −0.8MPa and −2.0 MPa respectively, during prolonged waterdeficits. Hence, OA is of a little importance as a possiblemechanism underlying cassava tolerance to drought. In recentstudies with potted greenhouse-grown cassava, Alves (1998)reported that the greatest increases in solutes after few daysof water deficit occurred in the youngest and folded (ie, notfully expanded) leaves, with the least increases in matureones, pointing to little importance of OA in mature leaves.Nevertheless, such studies need to be carried out on field-grown plants if results are to be extrapolated to fieldconditions, and for obviating acclimation problems (El-Sharkawy, 2005).

Since osmoregulation requires investment and accumulation ofsolutes and assimilates for its development under stresses,McCree (1986) discussed the relative carbon costs involved inthe process of OA in sorghum grown under both water deficitand salinity. This author concluded that the metabolic cost ofstoring photosynthate and using it for OA was less than thecost of converting it to new biomass, although the costincreased slightly under salinity. Under drought, changes inthe biosynthesis, content and distribution of plant growthregulators such as abscisic acid (ABA) within plant organs andtissues (particularly in roots, leaves and buds) may play animportant role in sensing changes in both soil water andatmospheric humidity, and in controlling stomatal movements,leaf formation and extension, root growth, bud dormancy. Theymay also be involved in other biological functions such asactivation and expression of PEPC, and in possibleswitching/induction from C3 to crassulacean acid metabolism(CAM) or C4 photosynthesis in some species (Ackerson, 1980;Chapin, 1991; Chu et al, 1990; Davies et al, 1986; Henson,

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1984a; 1984b; Huber and Sankhla, 1976; Jones and Mansfield,1972; Jones et al, 1987; Radin, 1984; Radin et al, 1982;Schulze, 1986; Taybi and Cushman, 1999; Turner, 1986; Ueno,2001; Walton, 1980; Zeevaart and Creelman, 1988; Zeiger, 1983;Zhang and Davies, 1989).

Figure 5. Leaf water potential in water-stressed and well-watered cassava crops during a stress period initiated at 90days after planting. Measurements were made with a pressure

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chamber in a field laboratory. Values are means of 5-10leaves from the upper canopy. A: predawn; B: midday. Notethe small differences between the two crops in the predawn

and midday water potential and the increases in waterpotential in the period of high ambient humidity. Thepredawn and midday levels were above −0.8 and −2.0 MPa,respectively, indicating the striking stomatal control in

cassava regardless of soil water status. Source: CIAT, 1991.

These remarkable physiological responses to mid-season waterstress point to cassava’s potential to tolerate prolongeddrought and to its resilience and ability to recover fromstress when water becomes available, such as in subhumid zoneswith intermittent dry spells or in seasonally dry zones withwell-marked bimodal rainfall distribution. Under theseconditions, longer leaf life coupled with resistance to pestsand diseases (Byrne et al, 1982; El-Sharkawy 1993; El-Sharkawyet al., 1992b; Lenis et al., 2006) which allows better leafretention, is advantageous in saving dry matter invested inleaves and in allowing partitioning of excess photosynthatestoward storage roots. In semi-arid zones with less than 600mmof rain annually and with periods of water deficits longerthan four to five months, such as in Northeastern Brazil,northeastern Colombia and sub-Saharan Africa (De Tafur et al,1997b; El-Sharkawy, 1993, 2004, 2007), the crop can survive,albeit with greater losses of leaf canopy and less dry matterin the storage roots. In this ecosystem, a second wet cycle isneeded to allow recovery of growth and complete filling ofroots.

Moreover, the use of gene manipulating/transgenicbiotechnology coupled with development of molecular markers tofacilitate the introgression into cassava cultivars gene(s)controlling ‘exotic’ and specific drought-tolerance relatedtraits such as ‘staygreen’ was recently suggested (Orek et al.2008; Vanegas, 2008; Zhang et al. 2010) which may accelerateidentifying genes controlling leaf retention, particularly inshort-stemmed cassava cultivars with small leaf canopy (El-Sharkawy and De Tafur, 2010).Transgenic cassava lines (eg,SAG12-IPT ) that express a cytokinin biosynthesis gene ( IPT )

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from a senescence enhanced promoter (SAG12) showed an extendedleaf life. Accordingly, several aspects of senescence aredelayed in the leaves of these transgenic lines, includingchlorophyll degradation, protein degradation and Rubiscoreduction. Cassava´s Rubisco activities are very sensitive towater stress (El-Sharkawy, 2004, 2006 b) which might beenhanced via this line of research. It appears that furtherphysiological and agronomical characterizations of these linesalso revealed that the induced expression of the gene ÍPTáffected photosynthesis, sugar allocation and nitrogenpartitioning (Zhang et al., 2010). Nevertheless,Vanegas (2008)reported that a transgenic clone ´529-28´that expressed thegene ÍPT´ showed longer leaf life and greater leaf biomass butwith reduction in dry root yield indicating a lack oftranslation into agronomic advantages. However, since wholeplant tolerance to water stress is apparently underpinned byseveral morphological, anatomical, physiological andbiochemical mechanisms and traits, transfering/inserting oneor few éxotic genes´ might not be the ultimate panacea fordrought tolerance in cassava (Bohnert et al., 1996). Suchapproach needs to be scrutinized through evaluating thesetransgenic lines for genetic stability, productivity andtolerance to natural prolonged drought at the farm level.

A recent obscure report (Okogbenin et al., 2010), and hencegiven conclusions, based on deficient experimentation schemesand not substantiated with relevant hard data must beseriously questioned concerning its utility for cassavaimprovement. In contrast, the pioneering ecophysiologicalresearch achievements highlighted in this chapter andelsewhere had laid the foundations for the first time of asuccessful strategy for cassava improvement in both favorableand stressful environments (El-Sharkawy and Cock, 1987b; Cockand El-Sharkawy, 1988a,b; El-Sharkawy et al., 1992b; Hersheyand Jennings,1992; Iglesias et al., 1995,1996; El-Sharkawy,1993, 2004, 2006a,b, 2010) . Furthermore, to increasethe benefit-cost ratio of research, it is recommended here tocombine the genetic engineering efforts with available soundagronomic, physiological, biochemical and conventionalbreeding/genetic information on whole plant responses to

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extended water shortages under field conditions (i.e.,holistic approach, El-Sharkawy, 2006a). Ryder (1984) wiselyremarked: “I believe very strongly that the technology we callgenetic engineering and its attendant sciences andtechnologies should be pursued. The potential benefits areworth the pursuit. I do not wish to see the support of geneticengineering undertaken, however, on the basis of broad edicts,at the expense of other aspects of plant breeding and itsattendant sciences and technologies”. Donors, scientists, andresearch managers must be aware of the shortcomings offashion-type (bandwagon!) research projects/programs thatserve mostly short-sighted self-interests. Moreover, abidingby scientific ethics must be the rule against violation ofintellectual property rights and plagiarism often occurring inscience. In this regard, Garfield (1991) wrote on the problemof literature citation violations, misuse and omissions byresearchers coining it “bibliographical negligence andcitation amnesia” and suggested that authors should sign apledge or oath that they have done a minimal search of theliterature and that to the best of their knowledge there is noother relevant original work not being correctly acknowledgedand properly cited (see Gallagher, 2009).

Cassava Photosynthesis and C3-C4 Intermediate Characteristics Underpenning Tolerance to Drought

Previous research on cassava photosynthesis demonstrated theimportance of elevated activity of the C4 enzyme PEPC that maypartially underlie the high photosynthetic capacity incassava, which was found to be correlated with highproductivity across environments, including marginal ones.

Table 3. Activity of C4 PEPC in leaf extracts. Values are meanof four leaves ± SD. Note the much higher activity in cassavaas compared to beans, a C3 species, and the very high activityin wild Manihot (about 30–40 percent of the activity in maize,

a C4 species). In a group of field-grown cultivars underprolonged water stress, net leaf photosynthesis (Pn) was

21


significantly correlated with PEPC activity measured on thesame leaves (El-Sharkawy, 2004), indicating the importance ofselection and breeding for elevated PEPC activity. It is alsonoteworthy that wild Manihot also possess an additional short

palisade layer beneath the lower leaf surface and withnumerous stomata on both leaf surfaces, two traits

advantageous for enhancing photosynthesis (El-Sharkawy, 2004).

Sources: Cassava Physiology Section database; El-Sharkawy,2004; El-Sharkawy and Cock, 1990; El-Sharkawy, Bernal and

López, unpublished observations)

SpeciesPEPC activity (µmol NADH)

gfw−1 min−1 mg chl−1min−1

Maize (cv CIMMYT 346) 15 ± 1.8 7 ± 3.6Common beans (cv Calima G4494)

0.2 ± 0.07 0.3 ± 0.1

CassavaM Mex 59 3.2 ± 0.6 2.2 ± 1.0M Nga 2 1.3 ± 0.1 0.4 ± 1.0Wild speciesManihot grahami 4.0 ± 0.9 2.8 ± 1.2Manihot rubricaulis 5.8 ± 0.6 3.4 ± 1.3Thus, several cassava cultivars and wild species showed

activities from 15 to 25 percent of those in C4 species such asmaize and sorghum, with activities ranging from 1.5 to over5µmol mg-1 chlorophyll min-1 (Table 3; Bernal, 1991; CIAT, 1990,1991, 1992, 1993, 1994; Cock et al, 1987; De Tafur et al,1997b; El-Sharkawy 2004, 2009; El-Sharkawy and Cock, 1987a;1990; El-Sharkawy et al, 1990,1992a ,1993; López et al, 1993;Pellet and El-Sharkawy, 1993a). These PEPC activities observedin cassava and its wild relatives are much greater than thoseobserved in C3 species such as field beans, and are comparableto activities found in several C3–C4 intermediate Flaveriaspecies with a limited functional C4 cycle and two to threetimes greater than those in the C3–C4 Kranz-like Panicum milioides(Brown and Bouton, 1993; Ku et al, 1983).

22


EFFECTS OF WATER STRESS ON PHOTOSYNTHESIS ENZYMES

Under prolonged drought in the field coupled with hot dryair under intense solar radiation, leaves of over 100 cassavacultivars remained photosynthetically active, although at muchreduced rates (De Tafur et al, 1997a,b; El-Sharkawy, 1993; El-Sharkawy et al,1990, 1992b). Three weeks after initiation ofwater stress, PEPC, ribulose-1,5-bisphosphatecarboxylase/oxygenase (Rubisco) and the C4 decarboxylasenicotinamide adenine dinucleotide–malic enzyme (NAD–ME) showedreduced activity, with the highest reduction occurring inRubisco activity in one month-old leaves that had developedbefore stress started (Table 4; CIAT 1993).

The PEPC/Rubisco ratio, which may indicate the relativeimportance of these two enzymes, was also reduced by stress.However, when leaves that developed under stress for eightweeks were assayed, PEPC activity across all clones was13 percent greater than unstressed crops with differencesamong accessions (Table 5; CIAT 1993), whereas Rubiscoactivity was 42 percent less in the stressed crops. Thisdifferential effect of stress on the activities of these twokey photosynthetic enzymes resulted in a much higherPEPC/Rubisco ratio in the stressed crops as compared to theunstressed ones.

Table 4. Activity of photosynthetic enzymes in leaf extractsof field-grown cassava as affected by three weeks of water

stress commencing 92 days after planting (DAP) at Santander deQuilichao, Colombia. Values are means ± SD; activities are

expressed in µmol mg chl−1 min−1. Note the much greaterreduction in activity of the C3 Rubisco, as compared with theC4 PEPC, in leaves that developed before initiation of stress.

Sources: Cassava Physiology Section database; CIAT, 1993;Lopez and El-Sharkawy, unpublished observations

Clone

Unstressed Stressed

PEPC Rubisco NAD-ME

PEPC/Rubisco

PEPC Rubisco NAD-ME

PEPC/Rubisco

CM 4013- 0.37 ± 0.31 ± 0.40± 0. 1.19 0.31 ± 0.41 ± 0.19 ± 0.76

23


1 0.60 0.05 06 0.03 0.09 0.05CM 4063-6

0.57 ± 0.06

3.72 ± 0.11

0.39 ± 0.06

0.15 0.41 ± 0.04

1.69 ± 0.10

0.17 ± 0.09

0.24

SG 536-1 0.67 ± 0.05

0.39 ± 0.20

0.55 ± 0.18

1.72 0.57 ± 0.12

0.81 ± 0.20

0.39 ± 0.50

0.70

M Col 1505

0.45 ± 0.01

1.18 ± 0.08

0.16 ± 0.02

0.38 0.49 ± 0.10

0.49 ± 0.12

0.29 ± 0.06

1.00

Average 0.51 1.4 0.38 0.86 0.45 0.85 0.26 0.68% change due to stress −12 −39 −32 −21

Table 5. Activity of some photosynthetic enzymes in leafextracts of field-grown cassava as affected by eight weeks ofwater stress commencing at 92 DAP at Santander de Quilichao;

values are means ± SD; activities are expressed inµmol mg chl−1 min−1. Note the large reductions in activity ofthe C3 Rubisco, as compared to the C4 PEPC, in leaves thatdeveloped under stress resulting in a greater PEPC/Rubisco

ratio. This photosynthesis-based biochemical assay has provedits utility in selection for tolerance to prolonged drought,see data in Tables 12 and 13. Sources: Cassava Physiology

Section database; CIAT, 1993; Lopez and El-Sharkawy,unpublished observations)

Clone

Unstressed Stressed

PEPC RubiscoPEPC/Rubisco

PEPC RubiscoPEPC/Rubisco

CM 4013-1 0.86 ± 0.12

0.28 ± 0.10

3.10 1.18 ± 0.17

0.30 ± 0.01

3.9

CM 4063-6 0.89 ± 0.05

2.30 ± 0.03

0.39 1.42 ± 0.26

0.62 ± 0.02

2.3

SG 536-1 1.46 ± 0.42

0.44 ± 0.12

3.30 1.33 ± 0.22

0.25 ± 0.08

5.3

M Col 1505 1.09 ± 0.10

0.57 ± 0.13

1.90 0.96 ± 0.16

0.89 ± 0.14

1.1

Average 1.08 0.9 2.2 1.22 0.52 3.2% change due to stress +13 −42 +45

These data indicate that, under prolonged water deficit, therelative importance of the C4 PEPC versus the C3 Rubiscobecomes more pronounced, and lends support to the hypothesisthat the C4 PEPC enzyme may play a significant role inphotosynthetic activity under drought coupled with high air

24


temperatures (CIAT, 1993; El-Sharkawy, 2004). This is ofparamount importance in reducing both photorespiratory andmitochondrial dark CO2 losses, and in increasing net carbonuptake and hence productivity. Moreover, the recent evidenceabout the possible location of PEPC in the upper end of thelong palisade parenchyma further supports the role of PEPCinvolvement in refixation/recycling respiratory CO2 when thehighly dense abaxial stomata are partially closed underdrought, high solar irradiances and high temperatures coupledwith dry air. This is particularly the case in hypostomatousleaves that normally possess more than 400 stoma per square mm(El-Sharkawy et al., 1984a). Besides increasing carbon uptake,such a CO2 recycling mechanism protects the leaves fromphotoinhibition via dissipating excess absorbed photons(Osmond et al, 1980; Osmond and Grace, 1995).

CHARACTERIZATION OF WATER STRESS TOLERANCE

Mechanisms Underlying Stomatal Response to Air Humidity

Many workers have reviewed and discussed the possiblemechanisms underlying stomatal sensing of changes in airhumidity and the role of the so-called ‘peristomataltranspiration’ – first hypothesised by Seybold (1961/1962) –due to water loss from the cuticle of the guard and subsidiarycells and their adjacent epidermal cells, in the control ofstomatal movement (Lange et al, 1971; Lösch and Schenk, 1978;Lösch and Tenhunen, 1981;Maier-Maercker, 1979a,b, 1983;Meidner, 1976; Meidner and Mansfield, 1968; Sheriff, 1977,1979, 1984; Tyree and Yianolis, 1980; Zeiger, 1983). Supportfor Seybold’s hypothesis on the role of peristomataltranspiration was demonstrated through extensive research byGerman workers using intact leaf and isolated epidermal stripsystems without water stress (Lange et al, 1971; Maier-Maercker, 1979a,b, 1983; Lösch and Tenhunen, 1981). Others(Meidner and Mansfield, 1968) have argued that stomatalmovements are most likely to be affected primarily by the

25


water status of mesophyll tissue through a feedback reaction,rather than by changes in atmospheric humidity.

Kramer (1983) cautioned against the proposed role ofperistomatal transpiration until more information becameavailable concerning the degree of cutinization of mesophylltissue (where the bulk of evaporation presumably takes place),of the epidermis and of the inner/external walls of guardcells. Appleby and Davies (1983) demonstrated possible sitesof evaporation in cuticle-free areas in the guard cell wallsof oak (Quercus robur), poplar (Populus nigra) and Scots pine (Pinussylvestris) which could be exposed on the outside of the leafduring stomatal closure in dry air. Also, Körner and Cochrane(1985) reported lesser degrees of cutinisation of the externalwalls of guard cells in Eucalyptus pauciflora that may underlie itsstomatal sensitivity to changes in air humidity.

Sheriff (1977, 1979, 1984) suggested that the mechanismunderlying direct stomatal response to low humidity involvesboth evaporation from the epidermis and lower hydraulicconductivity within the leaf that may accelerate water stressin the epidermis, regardless of leaf water content. Recently,Pieruschka et al. (2010) reported that the water balance inthe epidermis is very sensitive to differences between thetranspiration rate and the rate at which absorbed radiationproduces water vapor inside the leaf. These authors suggestedthat leaf heat load is tightly linked to water transport frommesophyll cells, through the epidermis, to the leaf’senvirons. This important finding further explains why cassavaleaves orient themselves towards the sun in early morning andlate afternoon (also called heliotropism or sun tracking) whenVPD is lowest, and droop at mid-day (also calledparaheliotropism or sun avoidance) when VPD is highest (El-Sharkawy and Cock 1984; Berg et al.1986), thus optimizingwater-use efficiency. Tyree and Yanoulis (1980) used physicalmodels of the substomatal cavity to calculate water vapourdiffusion patterns and concluded that, due to high evaporationfrom guard cells, stomata could close in direct response tolow humidity. They suggested that localised water stress ordehydration in guard cells may take place due to a high leaf

26


resistance to the flow of liquid water from the minor leafveins to the guard cells.

The strong association between stomatal density (ie, exposedepidermal areas) and the degree of sensitivity to changes inair humidity that was observed in well-watered plants acrossmany herbaceous and woody species (El-Sharkawy et al, 1985)may indicate the occurrence of localised dehydration in thestomatal apparatus and adjacent exposed epidermal cells, hencesupporting the role of peristomatal transpiration incontrolling stomatal movement.

Moreover, the poor physical connection between the numerousstomatal areas (where evaporation may take place) and themesophyll tissue observed in the cassava leaf (El-Sharkawy andCock, 1986) could accelerate water stress in the epidermis andstomatal apparatus, thus leading to the striking sensitivityto changes in atmospheric humidity without noticeabledecreases in bulk leaf water potential (Figures 5, 6, 7, and8; also see Cayón et al, 1997; Connor and Palta, 1981; DeTafur et al, 1997a; El-Sharkawy, 1990; El-Sharkawy and Cock,1986; El-Sharkawy et al, 1984d, 1992b; Porto, 1983). Thisconclusion was further substantiated by the closure of stomatain field-grown cassava in response to high wind speed, despitewet soil and high bulk leaf water potential conditions (El-Sharkawy, 1990).

27


Figure 6. Responses of leaf photosynthesis to changes in airhumidity.

Plants of cv M Col 88 grown in 40 liter pots. The pots wereleft in the open throughout the growing period and plantswere regularly irrigated whenever needed. Pots of unwatered

plants were covered at soil level with plastic covers33 days after planting to exclude rain water. Measurementsof gas exchange were conducted on fully expanded young

attached leaves under controlled laboratory conditions atsaturating photon flux density and normal air using

differential multi-channel open end infra red gas analyser. Source: El-Sharkawy and Cock, 1984.

a

28


b

c

Figure 7. Respnses of: (a) leaf photosynthesis; (b)transpiration; and (c) leaf conductance to water vapour to

stepwise increases in leaf-to-air VPD in cv M Col 90. Growthconditions and gas measurements were as in Figure 6.

Source: El-Sharkawy and Cock, 1984.

29


Bunce (1985) also reported on greater water loss under highwind speed from the outer surface of the epidermis ofherbaceous species, providing further evidence in support ofperistomatal transpiration.

Figure 8. (a) Responses of leaf photosynthesis to changes inair humidity in field-grown cassava (cv M Col 1684) with andwithout misting using high pressure misters installed in the

misted plot (about 1000m2) at 5 x 5m distances. Furrowirrigation was applied weekly to both crops to keep the soil

wet throughout the trial period. The misted plot (mistedfrom 1000–1500h daily) was guarded by two rows of elephantgrass as wind barriers. Gas exchange was conducted by usingthe syringe method to withdraw air samples from the leafchamber enclosing upper canopy fully expanded attached

leaves exposed to sun radiation greater than1,000µ mol photons m−2 s−1, the CO2 concentration in samples

was determined by using the same gas analyser as in Figure 6but in a closed system. The gas analyser was periodicallycalibrated using a series of standard CO2 cylinders with arange of concentrations. Sources: Cock et al, 1985; El-

Sharkawy and Cock, 1986. (b) Oven-dried storage root yieldin cv M Col 1684 at periodical harvests after 3, 6 and 9

30


weeks of misting. Ages of plants at harvests were 65, 85 and105 days, respectively. The differences in yield between themisted and control crops were significant at all harvests(p < 0.01). Top biomass and LAI were not different betweenthe two crops, while total biomass was significantly largerafter 6 and 9 weeks of misting. Sources: Cock et al, 1965;El-Sharkawy and Cock, 1986. (c) Response of leaf WUE to VPDin field-grown cassava in a mid-altitude, warm sub-humidclimate. Measurements of gas exchange in upper canopyattached leaves were always made between 0900 and 1300h

local time, when solar irradiance always exceeded1,000µ mol photons m−2 s−1, as measured using a portable

infrared gas analyser. VPD levels progressively increasedfrom morning to midday. 33 clones were evaluated and weregrouped into humid, sub-humid/seasonally-dry and semi-arid

habitats. Sensitivity to VPD increased from the humid to thesemi-arid habitat. Differences between plant groups

illustrate the genetic diversity within cassava germplasm inresponse to changes in atmospheric humidity. Sources: El-Sharkawy, 2004; El-Sharkawy, Amézquita, Ramirez and Lema,

unpublished observations.

BREEDING STRATEGY AT CIAT FOR DROUGHT TOLERANT CASSAVA CULTIVARS

Introduction, Background and Rational

There was some limited early work by western colonialcommunities in parts of Africa, Asia and Latin America during

the first half of the 20th century (Cock, 1985; Cours, 1951;Hunt et al, 1977; James, 1959; Nijholt, 1935; Verteuil, 1917,1918). However, despite its potential productivity, cassavahas received little attention from either policy makers orresearchers in developing countries where it is widely grown.Although cassava is the most important carbohydrate foodsource after rice, sugarcane and maize for over 500 millionpeople in developing countries within the tropical andsubtropical belt, the crop was overlooked by the so-called‘Green Revolution’. This early effort by the international

31


agricultural research centres, CIMMYT at Mexico and IRRI atPhilippines, in the 1960s focused on improvement of the maincereal crops such as wheat, rice and maize, with the help ofinternational agricultural development and research agenciessupported by few western donors.

For this reason, the Consultative Group on InternationalAgricultural Research (CGIAR) that was established in 1971under the sponsorship of the World Bank, the United NationsDevelopment Programme (UNDP), and the Food and AgricultureOrganization of the United Nations (FAO; Wortman,1981), gavehigh priority to research on other crops including cassava, aswell as on production ecosystems in the humid tropics ofAfrica and South America. The work was conducted in Africathrough the International Institute of Tropical Agriculture(IITA), located in Nigeria, and in South America through theCentro Internacional de Agricultura Tropical (CIAT) located inColombia. Given the financial support that became available,core teams of international multidisciplinary scientists wereable, for the first time, to conduct extensive research oncassava, in collaboration with the few existing nationalresearch programmes. They achieved improvements in germplasmcollecting and characterization, breeding, agronomy andcropping systems management, pests and diseases, andutilisation of the crop, based on a better understanding ofthe physiological processes involved. Recent publications(Hillocks et al, 2002; Kawano, 2003) review results on themany aspects of cassava research in Africa, Asia and LatinAmerica over the last three decades.

The multidisciplinary cassava programme at CIAT wasestablished in the early 1970s, with a global mandate forcassava. The programme centred its research strategy oncollecting, conserving, and characterizing the germplasmavailable world-wide that originated mainly in Latin America,and on selecting and breeding more broadly-adapted germplasmfor the various environments prevailing in the tropics andsubtropics in both Latin America and Asia. In the earlystages, breeding objectives were directed toward developinghigh yielding cultivars under favorable conditions in theabsence of biotic and abiotic stresses (Cock et al, 1979;

32


Kawano et al, 1978). This strategy was based mainly onselection for genotypes with high yield per unit land area (incontrast to traditional vigorous cultivars/landraces suitedfor intercropping), high dry matter content (ie, high starchcontent) in the storage roots, and a higher HI (expressed asroot yield/total plant biomass) than the values of 0.5 or lessfound in most low-yielding traditional varieties and landraces(Kawano, 1990, 2003). This early work showed that cassavagermplasm is genetically diverse with a high potential forproductivity under near optimum environments. Thus, the needto transfer traits from wild relatives (reasonably advocatedeven as recently as 2010 by Nassar and Ortiz) was largelyobviated.

However, since most cassava production occurs inenvironments having various degrees of stress, and with littleor no production inputs by resource-limited small farmers, thegoals of subsequent breeding efforts have centred uponselecting and developing cultivars with reasonable and stableyields, plus the ability to adapt to a wide range of bioticand abiotic stresses (Hershey, 1984; Hershey and Jennings,1992; Hershey et al, 1988; Jennings and Iglesias, 2002; Kawano,2003; Kawano et al, 1998). This strategy was further stimulatedby the inherent capacity of cassava to tolerate adverseenvironments, particularly where other main staple food cropssuch as cereals and grain legumes would fail to produce, andby the opportunity that it offered to reduce or avoid thenegative environmental consequences of adopting high-inputagrochemically-aided production systems (El-Sharkawy, 1993).The strategy took advantage of the wide genetic diversitywithin the more than 6,000 accessions, mostly of LatinAmerican origin, conserved at CIAT Headquarters. It also tookadvantage of the diversity of conditions with high pest anddisease pressures that exist in various ecozones throughoutColombia – seven or eight zones with a wide range of climaticand edaphic conditions that are representative of most cassavaproduction ecosystems in the tropics and subtropics (El-Sharkawy, 1993; Hershey and Jennings, 1992).

33


In the light of this environmentally-sound breedingstrategy, research on cassava physiology has focused oninvestigating both basic and applied aspects of the crop underthe prevailing environments, mainly in the field, to elucidateand understand better the characteristics and mechanismsunderlying productivity and stress tolerance (Cock and El-Sharkawy 1988a,b; El-Sharkawy, 1993, 2004). The breedingobjectives included: (i) characterisation of the coregermplasm for tolerance to extended water shortages, eithernaturally or imposed, and to low-fertility soils; (ii) studyof leaf photosynthetic potential in relation to productivityunder various edaphoclimatic conditions; and (iii)identification of other plant traits that might be of use inbreeding programmes. The multidisciplinary research approachadopted was pivotal in achieving these objectives.

Selection of parental materials for tolerance to waterstress and infertile soils has resulted in breeding improvedgermplasm adapted to both wet and water stress environments. Aset of elite cassava germplasm with drought-tolerantattributes has been selected for detailed phenotypic analysisunder water stress. The International Fund for AgriculturalDevelopment (IFAD, ROME) has funded a long-term project forselection in different semi-arid environments in NortheasternBrazil (where the greatest genetic diversity of cassavagermplasm for adaptation to drought is found, see El-Sharkawy,1993) and distribution of the elite germplasm throughoutAfrica (Fukuda and Saad, 2001). Farmers had participated inevaluating and selecting adapted germplasm that resulted inrapid acceptance and ,consequently, in the release of severalimproved clones (Saad et al., 2005).

Responses of Field-Grown Cassava to Air Humidity and Its Implications for Breeding Strategies in Different Edaphoclimatic Zones and Ecosystems

Cassava stomatal sensitivity to atmospheric humidity wasobserved at two locations in Colombia: in field-grown cassavain wet soils at the mid-altitude CIAT Headquarters station at

34


Palmira, Valle Department, and at the low-altitude CarimaguaICA-CIAT station, Meta Department (Berg et al, 1986; Cock et al1985; El-Sharkawy 1990). Over a range of cultivarsrepresenting the core cassava germplasm from differenthabitats and grown at a mid-altitude CIAT experimental stationat Santander de Quilichao, Cauca Department, Colombia,significant differences in stomatal sensitivity to humiditywere observed among cultivars (Figure 8, El-Sharkawy 2004).Furthermore, total biomass and storage root yield were greaterin high humidity environments enhanced by misting thatresulted in higher leaf photosynthesis, indicating thatstomatal sensitivity to changes in VPD was translated at thecanopy level (Figure 8, Cock et al 1985; El-Sharkawy and Cock1986).

Recent research on whole-plant water relations of field-grown cassava under prolonged natural water deficit in Ghana,West Africa, showed that both canopy conductance andtranspiration declined with increasing VPD (Oguntunde 2005).These findings have important practical implications forcassava breeding and improvement for different ecosystems andedaphoclimatic zones. In wet/humid zones such as the Amazonianbasin, equatorial west Africa, west Java in Indonesia, and inzones with short intermittent water deficits, less sensitivecultivars (with a lower stomatal density on the abaxialsurface of hypostomatous leaves and/or with amphistomatousleaves with equal total conductances) should be bred for andselected in order to maximise productivity, since optimisingWUE is not of importance in this situation (El-Sharkawy, 2004;El-Sharkawy and Cock, 1986)( more information on ontogenesisof leaves and the impact of stomatal density, size and patternof distributions on both leaf sides, in terms ofphotosynthesis as well as the comparative adaptive advantagesof amphistomatic versus hypostomatic characteristics can befound in: Gutschick, 1984; Mott et al, 1982; Parkhurst, 1978;Pospisilova and Solarova, 1980; Tichá, 1982).

On the other hand, in subhumid/seasonally dry and semi-aridzones where there are prolonged periods of water deficit (morethan three months), it is advantageous to breed and select for

35


more sensitive cultivars in order to conserve the limited soilwater and deplete it slowly, thus optimising WUE rather thanmaximising productivity, over a longer period during thegrowth cycle. In this case weed control must be practiced toavoid competition for water. Also, plant residual mulch, ifavailable, would lead to better water conservation for cropuse (Cadavid et al., 1998).

Since new leaf formation is very restricted under prolongeddrought (Connor and Cock, 1981; El-Sharkawy and Cock, 1987b;El-Sharkawy et al, 1992b; Porto, 1983), higher degrees ofstomatal sensitivity should be combined with greater leafretention, ie, longer leaf life and duration (El-Sharkawy,1993, 2004). Recently, leaf retention was found to bepositively correlated, over a wide range of cultivars andbreeding lines, with productivity under naturally extendedwater deficits (Lenis, et al 2006). Moreover, it had beenreported that leaves of plants subjected to prolonged imposedwater stress (more than two months) in the field in subhumidzones had 40 percent of the net photosynthesis of well-wateredplants and were capable of recovering completely aftertermination of the stress (CIAT, 1987, 1988, 1989,1990,1991,1992,1993, 1994; El-Sharkawy, 1993). Selection for longer leaflifespan is advantageous in saving dry matter already investedin leaf canopy formation (Chabot and Hicks, 1982), resultingin more assimilates being diverted toward storage roots, andleading to a higher HI and harvestable yield (Cock and El-Sharkawy, 1988a; El-Sharkawy, 1993).

De Tafur et al (1997b) reported a wide variation in net leafphotosynthesis among rain-fed cassava, as measured in thefield during the driest months in a seasonally dry zone (Pn

ranged from 27 to 31µmol CO2 m−2 s−1) and in a semi-arid zone (Pn

ranged from 7 to 20 µmol CO2 m−2 s−1). Significant differenceswere observed among cultivars that could be exploited inbreeding improved genotypes. In this case, host-planttolerance/resistance for pests and diseases must beincorporated into cultivars targeted to seasonally dry andsemi-arid zones in order to maintain functioning leaf canopyas much as possible over extended periods of time (Bellotti,2002; Byrne et al, 1982; Calvert and Thresh, 2002; Hershey and

36


Jennings, 1992; Hillocks and Wydra, 2002). There is also awide genetic diversity in stomatal density within cassavagermplasm, with a small percentage of the genotypes possessingamphistomatous leaves that may be used in breeding programmes.Thus, several accessions have been identified with asignificant number of stomata on the upper surface, but theseare less than 5 percent of more than 1,500 landraces andcultivars that were screened in the field. Screening was doneusing the transient porometer technique and microscopicobservation on replicas of leaf surfaces made by sprayingleaves with a collodion solution (El-Sharkawy et al, 1984a;1985; Guzman, 1989). Both porometry (Kirkham 2005) and leafsurface replicas combined with microscopic observation areeasy to handle in screening large amounts of breeding materialin the field for stomatal characterisation, although the leafreplica method has some limitations in the case of hairyleaves and sunken stomata (North, 1956; Slávik, 1971). Theleaf surface replica method was effective using young tissue-cultured seedlings (El-Sharkawy et al, 1984a). This mayfacilitate early screening of large populations. Zelitch(1962) described a similar technique using silicon rubbercombined with a cellulose acetate solution to obtain stomatalimpressions.

Screening Cassava Germplasm for Leaf Photosynthesis

Having pointed out the importance of field research and theneed to assess cassava potential photosynthesis underrepresentative environments, we studied photosynthesis ofrecently matured upper canopy leaves in groups of cultivars,landraces and improved CIAT breeding material grown in threesites used by the cassava breeding programme for evaluation ofgenetic performance. The objective was to identify cultivarsand lines with high photosynthetic potential in the field tobe used as parental materials in crosses and breedingprocesses for improved productivity (El-Sharkawy, 1993), incombination with the other main breeding objectives of yieldstability, broad-adaptation and tolerance/resistance to

37


edaphoclimatic stresses, pests and diseases (Hershey andJennings, 1992; Jennings and Iglesias, 2002). This objectivewas warranted, since our previous research in differentlocations in subhumid, seasonally dry and semi-aridenvironments showed a significant correlation, across a widerange of core germplasm and edaphoclimatic conditions, betweenupper canopy leaf photosynthesis – as measured in the fieldwith portable infrared gas analysers – and total biomass andstorage root yields (Figure 9; CIAT, 1987-1995; De Tafur,2002; De Tafur et al, 1997b; El-Sharkawy, 2004; El-Sharkawy andCock, 1990; El-Sharkawy et al, 1990, 1993; Pellet and El-Sharkawy, 1993a).

5 10 15 20 25 30 35 400.0

0.5

1.0

1.5

2.0

f(x) = 0.0622917018759506 x − 0.544540307588304R² = 0.729350482909918

Pn (µmol CO2 per m2/s)

Dry root yield (kg/m2)

A Santander de Qulichao

Santo Tomás

Riohacha

38


100 150 200 250 300 350 4000.0

0.5

1.0

1.5

2.0

f(x) = − 0.00958136542988349 x + 3.03112563239288R² = 0.811969741646728

Internal CO2 (µmol/mol)

Dry

root

yie

ld (

kg/m

2)

Santander de Qulichao

Santo Tomás

B

Riohacha

Figure 9. Relationship between dry root yield and uppercanopy leaf photosynthesis (A) and intercellular CO2 (B) for

groups of cultivars grown in Santander de Quilichao(subhumid), Santo Tomas (seasonally dry) and Riohacha (semi-arid). Sources: El-Sharkawy,2006; De Tafur, 2002; De Tafurand El-Sharkawy, unpublished observations; De Tafur et al,

1997b; El-Sharkawy et al, 1993.

Tables 6, 7 and 8 present data on upper canopy leafphotosynthesis measured in the high-altitude cool climate (atCajibio, Cauca Department, Colombia, elevation ca 1,800m, meanannual temperature ca 19°C) and the mid-altitude warm climate(at the CIAT Quilichao experiment station, Cauca Department,and at CIAT Headquarters, Palmira,Valle Department, withelevations about 965–1,000m, and a mean annual temperature ofca 24°C). Crops were grown under rain-fed conditions withminimum fertilizer applications. Measurements were made onseveral occasions, mainly during dry periods, and thenaveraged. Chambers enclosing whole or part of central leaflobes were always directed toward the sun and at photon fluxdensities greater than 1,000µmol m−2 s−1 between 0900 and1200h local time on four- to six-month-old plants, when theleaf canopy was nearly closing up (high leaf capacity source)and storage root bulking was at its highest rates (high rootsink demand).

39


In all locations, the average leaf photosynthesis variedsignificantly among screened cultivars and landraces, withrates greatly reduced at the high-altitude cool climate,confirming results and patterns observed with potted cassava(compare data of Tables 6, 7 , 8 and Figure 11). Theaccessions evaluated in the high-altitude cool climate wereall local traditional cultivars or landraces from cool climateregions collected from several countries and included improvedCIAT materials bred and selected for better adaptation to thisclimate. Compared to the overall mean photosynthetic rate(12.3µmol CO2 m−2 s−1), the few higher ranking materials withrates from 15.7–17.3µmol CO2 m−2 s−1 were four CIAT improvedclones and a Peruvian cultivar (M Per 501) as shown in Table6. These findings indicate the narrow genetic base for thisecosystem. They also confirm the relative effectiveness of thebreeding strategy adopted by the cassava programme at CIAT forspecific edaphoclimatic zones and ecosystems as discussedabove, and point to the importance of including leafphotosynthesis as a selection criterion in parental materialsfor enhancing productivity (El-Sharkawy, 2004; El-Sharkawy andCock, 1990; El-Sharkawy et al, 1990).

Table 6. Leaf net photosynthesis (Pn; µmol CO2 m−2 s−1), stomatalconductance (gs; mmol m−2 s−1) and internal CO2 (Ci ;

µmol CO2 mol−1) for some selected cassava clones with relativelyhigh photosynthetic capacity. Plants were grown in 1992 and1993 on a private farm at Cajibio, Cauca Department, Colombia(altitude 1,800m; cool subhumid climate). Measurements weremade with portable infrared CO2 analysers on recently matured

upper canopy leaves of 4–6-month-old plants. Note the higher Pn

rates and the lower values of stomatal conductance and ofinternal CO2 in this group of clones, as compared with themeans of the trial. This indicates the importance of non-

stomatal (ie, biochemical/anatomical) factors in selection forenhanced photosynthetic capacity. There is a need to improve

the genetic base for the cooler ecosystems in the highaltitude tropics and in the subtropics where cassava is grown.

Sources: Cassava Physiology Section database; CIAT, 1994

Selected clones Pn Stomatal Internal CO2

40


conductance (gs) (Ci)SM 1061-1 17.3 196 98SM 526-12 16.7 320 154SM 1054-4 16.6 225 114M Per 501 16.4 391 166SM 1053-9 15.7 225 122Mean 16.5 271 131Mean of all accessions (n=107)

12.3 312 183

LSD 5% 1.3 32 14

The enhanced photosynthesis in the few superior clones (Pn

was 134% of overall mean of all accessions) could not beattributed to stomatal control, since their average stomatalconductance (with 271 mmol m−2 s−1) was significantly lower thanthe overall mean of all accessions (with 312 mmol m-2 s-1)(Table 6). However, the intercellular CO2 concentration wasgreatly reduced in these clones (Ci was 71% of the overall meanof all accessions), indicating possible control by non-stomatal factors such as leaf anatomy and biochemistry (eg,enzyme activity). Since the rate of leaf formation is muchslower in a high-altitude cool climate but leaf life is muchlonger compared to warm climate conditions (Irikura et al,1979), selection for enhanced photosynthesis and tolerance tolow temperatures becomes even more important.

Table 7. Leaf net photosynthesis (Pn) (µmol CO2 m−-2 s−1) inupper canopy leaves of the cassava core collection grown atSantander de Quilichao in 1993–1994. Measurements were madewith a portable infrared gas analyser from 5–6 months afterplanting. Values are means of 7–11 measurements made duringthe dry period. These higher values of Pn obtained in a warm

subhumid habitat can be compared with those obtained in a coolsubhumid habitat shown in Table 6.The cultivar M Mal 48 from

Malaysia had the highest Pn rate and the highest dry root yieldin this trial.

Sources: Cassava Physiology Section database; CIAT, 1994

Clone Pn Clone Pn

41


M Mal 48 27.6 M Tai 1 24.4M Bra 900 27.6 M Pan 51 24.3M Bra 12 26.8 M Bra 383 24.2M Bra 191 26.7 M Ind 33 24.1M Mal 2 26.4 CM 849-1 23.6HMC-1 26.0 M Col 1684 23.4MCol 1468 25.8 M Mex 59 23.2MCol 2061 25.4 M Ven 25 23.2M Gua 44 25.4 M Bra 885 23.1M Chn 1 25.3 M Cub 51 22.8M Col 22 25.1 M Col 2215 22.3M Arg 13 25.0 M Cub 74 22.3M Ven 45A 24.8 M Per 205 22.0M Col 1505 24.8 M Ptr 19 21.3M Bra 110 24.6 M Ecu 82 21.0LSD (5%) 4.8

In the mid-altitude warm climate sites, averagephotosynthesis rates were much greater than in the coolclimate, particularly at the CIAT Headquarters location(Tables 7 and 8).The measurements were all made during the dryperiod. Thus, they were lower than the maximum rates observedin wet conditions (see Table 9). The majority of the materialsevaluated at CIAT Headquarters were a collection of cultivarsand landraces from Brazil, plus eight accessions fromArgentina and one each from Colombia (HMC-1) and Bolivia(M Bol 1). The mean rate of photosynthesis was significantlygreater in the few accessions from Argentina(26µmol CO2 m−2 s−1) compared to the germplasm from Brazil(Table 8).This was due to the high number of Brazilianaccessions with rates lower than their origin overall mean of22µ mol CO2 m−2 s−1. Nevertheless, there were several Brazilianaccessions within the highest photosynthesis range,particularly M Br 12 (also see Figure 11B) and M Br 110, thatcould be used in crossing and breeding for warm climateecosystems.

Since the accessions from Argentina are, presumably, moreadapted to subtropical ecosystems than the warm climategermplasm from tropical ecosystems and have some tolerance to

42


low winter temperatures, they could be used in crossing andbreeding for enhancing photosynthesis in high-altitude coolclimate germplasm. In this group of clones, Pn was highlynegatively correlated with intercellular CO2 (r2 =- 0.97, P <0.0001; regression: intercellular CO2 = 315 - 7.83 Pn, Figure10 ), indicating that differences in Pn were caused by non-stomatal factors, that is, anatomical and/or biochemicalfactors such as enzyme activity and leaf anatomy (El-Sharkawyet al. 1990, 2008; de Tafur et al. 1997b; El-Sharkawy 2006,2010).

The accessions screened at Quilichao were a mix of cultivarsand landraces from Latin America, which were the majority, andsome from Asia (Table 7). Again average photosynthesis ratesvaried widely among cultivars, with several high-rankingaccessions from Brazil, Colombia and Malaysia. The highestranking accession from Malaysia, M Mal 48, also had thehighest dry root yield (15.6t ha−1) compared with the overallmean of the trial (10.6 tha−1). This clone had already beenused in crossing and breeding at CIAT.

10 15 20 25 30 35

0

50

100

150

200

250

f(x) = − 7.82928418505073 x + 315.401191473518R² = 0.899652163132543

PN (µmol CO2 m-2 s-1)

Intercellular CO2 (µ mol mol-1)

Figure 10. Relationships between Pn and intercellular CO2

concentration (Ci) in 53 cassava accessions (data of Table8). Note the negative correlation between Pn and Ci, whichindicates that the association was caused by non-stomatalfactors (i.e., biochemical and/or anatomical mesophyll

43


traits) (SM de Tafur and MA El-Sharkawy 1995, unpublished).

Nevertheless, during rainy period maximum photosyntheticrates of several cultivars of field-grown cassava were morethan 40 µmol CO2 m-2 s-1, with a mean Ci /Ca ratio of 0.42 (Table9). These values are comparable with those observed in C4

species and much less than those obtained in C3 species.

Table 8. Leaf net photosynthesis (Pn) in µmol CO2 m−2 s−1 ofupper canopy leaves and intercellular CO2 (Ci) (µmol CO2 mol−1)

for 53 accessions of the core collection grown at CIATHeadquarters in 1991–1992. Measurements were made with

portable infrared CO2 analysers during dry periods in four-month-old plants. These higher Pn rates in warm subhumid

habitat can be compared with rates obtained in a cool subhumidhabitat as shown in Table 6. Note that few accessions from

Argentina and Brazil have relatively high Pn rates as comparedto the trial mean.

(Cassava Physiology Section database; CIAT, 1992.)

Accessi

onPn

Intercellular

CO2 (Ci)

Accessi

onPn

Intercellular

CO2 (Ci)M Arg 1 32 73 M Bra 2 22 143M Bra 1 30 82 M Bra 2 22 128M Bra 1 30 74 M Bra 7 22 145HMC-1 29 87 M Bra 2 22 144M Arg 2 28 95 M Arg 1 22 146M Bra 1 28 88 M Bra 4 22 151M Bra 1 27 83 M Arg 1 22 139M Arg 1 27 105 M Bra 3 22 156M Bra 3 27 127 M Bra 1 21 145M Bra 7 26 111 M Bra 3 21 162M Arg 7 26 119 M Bol 1 21 147M Bra 8 26 112 M Bra 3 21 148M Arg 9 26 110 M Bra 4 21 159M Bra 1 26 97 M Bra 4 21 169M Bra 1 26 100 M Bra 3 20 159M Bra 4 25 131 M Bra 4 20 173M Bra 1 25 108 M Bra 3 19 177M Arg 5 25 115 M Bra 1 19 137M Bra 2 24 133 M Bra 3 18 169

44


M Bra 2 24 133 M Bra 2 17 173M Bra 1 24 114 M Bra 3 17 195M Bra 2 23 132 M Bra 4 17 196M Bra 4 23 143 M Bra 3 17 182M Bra 7 23 134 M Bra 3 16 188M Bra 2 23 140 M Bra 3 16 191M Bra 4 23 151 M Bra 3 14 187M Bra 1 23 129LSD 5% 6.2 23

45


Figure 11 A and B. Responses in cassava of netphotosynthetic rate (Pn) to leaf temperature for: (A) cv

M Col 2059; habitat: cool humid; (B) cv M Bra 12; habitat;hot humid. ∆ = leaves developed in a cool climate;

● = leaves developed in a cool climate and then acclimatedfor one week in a warm climate; ๐ = newly developed leavesin a warm climate of the same plants. The apparent upwardshift in optimum temperature from cool to warm-acclimatedand warm climate leaves reflects the adaptation to warm

climate in both cultivars. Also note: (i) the lack of lightsaturation (11C) in warm climate leaves as compared to cooland warm- acclimated leaves indicating the high capacity forCO2 fixation; (ii) the higher maximum photosynthetic ratesin all sets of leaves of cv MBr.12 (11B)from hot-humidhabitat compared to the cool-climate cv M Col 2059(9A).

Sources: CIAT, 1992; El-Sharkawy et al, 1993; also see El-Sharkawy et al, 1992a.

Figure 11C. Respnses in cassava of net photosynthetic rate(Pn) to irradiance (PAR) in cv M Col 2059. ∆ = leaves

developed in a cool climate; ● = leaves developed in a cool

46


climate and then acclimated for one week in a warm climate;๐ = newly developed leaves in a warm climate.Sources: CIAT,1992; El-Sharkawy et al, 1993; also see El-Sharkawy et al,

1992a.

Table 9. Leaf net photosynthesis, Pn, of field-grown cassava atSantander de Quilichao, Cauca Department (warm subhumid)

during the 1990–991 season. Maximum photosynthetic rates wereobtained during wet periods and high air humidity.

Measurements were made on upper canopy leaves using portableinfrared CO2 analysers. The Ci/Ca ratio (intercellular CO2

divided by atmospheric CO2). is commonly used to differentiateplant species based on their photosynthetic capacities; ie,the lower the ratio the higher the capacity. Note the Ci/Cavalues here which are comparable to those in C4 species andmuch lower than those in C3 species, indicating the highphotosynthetic capacity of cassava as expressed in nearoptimum environments. In this group of cultivars, average

seasonal Pn was correlated with final root yield. Sources: Cassava Physiology Section database; El-Sharkawy et

al, 1992a, 1993

Cultivar

Maximum net photosynthesis µmol CO2 m-2 s-1 (n = 6)

Ci/Ca (n = 6)

Seasonal average netphotosynthesis µmol CO2 m-2 s-1 (n = 30)

CG 996-6 49.7 0.37 33.8M Bra 191 47.4 0.37 35.5CM 4864-1 45.1 0.39 34.0CM 4145-4 43.9 0.40 31.7CM 3456-3 43.7 0.43 31.9

Table 9. (Continued)

CultivarMaximum net photosynthesisµmol CO2 m-2 s-1 (n = 6)

Ci/Ca(n = 6)

Seasonal average net photosynthesisµmol CO2 m-2 s-1 (n = 30)CM 507-37 43.7 0.38 28.7

CM 4716-1 43.6 0.42 31.8M Col 1684 43.0 0.42 30.9CM 4575-1 42.8 0.39 33.2

47


CM 4617-1 42.8 0.46 31.4CM 523-7 42.3 0.45 30.1M Col 1468 42.3 0.44 30.3CM 4701-1 42.2 0.45 30.9CM 4711-2 41.3 0.45 30.9CG 927-12 39.3 0.43 26.2Mean of all cultivarsss

43.5 0.42 31.4LSD (0.05) 1.70 0.08 1.80

Evaluation of Cassava Core Germplasm for Leaf Area Duration (Seasonal Average Leaf Area Index) and Productivity in a Mid-Altitude Warm Climate

To complement the joint physiology and breeding efforts incharacterising cassava core germplasm and in theidentification of useful yield-determinant traits, a fieldtrial was conducted at the CIAT mid-altitude warm climateexperimental station at Quilichao where 30 clones wereevaluated for leaf duration over the growth cycle by measuringthe seasonal average LAI using a leaf canopy analyser.

Data on yield, shoot and total biomass, seasonal average LAIand root dry matter content are given in Table 10 (CIAT,1995).

Wide variations among clones were found in standing shootbiomass (top, excluding fallen leaves) and total biomass,yield, dry matter content of roots and seasonal LAI. It isnoteworthy that several accessions from Brazil were among thehighest ranked in terms of yield, total biomass and dry mattercontent in storage roots, thus highlighting the importance ofthe Brazilian germplasm.

Breeding at CIAT, while diversifying the genetic base, hasincorporated many of these accessions for their useful traits.Outstanding among these accessions is the clone M Br 12, withits high leaf photosynthesis in cassava grown both outdoors inpots or in the field in a mid-altitude warm climate (seeFigure 11B and Table 8), and its high yield coupled withresistance to mites (Byrne et al, 1982).

48


Other accessions of Brazilian origin, M Br 383 and M Br 191,that ranked high in this group of clones, were also reportedto be among the highest ranked clones (fourth and fifth,respectively, among 33 evaluated) for tolerance to soils lowin phosphorus (CIAT, 1990; El-Sharkawy, 2004).

Table 10. Seasonal average LAI, dry root yield, top and totalbiomass, and root dry matter content of 30 clones from thecassava core collection. Plants were grown at Santander deQuilichao in 1994–1995. Leaf area duration, as estimated byseasonal average LAI, was significantly correlated with rootyield (see Figure 12), indicating the importance of this traitin breeding and selection for improved cultivars. Sources:

Breeding and Physiology Sections database, CIAT,1996

ClonesSeasonal averageLAI m2 m-2

Dry top biomasst ha-1

Dryroot

Total biomass

Root dry matter%

M Bra 383 1.3 6.0 15.5 21.5 41.7M Bra 12 1.0 5.3 15.3 20.6 38.2M Pan 51 1.8 10.2 14.7 23.9 40.8CM 849-1 1.4 6.3 14.1 20.4 41.7M Bra 191 1.5 5.7 14.0 19.7 41.3M Mal 48 1.9 4.2 13.9 18.1 41.0M Bra 885 1.6 5.4 13.8 19.2 41.6M Ven 25 1.1 4.9 12.6 17.5 40.0HMC-1 1.6 4.8 12.2 17.0 38.5M Ind 33 1.6 5.9 11.6 17.5 36.6M Bra 100 1.9 6.4 11.3 17.7 40.6M Gua 44 1.2 4.6 11.2 15.8 38.9M Cub 74 0.9 3.9 10.8 14.7 39.8M Tai 1 1.2 5.6 10.6 16.2 37.5M Mex 59 1.6 6.8 10.3 17.1 40.7N Arg 13 0.9 2.4 9.3 11.7 39.1M Mal 2 1.8 6.9 8.4 15.3 36.2M CHN 1 1.0 1.9 8.0 9.9 36.2M Col 22 1.4 1.7 7.8 9.5 37.8M Ven 45A 1.0 5.1 7.7 12.8 37.4M Col 1684 0.8 2.2 7.0 9.2 34.6M Ecu 82 0.8 3.4 6.7 10.1 38.6M Ptr 19 1.1 4.0 6.1 10.1 40.0M Col 2215 0.7 2.4 5.9 8.3 40.3

49


M Col 1468 0.9 1.9 5.6 7.5 36.7M Col 2061 0.9 3.5 5.3 8.8 30.7M Per 205 1.0 3.8 5.3 9.1 38.7M Col 1505 0.7 2.1 5.1 7.2 40.6M Cub 51 0.7 3.1 4.9 8.0 39.9M Bra 900 0.9 1.3 4.7 6.0 31.4Mean of all clones 1.2 4.4 9.7 14.0 39.6LSD 5% 0.5 2.0 3.5 4.6 3.6

In this group of accessions, standing shoot biomasscorrelated with root yield (r = 0.70; p < 0.001), confirmingprevious findings that suggest using this trait as a proxy forleaf area formation and duration when evaluating largebreeding populations (CIAT, 1990; El-Sharkawy, 2004; El-Sharkawy et al, 1990).

LAI0 1 2

Dry root yield (t ha-

1 )

4

6

8

10

12

14

16

18

y=2.34 + 6.07xr=0.65 (p=0.001)

Figure 12. The relationship between final dry root yield andseasonal average LAI in 30 clones from the core cassava

germplasm collection at CIAT. Crops were grown at the CIATQuilichao station with a mid-altitude warm climate. Leafarea was determined throughout the growth period using a

leaf canopy analyser. The significant correlation indicatesthe importance of leaf area duration for yield formation.Due to the small leaf area canopy in the first 1–3 monthsand in the final 8–12 months, the seasonal average canopyarea still limits yield and indicates the need to breed andselect for higher and more sustainable canopy during most of

50


the growth cycle, combined with enhanced leafphotosynthesis, high HI and a strong root sink (a higherstorage root number per plant). It is noteworthy that cv

M Br 12 had a high yield with an LAI lower than the overallaverage of the trial, indicating its high leaf

photosynthetic potential (also see Figure 11B). Source:CIAT, 1995.

Also, as shown in Figure 12, dry root yield correlated withseasonal LAI in this group of clones (r = 0.65, p < 0.001). Thisfurther substantiates earlier reports (Pellet and El-Sharkawy,1993a) and supports the concept of breeding for longer leaflife and optimum leaf area duration, for maximisingproductivity under favorable conditions as well as forsustainable yields in stressful environments (Cock and El-Sharkawy, 1988a,b; El-Sharkawy, 1993, 2004; El-Sharkawy andCock, 1987b; El-Sharkawy et al, 1992b; Lenis et al, 2006).

In conclusion, the use of leaf photosynthesis as a selectioncriterion in cassava improvement programs might be difficultto handle when evaluating large breeding populations. Despitethis, it should be included at least in the processes toevaluate and select parental materials, in combination withother important yield-related traits, particularly relativelyhigh HI (> 0.5; Kawano, 1990, 2003), large root sink usingroot number per plant as a criterion (Cock et al, 1979; Pelletand El-Sharkawy, 1993a,1994), and longer leaf life, ie,greater leaf retention and duration over the growth cycle(Cock and El-Sharkawy, 1988a,b; El-Sharkawy, 1993, 2004; El-Sharkawy and Cock, 1987b; El-Sharkawy et al, 1992b; Lenis etal, 2006). Recent advances in the area of molecular biology andin the development of more precise techniques andequipment,will further enhance and speed up elucidation of thefundamental mechanisms underlying photosynthetic potential andassociated beneficial traits and their controlling genes(Daniell et al., 2008; Raines 2006,2011).

51


Evaluation of Germplasm under Mid-Season Water Stress in a Field Drainage Lysimeter

Sixteen cultivars from the cassava core germplasm collectionwere evaluated over a number of years in a field drainagelysimeter under three months of water stress initiated 90–100 days after planting (ie, mid-season stress). Figure 13illustrates dry root yield accumulation patterns for fourrepresentative accessions as affected by stress during thegrowth cycle.

Months after planting

Figure 13. Dry root yield in a group of clones as affectedby a three-month water stress period initiated 90 days after

planting (ie, mid-season stress). The yield wassignificantly lower at the end of stress, but recovered

rapidly with watering and the final yields approached thoseof the controls. There were differences among cultivars with

CM 489-1 having the highest yield in both water regimes(also see Table 11). It is noteworthy that CM 489-1 had highleaf photosynthesis with the least reduction under stress

52


(see Figures 3 and 14) and high PEPC activities in leaves offield-grown crops under extended water stress. Sources:

CIAT, 1992; El-Sharkawy, 2004.

Water stress significantly reduced yield in all accessionsat the end of stress, as well as reducing shoot biomass (CIAT,1991, 1992; El-Sharkawy et al, 1992b). However, after recoveryfrom stress, final yields were equal to those of well-wateredplants in some accessions, while reduced in others (see Table11; El-Sharkawy, 1993).

There were also significant differences among cultivars infinal root yield, with the hybrid CM 489-1 having the highestyield under both stress and non-stress conditions (18t ha-1

and19t ha-1 respectively of oven dry roots). It is noteworthyto report here that CM 489-1 also showed high PEPC enzymeactivity in leaf extracts under extended field watershortages. This correlated with leaf photosynthesis across agroup of cultivars (El-Sharkawy, 2004), high values of yield,leaf photosynthesis, NUE in terms of root production,radiation-use efficiency (RUE) in terms of total biomassproduction, and a large number of harvestable storage rootsper plant across a range of phosphorus fertilizer levels inacidic soils in a subhumid warm-climate (Pellet and El-Sharkawy 1993a,b, 1994, 1997). Across accessions, reductionswere much greater in shoot biomass (28 percent) compared toroots (9 percent), with about 6 percent increases in HI,indicating the potential of cassava to tolerate prolonged mid-season stress in subhumid zones. It also indicates its abilityto recover and compensate for possible losses in productivity,giving it an advantage over other staple food crops (CIAT,1991, 1992; El-Sharkawy and Cock 1987b; El-Sharkawy et al1992b,). There is genetic variability in tolerance to stressthat should be exploited in breeding and improvement ofcassava germplasm for dry environments (CIAT, 1991, 1995; El-Sharkawy, 1993; Hershey and Jennings, 1992).

Table 11. Root yield and top biomass, and hydrogen cyanide(HCN) content in roots at final harvest (11 months) as

affected by three months of mid-season water stress commencing

53


90–100 days after planting. Data are the average of the 1987–1989 seasons at Santander de Quilichao. Note the increase inHCN content due to stress and the differences among cultivars.Clones with lower HCN under stress are good genetic sourcesfor breeding and selection for suitable materials for freshconsumption by humans, particularly in dry and semi-arid

zones. Sources: Cassava Physiology Section database; CIAT, 1991; El-

Sharkawy, 1993

Clone

Unstressed StressedBiomass(dry t ha−1) Total HCN

(mg kg−1

dry root)

Biomass(dry t ha−1)

Total HCN(mg kg−1

dry root)

Roots Tops Roots Tops

CM 489-1 19.1 7.2 214 18.0 7.1 401CM 922-2 14.8 7.6 142 15.0 5.9 190CM 1335-4 18.1 7.8 107 16.5 5.1 123CM 2136-2 19.3 12.4 166 15.5 7.3 338Average 17.8 8.8 157 16.2 6.4 263% change due to stress

−9 −28 +68

Most cassava cultivars show increases in hydrogen cyanide(HCN) content – as an indicator of cyanogenic potential – intheir storage roots when exposed to extended water deficits,thereby becoming less suitable for human consumption if notproperly processed to remove most, if not all, HCN (Dufour,1988; Essers, 1995; Rosling,1994). Some crop managementpractices, such as applying moderate amounts of NPKfertilizers and/or plant residues as mulch to infertile sandysoils in zones with long dry periods (Cadavid, et al 1998), orapplying potassium to clayey acidic soils low in potassium insubhumid zones (El-Sharkawy and Cadavid, 2000), will greatlyreduce HCN in cassava roots. However, selection for low HCNcultivars remains a main objective in most breedingprogrammes, particularly for germplasm targeted to stressfulenvironments (El-Sharkawy, 1993). In this case, theidentification of less sensitive and low HCN genotypes as

54


shown here (Table 11) offers a good genetic source forbreeding sweet cultivars. Nassar (1986, 2000) has alsoreported some wild species with low HCN and high protein intheir storage roots. Such wild species should be used asgenetic sources in future research. Acyanogenic (cynogen-free)line of cassava was recently genetically engineered (Siritungaand Sayre, 2003) and is currently under field evaluations.Also, transgenic plants of cultivar MCol 22 with a 92%reduction in cyanogenic glucoside content in storage roots andwith acyanogenic leaves were successfully produced (Jørgensenet al., 2005), which might be used either directly (afteragronomic evaluations in the field) or in crosses with highyielding and drought-tolerant cultivars such as MCol 1468(also named CMC 40) (Figure, 15) and CM 489-1(Table 11). Thecultivar MCol 22 was previously reported to be less droughttolerant (Connor et al., 1981; El-Sharkawy and Cock, 1987b).

Despite these reports, others (Pereira, 1977; Poulton, 1990)argue that high levels of HCN in plants may play a role as adefensive mechanism in protecting crops against predators andherbivores or serves as a source of stored nitrogen,particularly in seeds. However, a putative defensive roleascribed to HCN has not been reflected in the incidence ofcassava pests and diseases (Brekelbaum et al., 1978). Forexample, field observations in Northeastern Brazil andnorthern Colombia, where cassava crops experience severalmonths of water shortage, showed higher mite infestationsunder water stress when leaf HCN is normally elevated in mostcultivars, compared to lesser degrees of infestation inunstressed crops (El-Sharkawy, unpublished observations).Similarly, thrips was found to feed on cassava regardless ofleaf HCN levels (van Schoonhoven, 1978).

Other pests with different feeding habits, whether on shootor on root, may present different responses. Work at CIAT(Bellotti, 2002; Bellotti and Arias, 1993; Bellotti and Riis,1994; Bellotti et al, 1988) showed that the root-burrowingbug, Cyrtomenus bergi, preferred feeding on cassava roots low inHCN as compared to bitter cassava, particularly in wet soils,although several sweet cultivars were noted as having

55


potential resistance/tolerance to the bug (Riis, 1997). Onemechanism that may reduce attack or deter the bug from feedingon sweet cassava is a high HCN content in the storage rootpeel compared to the parenchyma tissue (Riis, 1997). Since thefeeding habit of the bug’s first two nymphal instars withshort stylets is confined mainly to the root peel (Riis, 1990;Riis et al, 1995), selection for sweet cultivars having highHCN in thicker root peel might be advantageous. Culturalpractices such as intercropping cassava with the sunn-hempCrotalaria sp, which possesses natural insecticidal substances,were found to effectively reduce bug attack and damage tocassava roots, although cassava yield was reduced due tocompetition and land occupation by Crotalaria (Bellotti et al.1988; Bellotti 2002).

In a recent study conducted in the northwestern Amazonianbasin in Brazil with the native Tukanoan Indians, whosesubsistence depends more on cultivating bitter cultivars highin HCN, no consistent relationship was demonstrated betweenthe social preferences of cultivating bitter cultivars versussweet ones and resistance to predators, particularly pests anddiseases (Wilson, 2003).

56


Figure 14. Leaf photosynthesis in the upper canopy asaffected by mid-season water stress. Measurements were madeduring the dry period using portable infrared gas analysers.

Values are means of five to eight leaves from differentplants. Note the progressive decreases in photosynthesisover time due to water stress and the recovery after

termination of stress in old leaves, and the consistentlyhigher rates in newly developed leaves in previouslystressed crops as compared to the controls. There were

apparent cultivar differences. Note: the least reductions in

57


Pn of CM 489-1, as compared with other cultivars. Source:CIAT, 1991.

Although dependence on bitter cultivars may be due to theirpredominance – sweet cultivars are less abundant – rather thanto an inherent adaptive advantage, Wilson and Dufour (2002)reported that the higher yield often observed in bittercultivars is the likely criterion for the natives of theAmazonian basin to choose high HCN cassava. However, to ourknowledge there is no conclusive evidence based on soundresearch of an inherent superior potential productivity inbitter cultivars compared to sweet ones.

Data in Table 10 and those reported in 14 other cultivarstested for five consecutive growth cycles under differentrates of application of potassium fertilizer in acidic clayeysoils in the subhumid zone in Colombia (El-Sharkawy andCadavid, 2000), indicated no consistent relationship betweenproductivity and root HCN content.

Moreover, several of the clones tested such as HMC-1, HMC-2,M Cub 74, M Pan 70, M Col 1505, CM 91-3,CM 523-7,CMC 40,CM 1585-13, as well as those shown in Table 10, have highyields and moderate to low HCN levels in the root parenchyma.Most of these clones are improved materials, thus indicatingthe compatibility of selection and breeding for both highyield and low HCN. Therefore, more research is warranted touncover other possible reasons behind the choice of bittercassava in the Amazonian region and elsewhere.

Evaluation of Germplasm for Tolerance to Prolonged Early Water Stress, Mid-Season Stress and Terminal Stress

Three-year field trials were conducted at the CIAT Quilichaoexperimental station to study the effects of prolonged waterstress imposed at different growth stages on cassavaproductivity, nutrient uptake and NUE, leaf photosynthesis andpatterns of water uptake (Caicedo, 1993; CIAT, 1992, 1993; El-Sharkawy and Cadavid, 2002; El-Sharkawy et al 1998b).

58


Figure 15 illustrates the dynamics of dry matteraccumulation in storage roots over the growth cycle of fourcontrasting clones. Under early stress, initiated at twomonths after planting and terminated at six months, root yieldat six months was significantly smaller than the control forall clones in both growth cycles. The same trends wereobserved in shoot biomass but with greater reductions thanobserved in roots (Caicedo, 1993; CIAT, 1992,1993; El-Sharkawyand Cadavid, 2002; El-Sharkawy et al, 1998b).

Under mid-season stress, initiated four months afterplanting and terminated at eight months, yield at eight monthswas also significantly lower compared to the well-wateredcontrol in both cycles except for CMC 40 (or MCol 1468, itsname in Colombia). Reductions in shoot biomass were lesspronounced compared to those under early stress (Caicedo,1993; El-Sharkawy and Cadavid, 2002; El-Sharkawy et al,1998b). Leaf area, as determined from periodical harvests, wasalso significantly smaller in both early and mid-season stresscompared to the controls, resulting in significantly reducedcanopy light interception (Figure 16a, CIAT, 1992; El-Sharkawyand Cadavid, 2002).

After the crop was allowed to recover, new leaf area formedrapidly, with values in early and mid-season stressed cropssimilar to or greater than controls, thereby resulting ingreater light interception (Figure 16a). In the early stressedcrops, increases in shoot biomass were less and remained lowerthan other water regimes, indicating adverse effects of theearly stress on shoot biomass recovery (Caicedo, 1993; El-Sharkawy and Cadavid, 2002; El-Sharkawy et al, 1998b).

59


Figure 15. Storage root dry matter yield (ton ha-1) inresponse to prolonged water stress imposed at different

stages of growth: 2–6early, 4–8 mid-season, 6–12 terminal,months after planting in four cassava cultivars. Crop

cycles: a: first season(left panels), b: second season (rightpanels). ■ control, ○ early stress, midseason stress, ▲

terminal stress. Note the reduction in yields during stress

60


and the recovery at final harvest in early and midseasonstress. There were cultivar differences with cv. CM 40 (MCol 1468) having higher yield under stress (El-Sharkawy and

Cadavid 2002).

61


Figure 16. Photon interception (x102 %) (A–C) and netphotosynthetic rate, Pn(D–F) of cassava crops (four

cultivars) as affected by early (A), midseason (B), andterminal (C) water stress. ● stress, ○ control, ↓ stress

start, ↑ recovery, DAP = days after planting. Note in A thelarge reduction in photon interception in early stress andthe recovery in both early and midseason stresses thatexceeded the control. Greater reduction was found in PN

during terminal stress as compared to early and midseasonstress treatments

(CIAT 1992).

Under terminal stress initiated at 6 months after plantingand remaining until final harvests at12 months, with theexception of CMC 40 whose yield was higher under stress, finalroot yields at 12 months were less than the control, with thelargest reduction in CM 523-7 (or ICA Catumare, its name inColombia). Genotype by water regime interaction wassignificant (p < 0.01), indicating the soundness of thestrategy to breed and select for specific edaphoclimaticzones.

Across clones in both years, final yields were notsignificantly different among water regimes (Table 12),indicating the capacity of cassava to tolerate extended waterdeficits in subhumid and seasonally-dry warm climates withbimodal precipitation patterns. It is noteworthy that cloneCMC 40 had the highest yield and shoot biomass under terminalstress, with the smallest leaf area as compared to CM 523-7.This result could be attributed mainly to high leafphotosynthesis observed in the field under diverseenvironments (El-Sharkawy et al, 1990,1992a; Pellet and El-Sharkawy,1993a). Moreover, upper canopy leaves of CMC 40showed greater activities of both the C3 and C4 main enzymescompared to CM 523-7. Values in µmol mg−1 chlorophyll min−1 were8.2 for Rubisco and 3.1 for PEPC in CMC 40 versus 3.6 and 1.6in CM 523-7 (Table 13, CIAT, 1992; López et al, 1993). Thesefindings point to the importance of selecting and breeding forhigh leaf photosynthesis, particularly under stress.Variations among clones in leaf photosynthesis, as measured inthe field, were observed (see Figure 16 D-F).

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Table 12. Effect of prolonged water stress imposed atdifferent growth stages on storage root yield and shoot

biomass at 12 months after planting, and on mean LAI over thegrowth cycle for four cassava cultivars grown at Santander deQuilichao, in the 1990/91, 1991/92 and 1992/93 seasons. Dataare for the second and third seasons. Note the highest rootyield of cultivar CMC 40 (or MCol 1468) under prolonged

terminal water stress and the highest activities of PEPC andRubisco in the same cultivar as in Table 13. *NS = Notsignificant at 5%. Sources; Cassava Physiology Section

database; Caicedo, 1993; El-Sharkawy and Cadavid, 2002; El-Sharkawy et al, 1998b

Cultivar

Treatment Treatment Treatment

Contro

l

Earl

yst

ress

Mid-

seas

onTerm

inal

stre

ss

Contro

l

Earl

yst

ress

Mid-

Term

inal

stre

ss

Contro

l

Earl

yst

ress

Mid-

seas

onTerm

inal

stre

ss

Root yield (t ha-1 drywt)

Shoot biomass (t ha-1

dry wt)Mean LAI

CM 507-37

14.0

11.1 11.3

11.1

6.0 2.7 5.6

5.3 2.3 1.3 1.8 2.3CM 523-7 13.

812.8 12.

19.7 5.3 4.2 5.

24.5 2.3 1.4 1.3 2.0

CMC 40 10.0

10.4 12.1

14.6

7.8 3.9 5.7

6.7 1.7 1.1 1.1 1.7M Col 1684

13.6

10.3 12.5

11.5

5.0 2.2 4.0

4.3 1.8 1.1 1.3 1.8

Average 12.9

11.2 12.9

11.7

6.0 3.3 5.1

5.2 2.0 1.2 1.4 2.0LSD 5%Treatment

NS* 0.8 0.3Treatmentx Cultivar

2.7 1.4 0.5

Table 13. Activities of some photosynthetic enzymes in leafextracts of field-grown cassava at Santander de Quilichao in1992. Values are means ± SD. Note the wide range of genetic

variations in enzymes activities that could be used inselection and breeding for enhanced photosynthesis and henceproductivity. It is noteworthy that the cultivar MCol 1486 (orCMC 40) had the highest activities of both Rubisco and PEPCand the highest root yield under prolonged terminal water

stress as shown in Table 12.

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Sources: Cassava Physiology Section database; CIAT, 1992;Lopez et al, 1993

CloneActivities (µmol mg chl-1 min-1) PEPC/

RubiscoPEPC Rubisco NAD-ME NADP-MECM 523 – 7 1.57 ±

0.103.62 ±0.62

1.84 ± 0.1

0.41 ± 0.04

0.43CM 507-37 1.91 ±

0.106.84 ± 0.66

1.37 ± 0.4

0.46 ± 0.18

0.28M Col 1684 2.90 ±

0.196.96 ± 1.18

2.05 ± 0.6

0.36 ± 0.03

0.42M Col CMC 40

3.07 ± 0.27

8.16 ± 0.71

1.84 ± 0.6

0.24 ± 0.05

0.38

Water Uptake and Water Use Efficiency

Patterns of water uptake across clones during extended waterstress imposed at different stages of growth are shown inFigure 17. In all stress treatments, cassava withdrew morewater from the deep soil layer (two meters in depth), afterthe upper layer was almost depleted. Moreover, the wateruptake from this deep layer increased as stress progressed,particularly in the terminal stress treatment, indicating thedeep rooting behaviour as previously reported (CIAT, 1991,1992, 1993, 1994; Cadavid et al, 1998; Connor et al, 1981; DeTafur et al, 1997a; El-Sharkawy and Cock, 1987b; El-Sharkawyet al 1992b). It is noteworthy that the available soil water byvolume in this soil ranges from 8 to 12 percent (see Connor etal, 1981; El-Sharkawy et al, 1992b).

Figure 17. Patterns of water uptake by cassava duringextended water deficit at Santander de Quilichao. Data are

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averages of four cultivars. Note the greater waterextraction from deeper soil layers that increased as waterstress progressed over time, particularly in terminally

stressed crops (El-Sharkawy et al. 1992b, CIAT 1993, De Tafuret al. 1997a, El-Sharkawy, 2006, 2007, 2010).

Hence, the water uptake under any of these prolonged stresstreatments would probably not exceed about 200mm (the totalavailable water in two meters depth of soil), showingcassava’s capacity to conserve and deplete deep soil waterslowly over an extended period of stress.

In two cultivars (MCol 1684 and its hybrid CM 507-37)subjected to a three month mid-season water shortage, El-Sharkawy et al (1992b) reported that total water uptake, asestimated from periodical sampling of soil cores at two metersdepth during 35 and 96 days of stress was around 100 and 160mmrespectively. The latter value is equivalent to 70-75 percentof the plant-available water at this depth, and much less thanthe rate of pan evaporation of about 4.4mm day−1 at the site ofthe trials. In recent studies, using the sap flow method,Oguntunde (2005) estimated daily cassava canopy transpirationunder prolonged natural stress in Ghana, at ca 0.8–1.2mm,which is equivalent to 24 percent of the potentialevapotranspiration.

El-Sharkawy et al (1992b) found that estimated crop WUEvalues during the 43-day period of peak canopy growth between117 and 160 days after planting, were around 4.4–4.8g kg−1 ofwater in the stressed crops as compared to 3.7–4.9g kg−1 innon-stressed crops for MCol 1684 and its hybrid CM 507-37,respectively (values being based on total oven-dried biomass).Because cassava has a long growth cycle and a low LAI during asignificant portion of its growing season, seasonal crop WUEis reduced. Nevertheless, estimated cassava seasonal crop WUEat about 2.9g total dry biomass per kg of water, in fieldlysimeter-grown crops compares favourably with values foundwith the C4 grain sorghum at ca 3.1g kg−1, and much greater thanthose in the C3 field bean at ca 1.7g kg−1 (El-Sharkawy, 2004;El-Sharkawy and Cock, 1986). Due to a higher HI in cassava(0.6–0.7), WUE in terms of economic yield would be even

65


greater than in both sorghum and field bean, with their lowerHI values.

Moreover, in a large yield field-trial with 16 improvedcassava cultivars grown in a seasonall dry zone in the PatiaValley, Cauca Department, Colombia, with less than 1,000mm ofprecipitation in 10 months, average harvestable total drybiomass, excluding fallen leaves and fine roots, was greaterthan 30t ha−1 (El-Sharkawy et al, 1990). In this trial, themean oven-dried root yield among cultivars ranged from 15 to27.4 t ha−1, with an overall mean of 20 t ha-1. If it isassumed that all rainfall was effectively used by these cropsand lost via plant transpiration and evaporation from exposedsoils only, ie evapotranspiration(although 60 percent of therainfall occurred in the sixth and seventh months during thegrowth cycle, that may imply some water runoff and deeppercolation into the clayey soil), an evapotranspiration ratio(water loss per unit total dry matter produced) of about 270–300 is then obtained. Such a ratio is comparable to values(excluding soil evaporation) observed in tropical C4 cropspecies such as maize, millet, sorghum and sudangrass, andmuch smaller than values obtained in C3 species (Stanhill,1986). The actual evapotranspiration ratio of cassava may havebeen even lower than the estimated values since fallen leavesmy account for 2-6 t ha−1 (El-Sharkawy and Cock 1987b; El-Sharkawy et al 1992b; Pellet and El-Sharkawy, 1997). In termsof economic yield, an estimated evapotranspiration ratio ofabout 500 in this trial is much less than values in grainsorghum (868), proso millet (567) and maize (1,405) obtainedin the Briggs and Shantz trials (see Stanhill 1986). Ifadjusted for moisture content in the grains of these cereals,the values would be much greater than in cassava. Thesefindings indicate the potentially high WUE of cassava, andfurther strengthen its comparative advantage in water-limitedzones.

However, under non-limiting rainfall or with irrigation,cassava would be more efficient in terms of annual caloriesproduced per unit land area and water consumption than mosttropical C4 grain crops (El-Sharkawy, 1993, 2004). It has beenpredicted (El-Sharkawy, 2005) that productivity of cassava

66


would probably be enhanced further due to rises in atmosphericCO2 and temperature (ie, the known global climate changephenomena), that should result in a much greater WUE. Thisprediction is substantiated by recent findings (Fernández etal, 2002) that leaf photosynthesis and root yield of field-grown cassava under elevated CO2 in the tropics (at 680cm3 m−3

within open-top chambers) were higher than values in ambientCO2-grown plants, indicating the absence of the photosyntheticdown-regulation often observed in some other species (seeKramer, 1981; Mooney, et al1991; Pettersson and McDonald, 1994;Webber et al, 1994; Woodrow, 1994). The absence of such down-regulation was apparently associated with greatercarboxylation efficiency of the C3 Rubisco, despite reductionsin soluble protein and nitrogen content in leaves, indicatinghigher nitrogen use efficiency in terms of CO2 uptake. El-Sharkawy (2004) reported significant positive correlationsbetween dry root yield and photosynthetic nitrogen useefficiency – expressed as CO2 uptake per unit of total leafnitrogen as measured in normal air and high solar irradiancein upper canopy leaves – across a wide range of field-growncassava cultivars without CO2 enrichment. Furthermore, thesoluble sugars and starch content in leaves of elevated CO2-grown plants were reduced, suggesting higher demands by strongsinks for assimilates, as indicated by the concomitantincreases in both shoot biomass and storage root yield(Fernández et al, 2002). Also, Ziska et al (1991) reported a56 percent increase in leaf photosynthesis of cassava plantsgrown for long periods in elevated CO2 under controlledconditions (at 300cm3 m−3 above ambient CO2) indicating theabsence of down-regulation. These photosynthetic attributescombined with a high optimum temperature for leafphotosynthesis (see Figure 11 A, B) and elevated activities ofthe C4 PEPC in cassava leaves (see Tables 3, 4,5 and 13) mayconfer an adaptive advantage upon cassava growth andproductivity in the case of global warming.

In contrast to the above findings, Gleadow et al. (2009)reported lower leaf photosynthetic rates in plants grown athigher than ambient CO2, particularly in those grown at the

67


highest level. They also found significant reductions in shootand storage root biomass. However, we point out that theseauthors studied potted cassava grown under greenhouseconditions at different levels of CO2, that is, at 360, 550,and 710 ppm CO2. Obviously, these findings indicated a feedbackinhibition due to the rooting systems being confined by thegrowth media used. Cassava is a tropical shrub (Figure 1) thatrequires large volumes of soil for the development of itsstorage roots. When grown under inappropriate conditions, itwill not express either its leaf photosynthetic capacity orits potential productivity. Thus, as warned earlier in thechapter, such findings are invalid and any resultingconclusions must be questioned. In contrast, field researchconducted in CIAT’s sunny, hot, humid, and tropicalenvironment, demonstrated cassava’s high photosyntheticcapacity and productivity.

Cassava’s deep rooting characteristics, combined withpartial stomatal closure in response to both soil andatmospheric water deficits, as well as a reduced leaf canopyand light interception while maintaining reasonable leafphotosynthesis, are of a paramount importance when the crophas to endure several months of prolonged drought inseasonally dry tropical ecosystems, where excess rains oftenrecharge deeper soil layers. This pattern of conserved wateruse results in optimising seasonal crop WUE (El-Sharkawy,2004; El-Sharkawy and Cock, 1986). Boyer (1996) reviewed anddiscussed advances in drought tolerance in field crops and thepossible mechanisms underlying enhanced crop WUE. The deeprooting characteristics accounted for a major part ofdifferences in drought tolerance among species. These inherentmechanisms may partially explain why stressed cassava is stillcapable of producing reasonably well, as compared to othercereal and grain legume food crops, and further strengthen thestrategy of expanding cultivation of cassava in drought-proneareas where severe food shortages might occur (De Tafur et al,1997a; El-Sharkawy, 1993, 2004; Hershey and Jennings, 1992).

68


SELECTION FOR SHORT-STEMMED CULTIVARS MORE EFFICIENT INNUTRIENT USE AND IN LEAF PHOTOSYNTHESIS

Research under prolonged water deficits in the field (El-Sharkawy et al., 1998b) showed that early and midseason waterdeficits increased nutrient use efficiency, in terms of rootyield, due to more reduction in aerial parts (stems andleaves) as compared to storage roots, and hence, less totalplant nutrient uptake.

This observation had led to search for genotypic variationsin productivity and nutrient use efficiency as affected byplant type. Among two groups of tall and short-stemmedcultivars, aerial parts were significantly lower in short-stemmed cassava while root yield was approaching values intall cassava (Table 14). Seasonal average leaf area index(LAI) was significantly lower in short-stemmed cultivars(Figure 18 and Table 14) while average leaf photosyntheticrate was significantly greater (about 12%) compared to tallcassava (Figure 19 and Table 14).

In these trials light interception was less in short-stemmedcassava planted at 10,000 plant ha-1 that indicated less canopyphotosynthesis per unit land surface area that could beimproved by increasing plant densities. Since the differencein photosynthesis was attributed mainly to nonstomatalfactors, ie. biochemical and anatomical features withinmeasophyll (El-Sharkawy and De Tafur, 2010) , selection forhigher activities of key photosynthetic enzymes, ie. Rubiscoand PEPC, might lead to greater yield in short-stemmedcultivars.

The powerful molecular biology tools and genomics research,if properly focused toward practical applications, mightfurther enhance progress in breeding and selection of moreefficient short cassava cultivars via identification, mappingand transferring specific genes related to leaf photosyntheticcapacity (including anatomy and biochemical traits), photo-assimilates translocation and sink strength of storage roots,as well as sugar synthesis and starch metabolismcharacteristics (Bonierbale et al., 2003; Raines, 2006, 2011).

69


A significant advance in that direction is the recentdetermination of the complete sequence andorganization/structure of the chloroplast genome of cassava,which is the first published genome sequence of a member ofthe family Euphorbiaceae (Daniell et al., 2008). However, theimplications of these findings for the process of cassavaphotosynthesis have yet to be investigated. Moreover, sincesignificant yield losses result from several arthropod pestsfeeding on cassava storage roots, leaves, and/or stems,particularly members of Lepidoptera, Diptera, and Hemiptera,chloroplast genetic manipulations might help in alleviatingthis problem through the use of a high-dosage strategy thatcan kill both susceptible and resistant insects to Bacillusthuringiensis toxins.

Thus, the chloroplast genome sequence may provides thenecessary information for the design and construction of anefficient chloroplast vector system (Daniell et al. 2008).Table 14 . Comparative productivity and leaf photosynthesis indifferent plant types grown under rain-fed conditions at CIAT-Quilichao Experiment Station, Cauca Department, Colombia. Dataare means of two years (1994/1995, 1995/1996). Seasonal leafphotosynthesis was determined in upper canopy leaves from 3 to8 month after planting by portable CO2 infrared gas analyserduring dry periods. Final harvests were conducted 10 months

after planting. Note: the higher harvest index (HI) values dueto the much lower dry shoot biomass in short-stemmed

cultivars. (El-Sharkawy and De Tafur, 2010)

Cultivar SeasonalLAI

Seasonal Pn

µmolCO2 m-2 s-1

Final dry root yieldtha-1

Final dry shoot biomass tha-1

Final total biomasstha-1

HIHarvest index

Tall – High LAICG 402 -11 3.13 15.68 11.9 8.0 19.9 0.60CM 4574 – 7 2.91 14.45 14.5 5.8 20.3 0.71MBra 110 2.46 17.18 11.4 7.6 19.0 0.60MMal 48 2.82 15.89 17.2 7.3 24.5 0.70CM 507 – 37 2.41 15.61 12.4 4.7 17.1 0.73

70


CM 4729 – 4 2.10 17.16 13.0 5.5 18.5 0.70SG 536 – 1 2.10 16.58 9.2 3.7 12.9 0.71Mean 2.56 16.08 12.8 6.09 18.89 0.68Short – Low LAIMCol 22 1.93 17.54 8.5 2.5 11.0 0.77MBra 900 1.86 21.44 8.5 2.7 11.2 0.76CG 1141 – 1 1.85 17.23 12.7 2.4 15.1 0.84CG 1420 – 1 1.77 17.93 9.0 2.2 11.2 0.80CM 2766 – 5 1.66 15.59 10.1 3.2 13.3 0.76MPan 51 1.63 17.86 8.7 4.9 13.6 0.64CM 3294 – 4 1.58 18.38 10.4 3.3 13.7 0.76SG 107 – 35 1.51 18.18 11.2 4.1 15.3 0.73Mean 1.72 18.02 9.89 3.16 13.05 0.76LSD 5% between groups means

0.4 1.75 1.3 1.1 1.8

Nutrient use efficiency in terms of dry root production wassignificantly greater in short-stemmed cultivars than valuesin tall ones (Table 15 ).Thus, breeding for short-stemmedcultivars is warranted since resource-limited cassavaproducers rarely use chemical fertilizers and most cassavaproduction occurs in marginal low-fertility soils.

Table 15. Nutrient use efficiency for root production at 10months after planting [kg(dry root) kg–1(total nutrient

uptake)] for groups of tall and short cassava cultivars. Meansof two years (1994/1995, 1995/1996). Source: (Adopted from El-

Sharkawy et al. 1998a)

Group N P K Ca MgTall 110 715 132 347 589Short 131 885 161 430 669LSD 5 % 17 85 22 77 91

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Tall - High LAIM ean 2.56

LAI

0

1

2

3

Short - Low LAIM ean 1.72

DAYS AFTER PLANTING

0 50 100 150 200 250 300 350

LAI

0

1

2

3

Figure 18. Time course of average LAI in tall- and short-stemmed cassava cultivars in the first growing cycle.

Calculated LAI values were determined nondestructively bylight-sensing canopy analyser based on differences betweenreadings of light incidence above canopy and those recordedbelow the canopy at soil level. Values are means of allcultivars within each group. Bars are ± SD. Note: (a) thedrop in mean LAI between 110- 150 DAP due to a prolongeddrought; (b) the steeper decline in LAI in short cultivars

from 200 to 300 DAP in contrast with trends in tallcultivars

Source: El-Sharkawy and De Tafur, 2010.

72


Combined to this cultivar trait, early bulking (earlystorage root formation and filling) should be selected forwhen cultivars are grown in water-limited environments (El-Sharkawy et al., 1998a, El-Sharkawy 2006b; Kamau et al.,2011). Moreover, longer leaf life (better leaf retention) andresistance to pests and diseases should be combined withshort-stem trait.

Tall - High LAIM ean 16.08

PN [µmol (CO 2 )m

-2 s-

1 ]

0

5

10

15

20

25

Short - Low LAIM ean 18.02

DAYS AFTER PLANTING

40 60 80 100 120 140 160 180 200

PN [µmol (CO 2) m

-2 s-

1 ]

0

5

10

15

20

25

Figure 19. Time course of upper canopy leaf photosyntheticrate of tall- and short-stemmed cassava cultivars. Rateswere determined in the field using portable infrared gas

analysers and leaf chambers at solar PAR irradiance greaterthan 1000 µmol m-2 s-1. Data are means of all cultivars within

each plant type group. Bars are ± SD. Note: (a) the lowrates near 120 DAP coincided with a long drought period; (2)

73


the higher rates in short-stemmed cultivars after recoveryfrom water stress, as compared to tall cultivars. Source:

El-Sharkawy and De Tafur, 2010.

SELECTION FOR PLANT TRAITS UNDERPENNING DROUGHTTOLERANCE IN CASSAVA

Biochemical, Physiological, and Morphological Traits Associated with Drought Tolerance

Under stressful environments in the seasonally dry and semi-arid tropics, cassava possesses some inherent adaptivemechanisms for tolerance. Most important is the remarkablestomatal sensitivity to changes in atmospheric humidity aswell as changes in soil water. By closing stomata under waterstress, the leaf remains hydrated and photosyntheticallyactive, albeit at reduced rates, over most of its life span.Coupled with this stress avoidance mechanism is the deeperrooting capacity, where stored water in two metres depth ofsoil could be extracted at a slow rate leading to not only thesurvival of the crop during dry periods exceeding three monthsbut also to a reasonable yield with efficient use of water andnutrients. Deeper rooting capacity is another important traitfor selection and breeding of improved germplasm targeted todrier zones.

In addition, the leaf canopy is much reduced under prolongedstress, contributing to lower crop water consumption. Whenrecovered from stress, cassava rapidly forms new leaves withhigher photosynthetic capacity, which compensates for yieldreductions due to previous prolonged stresses. Productivityover a wide range of germplasm and in different environmentscorrelates with upper canopy leaf photosynthesis as measuredin the field, and the relationship is due mainly to non-stomatal factors, ie, biochemical/anatomical leaf traits.Among these leaf traits are elevated activities of the C4

enzyme PEPC. Leaf area duration under stress, coupled withhost plant resistances/tolerances to pests and diseases, is a

74


critical trait, since yield correlates with plant leafretention capacity (Lenis et al, 2006).

Drought tolerance in cassava can be assessed by measurementof the associated physiological traits. The traits underlyingsuch high potential productivity in excess of 15t ha−1 oven-dried roots with 85 percent starch in 10–12 months underprolonged water stress include: (i) leaf conductance; (ii)deeper rooting capacity or greater extent of the fibrous rootnetwork; (iii) high leaf photosynthetic potential comparablewith those in efficient C4 crops (rates under high humidity,

wet soil, high leaf temperature and high solar radiation

exceed 40μmol CO2 m−2 s−1); (iv) long leaf life (> 60 days), theleaves remaining active during most of their life span; (v) asustainable leaf canopy that optimises light interceptionduring a significant portion of the growth cycle; (vi) a highHI (> 0.5) coupled with a strong root sink (larger number ofstorage roots per plant); and (vii) high weights of fresh rootand fresh foliage.

Germplasm Evaluationin in the Field for Selecting Drought-Tolerant Cultivars

Results also point to the importance of field researchversus studies carried out on plants grown indoors ingreenhouses and growth cabinets (El-Sharkawy 2004, 2005,2006a,b, 2007, 2010). Well-designed and planned fieldexperiments to determine relevant physiological traits are themost cost-effective way of evaluating drought tolerance incassava. Appropriate sites are seasonally dry and semi-aridregions with 600-800 mm of rainfall distributed over 5-8months of the year such as in Northern Colombia, PacificCoasts of Ecuador and Peru, Northeastern Brazil.

Cassava requires three months of rainfall for establishmentof the crop, after which, the crop tolerates extended waterdeficits greater than 3 months. Sites in Colombia used inconducting the research summarized above for evaluation andselection of drought tolerant cultivars under natural

75


precipitation (De Tafur et al., 1997a,b; El-Sharkawy 1993,2007, 2010; El-Sharkawy et al., 1990; El-Sharkawy and Cock,1990) included:

Semi-arid site at Rio Hacha, Guajira Department:latitude: 11°32' N ; longitude: 72°54' W.

Seasonally dry site at Santo Tomas, Atlantic Department:latitude: 10° 57' N; longitude: 74° 47' W.

Seasonally dry site at Patia Valley, Cauca Department:latitude 2° 09' N; longitude: 77° 04' W.

It is noteworthy to mention that all three testing siteswere small Colombian farmers fields who offered theircollaboration and hospitality to the CIAT cassava researchteam during the course of this long research. To them wededicate the hard-obtained achievements outlined in thischapter.

SUMMARY AND CONCLUSIONS

The research reviewed here on cassava productivity,physiology and/or ecophysiology, and responses toenvironmental stresses was conducted in collaboration with amultidisciplinary team at CIAT. The Center also holds adiverse germplasm bank of the crop, which has been assembledover 40 years. The research objectives revolved around thestrategy adopted for developing new technologies to enhancecrop productivity in most of the edaphoclimatic zones underwhich cassava is cultivated, particularly stressfulenvironments.

Under favorable environments in lowland and mid-altitudetropical zones with near-optimal climatic and edaphicconditions for the crop to realize its inherent potential,cassava is highly productive in terms of root yield and totalbiological biomass. For example, under trial conditions,improved germplasm can, after 10–12 months’ growth, attain >15t/ha of oven-dried roots, containing 85% starch. Thephysiological mechanisms underlying such high potentialproductivity are:

76


1. High leaf photosynthetic potential, comparable with thosein efficient C4 crops (assuming the following conditionsare common: high humidity, adequate soil moisture, highleaf temperature, high solar radiation, and a Pn ratethat exceeds 40 µmol CO2 m-2 s-1 );

2. Long leaf life (>60 days), with the leaves remainingactive for most of their life spans;

3. Sustainable leaf canopy that optimizes light interceptionduring a significant portion of the growth cycle; and

4. High harvest index (>0.5), coupled with strong root sink(i.e., larger number of storage roots/plant).

Under stressful environments in seasonally dry and semi-aridtropics, productivity is reduced, with more reduction inaboveground parts (shoots) than in storage roots (i.e., higherHI). Under these conditions, the crop possesses some inherentadaptive mechanisms for tolerance. The most important one isthe remarkable stomatal sensitivity to changes in atmospherichumidity, as well as in soil water. By closing stomata underwater stress, the leaf remains hydrated and photosyntheticallyactive, although at reduced rates, over most of its life span.

Together with this “stress avoidance mechanism” is a deeprooting capacity that enables the plant to slowly extractwater from as deep as 2 m. The crop therefore not onlysurvives dry periods of up to 3 months long, but also producesa reasonable yield through its efficient use of water andnutrients. Moreover, leaf canopy is much reduced underprolonged stress, contributing to lower crop waterconsumption. When it recovers from stress, cassava rapidlyforms new leaves with higher photosynthetic capacity, whichcompensates for yield reductions from the previous prolongedstress.

Productivity over a wide range of germplasm and in differentenvironments correlates with upper canopy leaf photosynthesis,as measured in the field. The relationship stems mostly fromnon-stomatal factors, that is, from biochemical and anatomicalleaf traits. Among these leaf traits is the elevated activity

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of the C4 PEPC enzyme. Breeding programs could exploit thegenetic variations found within cassava germplasm and wildManihot for both leaf photosynthesis and enzyme activity. Leafarea duration under stress, together with host-plantresistance or tolerance of pests and diseases, is a criticaltrait because yield correlates with leaf retention capacity(Lenis et al., 2006). Deep rooting capacity is anotherimportant trait for selecting and breeding improved germplasmfor drier zones.

In cooler zones such as higher altitudes in the tropics andlowland subtropics, cassava growth is slower and the cropstays in the ground for longer time to achieve adequateyields. Under these conditions, leaf formation is slower, leafphotosynthesis is much reduced, but leaf life is longer(Irikura et al. 1979; El-Sharkawy et al., 1992a, 1993). Widegenetic variations exist for photosynthesis that may bevaluable for selecting and breeding for genotypes that bettertolerate cool climates. Combining enhanced leaf photosynthesiswith the normally longer leaf life in cool climates mayimprove productivity.

Selecting for medium-statured and short cassava instead oftall cassava is advantageous for saving on nutrient uptake andensuring higher nutrient-use efficiency for root productionwithout sacrificing potential yield. Short cultivars showed atendency for early bulking, a favorable selectable trait forseasonally dry and semi-arid environments (El-Sharkawy et al.,1998a; El-Sharkawy, 2006b; El-Sharkawy and De Tafur, 2010) .Germplasm from the core collection was screened for toleranceof soils low in P and K, resulting in the identification ofseveral accessions with good levels of tolerance.

Results also point to the importance of field researchversus greenhouse or growth-chamber studies that do notcalibrate for representative environments to account foracclimation factors (El-Sharkawy, 2005). Calibration becomeseven more critical when data from indoor-grown plants are usedto extrapolate to the field or to develop crop models.

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FUTURE PROSPECTS FOR CASSAVA IMPROVEMENT

Much remains to be done to further improve productivitywhile conserving dwindling natural resources such as water andland. Developing countries, in particular, need more supportto continue with maintenance research, which aims to upgradeprevious findings and technologies; contribute to sustainableagricultural, economic, and social developments; and enhancefood supply to meet increasing demands under observed trendsin global climate changes. Cassava is unique among staplecrops in meeting these demands because of its inherenttolerance to adverse eco-edaphic conditions such as highertemperature, prolonged drought and poor soils.

Basic research can be cost-effective, with high returns,even if slower. It can be especially successful when conductedin collaboration with multidisciplinary and/or multi-institutional teams that follow well-planned strategies andare focused towards fulfilling a set of high priority goalsand objectives. Plant physiology, biochemistry and moleculargenetics are essential components in such endeavors. Sincecassava is genetically heterozygous and vegetative propagatedfor commercial production, genetic manipulation aided byadvanced biotechnology tools should further enhance progressin cassava improvement in the near future, particularly understressful environments, as the plant is amenable to genetictransformation (Li et al., 1996; Puonti-Kaerlas, 1998). Thisgenetic molecular approach is of paramount importanceparticularly for characterizing germplasm pools, selectingplants tolerant/resistant of devastating pest diseases, forfood and feed biofortifications of storage roots withessential nutrients (eg, higher content of protein, carotenes,trace minerals such as iron and zinc), all are characteristicsthat might enhance productivity and qualities of cassava end-products (Schuch et al., 1996; Bonierbale et al., 2003;Ferriera et al., 2008; Stupak ,2008;Montagnac et al., 2009b;Nassar and Ortiz, 2010; Abhary et al., 2011; Sayre et al.,2011; Vieira et al., 2011). Cassava germplasm is widelydiverse in storage root carotenes content (Iglesias et al.,

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1997; Ferriera et al., 2008) that are essential nutrients forprovision of Vitamin A in human diets. Breeding programs ofnational and international research institutions are currentlyembarked on developing improved cultivars rich in thesecompounds. It is anticipated that when released these improvedcultivars rich in pro-Vitamin A carotenes, will be alsodrought tolerant/resistant for its potential cultivation indrought-stricken tropical/subtropical regions where cassavaintake is quite high. Worldwide research effort forbiofortification of staple food crops via breeding improvedcultivars was launched in the past two decades (Welch andGraham, 2002).

International research and development organizations, donoragencies, and private sectors should take leading roles infinancing and supporting basic research efforts, particularlythose oriented towards serving the technological needs ofresource-poor developing countries. Without the steady fundingby only a few international donors during the 1940s and 1950s,the so-called ´Green Revolution´ of the 1960s, which had savedmany developing countries from famine, would probably neverhave happened (Wortman,1981). The Green Revolution´s researchwas mainly conceived and conducted by few committedinternational researchers working in close collaboration withnational programs across continents (Borlaug, 1983). Thecurrent CGIAR policy of conducting short-term researchprojects which in most cases are serving the self-interest ofthose involved, instead of mission-and-team-oriented andproblem-solving core research, is counterproductive and shouldbe reversed to avoid waste of resources and time (eg,Okogbenin, 2010). Scientists as well as research managers mustbe hold accountable for delivering the goods expected by thetax-providing public, donors, and developmental agencies.

ACKNOWLEDGEMENTS

The authors are indebted to the many colleagues, associates,students, workers and secretaries at CIAT whose dedication andsupport were crucial in realising the research achievements

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highlighted in this review article. The many useful reprintsreceived from G Bowes, V Gutschick, P Jarvis, C Körner, RLösch, F Meinzer, O Ueno and P Westhoff were appreciated. Wethank MB Kirkham for the copy of her invaluable text book onPrinciples of soil and plant water relations. Useful comments on anoriginal version were received from Drs D Laing (former DeputyDirector General for Research at CIAT) and JD Hesketh(USDA/ARS, University of Illinois, Urbana, Illinois, USA). Weare grateful to Farah El-Sharkawy Navarro for her invaluablehelp in searching the internet for pertinent information,assembling the numerous data in tables and figures scatteredin various published and unpublished documents, and in typingthe manuscript. The logistic and financial supports fromvarious governments and research-funding organisationsincluding Australia, Brazil, Colombia, Germany, Switzerlandand the USA, were crucial in conducting this research, whichis targeted to the needs of some of the poorest farmers indeveloping countries.

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