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Diseases of Quinoa (Chenopodium quinoa)Solveig Danielsen a; Alejandro Bonifacio b; Teresa Ames ca The Royal Veterinary and Agricultural University, Frederiksberg C, Denmarkb PROINPA Foundation, Choquenaira, La Paz, Boliviac International Potato Center (CIP), Lima, Peru

Online Publication Date: 05 January 2003To cite this Article: Danielsen, Solveig, Bonifacio, Alejandro and Ames, Teresa(2003) 'Diseases of Quinoa (Chenopodium quinoa)', Food Reviews International,19:1, 43 - 59To link to this article: DOI: 10.1081/FRI-120018867URL: http://dx.doi.org/10.1081/FRI-120018867

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Diseases of Quinoa (Chenopodium quinoa)

Solveig Danielsen,1,2,* Alejandro Bonifacio,3 and Teresa Ames1

1International Potato Center (CIP), Lima, Peru2The Royal Veterinary and Agricultural University, Thorvaldsensvej 40,

Frederiksberg C, Denmark3PROINPA Foundation, Choquenaira, La Paz, Bolivia

ABSTRACT

Downy mildew caused by Peronospora farinosa is the most damaging disease of

quinoa (Chenopodium quinoa), an ancient Andean grain crop. The disease has been

reported from all areas of quinoa cultivation. In the Andean highlands, it is considered

endemic. Despite the disease’s wide dissemination and significant effect on quinoa

crop production, little is known about its epidemiology, host specialization, population

structure, and host plant resistance. There is a similar knowledge gap regarding other

quinoa diseases, such as Rhizoctonia damping off, Fusarium wilt, leaf spot (Ascochyta

hyalospora), seed rot and damping off (Sclerotium rolfsii, Pythium zingiberum), and

brown stalk rot (Phoma exigua var. foveata). These diseases are less widespread than

downy mildew but are still considered potential production constraints, particularly

when the crop is introduced in areas outside its traditional growing regions. This article

provides an overview of current knowledge on downy mildew and other diseases

affecting quinoa production.

INTRODUCTION

Until recently, the diseases of quinoa (Chenopodium quinoa Willd.) received little

attention; few studies have been carried out on their epidemiology or their potential effects

43

DOI: 10.1081/FRI-120018867 8755-9129 (Print); 1525-6103 (Online)

Copyright q 2003 by Marcel Dekker, Inc. www.dekker.com

*Correspondence: Solveig Danielsen, Danish Government Institute of Seed Pathology for

Developing Countries (DGISP), Denmark; E-mail: soda@kvl.dk.

FOOD REVIEWS INTERNATIONALVol. 19, Nos. 1 & 2, pp. 43–59, 2003

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on crop production. The few available reports of quinoa disease occurrence around the

world have highlighted this knowledge gap. These reports include: Rhizoctonia damping

off and Fusarium wilt in Peru (Barboza et al., 2000); seed rot and damping off (caused by

Sclerotium rolfsii) in the United States (Beckman and Finch, 1980); damping off (Pythium

zingiberum) in Japan (Ikeda and Ichitani, 1985); and leaf spot (Ascochyta hyalospora)

(Boerema et al., 1977), and brown stalk rot (Phoma exigua var. foveata) in the Andean

region of South America (Otazu and Salas, 1977). These diseases have only been reported

sporadically, however, and are probably of minor importance as quinoa production

constraints.

In contrast, downy mildew caused by Peronospora farinosa is an important and

widespread disease in quinoa growing areas in Peru, Bolivia, Ecuador, and Colombia

(Alandia et al., 1979; Aragon and Gutierrez, 1992; Mujica et al., 1998). The disease is

consistently present in these areas and is thus regarded as endemic. Downy mildew has

also been detected in Canada (Tewari and Boyetchko, 1990) and Europe (John Hockenhull

and Sven-Erik Jacobsen, pers. comm., and Danielsen et al., 2002).

Despite the importance and wide dissemination of this disease, little is known about

its epidemiology, host specialization, and impact on grain yield, or the structure of its

pathogen populations and sources of resistance in quinoa. Estimates of yield losses due to

downy mildew vary between 20 and 25%, indicating that this disease is an important

constraint to quinoa production (Alandia et al., 1979). Because these data are based on

only one experiment with one cultivar, quantifying the effect of downy mildew on quinoa

yield requires further study.

Most research reports on downy mildew in quinoa focus on the detection of the

pathogen and the determination of differences in susceptibility among cultivars, under

natural growing conditions in the Andean region. This data is documented mainly in

technical reports from research center field stations, or in thesis reports, and is therefore

inaccessible to the public. Thus, the scientific literature on this disease is sparse compared

to that on downy mildew of spinach and beet, two economically important crops that are

also attacked by P. farinosa. A quick search of the CAB International abstracts database

(1973–2000) illustrates this disparity, generating 106, 109, and four hits for downy

mildew of beet, spinach, and quinoa, respectively.

To help fill this gap, we surveyed, compiled, and summarized existing data to provide

an overview of the current knowledge base on quinoa crop disease, with special emphasis

on downy mildew. The data presented below are based on a literature review and on recent

research carried out at the International Potato Center (CIP) in Lima, Peru.

LEAF AND STALK DISEASES

Downy Mildew

The Pathogen

Taxonomy

Peronospora farinosa (Fr.) Fr., the causal agent of downy mildew of quinoa, is an

oomycete belonging to the Peronosporaceae family (Peronosporales order), a group of

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highly specialized, biotrophic organisms that are parasitic on vascular plants and cause

downy mildew across a limited host range (Ingram, 1981). Oomycetes have recently been

excluded from the Fungi kingdom, but their exact classification remains controversial.

Some scientists place them in the Stramenopila kingdom, whereas others place them in the

Chromista kingdom. Peronospora farinosa attacks members of the Chenopodiaceae

family, including beet, spinach, and quinoa, and has been found on all continents

(Anonymous, 1988). A subdivision of P. farinosa was proposed by Byford (1967), who

found that isolates of P. farinosa from sugar beet (Beta vulgaris), fat hen (Chenopodium

album), and spinach (Spinacia oleracea) would only infect the host species from which

they were isolated. He therefore suggested the following classification: P. farinosa f.sp.

betae on Beta spp., P. farinosa f.sp. spinaciae on Spinacia spp., and P. farinosa f.sp.

chenopodii on Chenopodium spp. However, the failure of spores from C. album to infect

C. amaranticolor and C. capitatum (Byford, 1967) and the lack of cross-infection between

isolates from C. murale, C. album, and C. ambrosioides (Aragon and Gutierrez, 1992),

suggests that further specialization occurs. In other experiments, conducted in Peru, the

quinoa cv. Blanca de Junın was not infected by downy mildew isolates from the cv. La

Molina 89 (Aragon and Gutierrez, 1992), and another Andean grain crop, C. pallidicaule,

was not infected by P. farinosa isolates from quinoa (Alandia et al., 1979). This indicates

the existence of different pathotypes within this forma specialis, as well as different

sources of resistance among quinoa genotypes. In general, a high degree of physiological

specialization has been found within the Peronosporaceae family (Crute, 1981).

Infection Biology

The presence of free water and RH . 85% is necessary for conidia of the genus

Peronospora to germinate (Alandia et al., 1979; Develash and Sugha, 1996; Hartmann

et al., 1983). The germ tube penetrates the cuticle of the leaf and the mycelium ramifies

intercellularly, through the leaf and stalk tissues. Haustoria formed from hyphae penetrate

the cells, and sporangiophores emerge either individually or in groups, through the

stomata, to form ramifications with lemon-shaped sporangia. In general, Peronospora

species require moderate temperatures (10–208C) for optimal sporulation (Byford, 1981;

Develash and Sugha, 1996; Doshi and Thakore, 1993; Frinking and van der Stoel, 1987;

Hartmann et al., 1983; Shao et al., 1990). Species of the genus Peronospora do not form

zoospores. The asexual spores (sporangia; also called conidia) are dispersed by wind and

rain and are assumed to be of utmost importance for spread of the disease during the

growing season (Michelmore et al., 1988).

Sexual Reproduction

While heterothallism has been reported in P. farinosa f.sp. spinaciae (Asch and

Frinking, 1988; Inaba and Morinaka, 1984), the mating system of P. farinosa f.sp.

chenopodii has not yet been studied. Crosses of eight single-lesion isolates from different

regions in Peru and Bolivia in all possible combinations, using a detached leaf assay,

revealed the presence of two mating types, P1 and P2 (Danielsen et al., 2000), indicating

that P. farinosa f.sp. chenopodii is heterothallic. Oospores have been found in large

numbers in old, downy-mildew infected leaves from several quinoa growing areas in Peru

Diseases of Quinoa 45

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(Danielsen and Ames, unpublished), indicating that both mating types are present in these

areas. In contrast, oospores were not found in naturally infected quinoa leaves from the

coastal areas of Lima (Peru), indicating that only one mating type exists in that area or that

environmental conditions are unfavorable for oospore formation.

The specific role of soil- and seed-borne oospores in the spread and initiation of

epidemics of downy mildew of quinoa is not known. However, considering the harsh

climatic conditions of the Andean highlands, which include long periods of drought and

extreme temperatures, it seems clear that oospores play a crucial role in the survival of the

disease. Past research also provides strong indications that seed- and soil-borne oospores

act as a primary source of downy mildew infection. Alandia et al. (1979) reported the

presence of oospores in the integument of quinoa seeds, and International Potato Center

(CIP) scientists observed heavy downy-mildew sporulation on 3–6% of the cotyledons of

six quinoa cultivars from Puno and Cusco (Peru) in 2- to 3-week-old quinoa seedlings

raised from seed and grown in pots of sterilized soil in greenhouses under humid and

temperate conditions, followed by rapid spread to all seedlings (data not shown). While

microscopy of the seed washing water did not reveal any oospores, numerous viable

oospores were found inside the flower residues and seed integument. Based on these

observations, seed-borne inoculum should be an important consideration in the future

commercialization and certification of quinoa seed.

Peronospora Farinosa Populations

Despite the scarcity of data, the following indicators imply that downy mildew

populations in Andean countries are highly diverse: 1) the downy mildew host has a high

degree of genetic diversity and plasticity, making it adaptable to a wide range of

agroecological zones (Risi and Galwey, 1989); 2) downy mildew of quinoa is detected in

climatically and geographically diverse areas, indicating a high degree of adaptability; and

3) sexual reproduction of P. farinosa in quinoa occurs frequently, allowing the pathogen to

constantly expand its genotypic diversity and develop new and more aggressive

pathotypes. Deciphering the pathogen’s genetic composition is an important prerequisite

for developing an effective control strategy. Therefore, determining the presence of

pathotypes and mating types, and their relative frequency and geographic distribution,

would be a first step in developing an effective control strategy for this pathogen.

The only research conducted on virulence factors in downy mildew of quinoa is that

reported by Ochoa et al. (1999). Twenty isolates collected from different parts of Ecuador

were tested on 39 quinoa lines, using a seedling assay to identify virulence factors. Four

virulence groups and three resistance factors were identified, and a preliminary differential

set of four quinoa lines was proposed for identification of virulence groups.

For some purposes, virulence factors are excellent markers for genotypic variation

within a population. However, these types of markers are vulnerable to the process of host

selection. As the use of molecular markers provides a means of testing genotypic variation

with neutral markers, DNA fingerprinting (Random Amplified Polymorphic DNA

[RAPD]) has been used to identify P. parasitica pathotypes (Jensen, 1996; Tham et al.,

1994), and Restriction Fragment Length Polymorphism (RFLP) and AFLP markers are

being used now to characterize strains of Phytophthora infestans from potato in Peru

(Gamboa et al., 1999). AFLPs offer a potentially powerful tool for detecting polymorphic

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DNA sequences in fungi (Lin et al., 1996; McDonald, 1997). The advantage of this

technique is that no previous knowledge on DNA sequences is required, and only small

amounts of DNA are needed to perform the test.

At present, research is being carried out at the CIP to characterize populations of the

downy mildew pathogen in Peru and Bolivia using virulence and Amplified Fragment

Length Polymorphism (AFLP) markers.

The Disease

Symptoms

Quinoa plants infected by P. farinosa present a variety of symptoms, depending on the

cultivar, the growth stage, and the environmental conditions. Typical symptoms include

pale or yellow chlorotic lesions on the surface of the leaf (which cause a reduction in the

photosynthetic area of the plant and eventually turn necrotic) and gray-violaceous

sporulating areas on the underside of the leaf. In some cultivars, the lesions are small and

numerous, whereas in others, the lesions are large, diffuse, and irregular. In some cultivars,

the lesions turn reddish to purple; a hypersensitive type of reaction (small necrotic flecks)

has also been observed. The degree of sporulation varies considerably within cultivars,

most likely due to genetic variation within the pathogen population and differences in the

cultivar response. It has also been noted that severe infection leads to heavy premature leaf

loss (Alandia et al., 1979). However, it is difficult to estimate how much defoliation is

caused specifically by downy mildew, as there are a number of other known factors, such

as physiological stress (e.g., drought, salinity, and frost) that cause defoliation. Systemic

infection has been observed, which may lead to dwarfing and yellowing (Alandia et al.,

1979; Frinking and Linders, 1986; Tewari and Boyetchko, 1990). Systemic infection is

probably caused by seed-transmitted oospores, as seen in pea and buckwheat (Vulsteke

et al., 1997; Zimmer et al., 1992).

Downy Mildew in the Andes

The endemic nature of downy mildew in the Andean region makes it an omnipresent

threat to quinoa production whenever conditions are favorable for disease development. It

has a high capacity for spread and development throughout the region, but it does not

occur with the same intensity in the various quinoa production zones defined for Andean

countries. In Bolivia, quinoa production regions have been divided into different types of

ecoregions, including Northern high plateau, Central high plateau, Southern high plateau,

and inter-Andean valley. In the high plateau, average annual rainfall and relative humidity

declines moving from north to south and from east to west. The temperature does not vary

much in this area, although the presence of Lake Titicaca causes a drop in temperatures

during the cropping period (Bonifacio, unpublished).

The conditions most favorable for disease development occur in the northern high

plateau of Bolivia, particularly in the areas surrounding Lake Titicaca. The valleys, which

tend to have a greater quantity of annual rainfall than the high plateau, are also endemic

zones for downy mildew. In the Southern high plateau, where rainfall is scarce, and

humidity is very low, the occurrence of downy mildew is extremely rare and, thus, is not

Diseases of Quinoa 47

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considered an important production constraint. The conditions of the Central high plateau

(considered a transition zone between the Northern and Southern high plateaus) are only

favorable for the growth of downy mildew when average annual rainfall exceeds normal

levels or when precipitation is concentrated in short periods during the growing season.

Disease Assessment and Yield Loss

A reliable disease assessment method is crucial for disease epidemiology research,

crop-loss assessment, pathogenicity and virulence testing, and screening for resistance/

susceptibility. A large number of disease assessment scales have been proposed for

evaluation of downy mildew in several crops. Downy mildew in pea is measured on

a 0–10 severity scale by Falloon et al. (1995) and on a four-point scale by Mogling and

Broschewitz (1990), while Stegmark (1991) scores the percentage of leaf area infected.

Downy mildew in cabbage crops is measured on 1–9 and 0–5 scales by Jensen et al.

(1999b) and Sousa et al. (1997), respectively. Conclusions from comparison studies of the

various assessment methods indicate that care should be taken when choosing a scale for a

specific purpose. For example, assessment of the use of different methods in detecting the

resistance reaction in potato against early blight (Alternaria solani) showed that cultivar

ranking varied according to the assessment method used (Christ, 1991). Studies measuring

the severity of corky root (Rhizomonas suberifaciens) in lettuce indicated that no single

scale was optimal in all situations (O’Brien and van Bruggen, 1992). Another aspect that

should not be ignored is the effect of human error, which may influence results

significantly (O’Brien and van Bruggen, 1992; Stonehouse, 1994).

Different methods are now being used in Peru and Bolivia to assess the level of downy

mildew in quinoa. A 0–10-point scale has been defined by Otazu et al. (1976), where

0 ¼ no infection, 1 ¼ 1–10% leaf area infected, 2 ¼ 11–20%, etc. Based on this scale,

quinoa cultivars are divided into four groups: resistant ¼ 1–4% infection; moderately

resistant ¼ 5–19%; susceptible ¼ 20–49%, and very susceptible ^ 50%: However, this

scale does not take into account the defoliation caused by downy mildew. Another

evaluation method, developed by Bonifacio and Saravia (1999), considers the effect of

defoliation by only including the middle, foliated third of the plant in the evaluation. The

percentage of infected leaf area in this fraction of the plant is scored on a 0 to 5 scale,

where 0 ¼ no infection; 1 ¼ 1–20% leaf area infected, 2 ¼ 21–40%, etc.

To evaluate existing disease assessment methods and to assess yield loss due to

downy mildew, a field trial was carried out at the International Potato Center (Lima, Peru)

during the winter months of 1999. Quinoa is not usually grown along the Peruvian coast,

where mean annual temperatures are higher than in the traditional quinoa growing areas in

the highlands. The trial included eight quinoa cultivars and two levels of downy mildew

infection (with and without fungicide treatment) in a split plot design with three replicates,

where fungicide treatment was the main plot and cultivar the subplot. Yield data were

adjusted according to the number of plants in each plot, using covariance analysis, and

then correlated to the area under the disease progress curves (AUDPCs), based on disease

severity measurements of the whole plant, the first (lower) section, the second (middle)

section, and the third (upper) section, and on the VO-scale (Otazu et al., 1976), the

AB-scale (Bonifacio and Saravia, 1999), and disease incidence (percent of plants infected)

(Table 1). The disease was assessed three times during the growth period. The downy

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Table 1. Grain yield of quinoa and area under disease progress curve (AUDPC) data from field trial conducted at CIP–Lima 1999.

Grain yield (g)a AUDPCb

Cultivar Fungicide treatedc Untreated Yield red. (%) Whole First Second Third AB VO Incidence

Salcedo INIA 1537 1267 18 174 a 198 abc 222 b 108 bc 47 51 4753

LP-4B 1679 1170 30 176 a 165 ab 237 bc 126 c 49 50 4763

La Molina 89 2695 2110 22 241 b 454 d 194 ab 77 ab 63 81 7183

Blanca de Juli 2052 1585 23 239 b 264 bc 283 c 170 d 44 51 4548

Kancolla 2159 1813 16 174 a 183 ab 236 bc 100 bc 56 64 6050

Jujuy 1753 1545 12 295 b 322 c 355 d 206 e 52 67 5693

Amarilla de M 2666 2514 6 139 a 113 a 228 bc 76 ab 64 74 7344

Ingapirca 2200 1709 22 109 a 157 ab 127 a 46 a 51 56 5295

a Grain yield is the average of three plots ð3:5 £ 3:5 mÞ adjusted by covariance analysis according to the number of plants in the plot.b The AUDPC values listed in the table are the difference between the AUDPC for the fungicide-treated and untreated plots, averaged from three

replicates. The AUDPCs are calculated according to Campbell and Madden (1990) and are based on seven different disease assessment methods:

whole ¼ percentage infected leaf area of the whole plant; first ¼ percentage infected leaf area of the first (lower) foliated third of the plant;

second ¼ percentage infected leaf area of the second (middle) third of the plant; third ¼ percentage infected leaf area of the third (upper) foliated third of

the plant; AB ¼ the severity measurements of the middle third were translated to a 0–5 scale according to Bonifacio and Saravia (1999); VO ¼ the

severity measurements of the whole plant were translated to a 0–10 scale according to Otazu et al. (1976); incidence ¼ percentage infected plants.

Numbers followed by the same letter are not significantly different at the 5% level.c The fungicide-treated plots were sprayed with metalaxyl 2 weeks after sowing, followed by three applications of mancoceb at weekly intervals. This

cycle was repeated twice.

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mildew level was kept low in the fungicide-treated plots. The general disease level in the

untreated plots was low, the AUDPC not exceeding 454 (as per measurement of the first

third part of the plant) in any cultivar.

A reduction in grain yield due to fungicide treatment was found in all cultivars

(6–29%); however, the yield loss was not significant in any cultivar, due to large

differences in variation coefficients ðR ¼ 1%–59%Þ: By contrast, a significant negative

correlation was found between yield and AUDPCwhole, AUDPCfirst, AUDPCsecond, and

AUDPCthird ðR ¼ 240–42%; p ¼ 0:0033 2 0:0054Þ: The AUDPCAB, AUDPCVO, and

AUDPCincidence values were not significantly correlated to yield. This shows that only

about 40% of the yield loss can be explained by downy mildew assessed by the first four

disease assessment methods, and that the five-point and 10-point scales and disease

incidence are not useful methods for downy mildew assessment when disease pressure is

low. The differences in yield and AUDPC (whole, first, second, third) between treated and

untreated plots were ranked using the Mann–Whitney test and subsequently compared

using a P2 test, where yield was the theoretical value and the AUDPCs the observed

values. None of the AUDPC rankings showed significant similarity to the yield ranking,

with AUDPCfirst showing the best fit and AUDPCsecond the worst. This underscores the fact

that, in this case, AUDPCs based on the measurement of percent leaf area infected may be

inadequate to predict yield loss. However, further study is required to test the value of the

different disease assessment methods under varying disease levels.

The tendency of the quinoa plant to defoliate under various stress conditions

(drought, salt, frost, downy mildew, etc.) complicates disease assessment in this crop, as

the measurement of the percent of diseased leaf area does not take into account the total

amount of foliage. One consequence of this leaf shed is that the level of downy mildew

infection of the lower part of the plant will not be registered properly, which may result in

skewed disease scores. This fact is clearly illustrated by the disease progress curve for cv.

La Molina 89 based on the lower third part of the foliage (Fig. 1). For the untreated plot,

there is a drastic drop in disease severity from the first to the second evaluation, due to the

fact that the infected leaves on the lower part of the plant were shed during this period, and

because the new and upper leaves were not reinfected at the same degree. Scoring shed

leaves at 100% disease severity does not correct the problem, due to the risk of including

leaves in this category that are shed for reasons other than downy mildew.

Figure 1. Disease progress curve for cv. La Molina 89 based on severity measurements of the

lower-third part of the foliage.

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Potential ways to overcome this problem include measurements of the green leaf area

(Bryson et al., 1997), percent reflectance at 800 nm wavelength (Nutter, 1989), or

reflectance at two wavelengths (Jacobsen et al., 1998). In the latter case, it is possible to

calculate a Relative Vegetation Index (RVI), which is highly correlated to biomass and

final seed yield and should, therefore, reveal any difference in leaf shed due to different

levels of downy mildew within a cultivar. Reflectance measurements may be a valuable

additional parameter for measuring disease severity and predicting yield loss, when a

negative control is available.

Control Measures

The traditional way of controlling downy mildew in various crops is through

application of fungicides such as metalaxyl. However, the use of such fungicides exposes

the environment and humans to health hazards. There is also a risk that the pathogen will

develop resistance to metalaxyl, as shown for P. parasitica (Crute and Gordon, 1986) and

Phytophthora infestans (Davidse et al., 1981). Moreover, the majority of quinoa growers

are resource-poor farmers who tend to practice low-input farming. Within a scenario of

rapidly spreading, endemic disease and sexually reproducing pathogen populations, these

farmers have only two options for disease control: effective cultural practices and the use

of durable host plant resistance.

Cultural Practices

Experiences from Bolivia show that cultural practices that minimize the relative

humidity in the microclimate may have an effect on the severity of downy mildew. Among

these are: adjusting the spacing between rows and individual plants, orienting the field

against the predominant wind direction, and avoiding excess water in the field (Bonifacio,

unpublished). However, cultural practices alone are insufficient for controlling a disease

such as downy mildew in quinoa, which has the ability to adapt, spread, and reproduce.

Host Resistance

Resistance to downy mildew has been the subject for genetic improvement for several

years. To date, however, improved varieties with reliable resistance are still not available,

although differences among quinoa cultivars in susceptibility to downy mildew have been

observed. A 1976 study from Peru describes 11 C. quinoa genotypes as resistant or

moderately resistant to P. effusa (former name of P. farinosa) at flowering and

fructification (Otazu et al., 1976). In Bolivia, plant breeders are working to increase the

level of durable resistance against downy mildew in quinoa, and a number of promising

accessions have been selected for future crossings (Bonifacio and Saravia, 1999). These

studies show that resistance sources are available, but the genetic mechanisms behind the

resistance (horizontal versus vertical) have not yet been investigated.

Quinoa farmers in the Andean region, however, have accumulated a large amount of

knowledge about the growing characteristics of quinoa cultivars, including grain

characteristics, adaptability to different geographic zones, and reaction to adverse factors

Diseases of Quinoa 51

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such as drought, cold, salinity, and downy mildew. Susceptibility to downy mildew is

believed to be related to the length of the growth season, as the early cultivars appear to be

the most susceptible (Bonifacio and Saravia, 1999).

Within the C. quinoa species, the highest degree of resistance to downy mildew is

found in accessions from the valleys or lower ecoregions of Bolivia, Peru, and Ecuador. In

contrast, the ecotypes of the Southern high plateau are the most susceptible. In

evolutionary terms, this can be explained by the domestication process of the species,

where only genotypes with high resistance have survived in environments with favorable

conditions for downy mildew occurrence. Inversely, genotypes domesticated in very dry

areas have no resistance to downy mildew, either because the resistance genes have been

“lost” during evolution, or because genotypes without resistance have an evolutionary

advantage over resistant genotypes in these areas.

Genetic resistance to downy mildew is found not only in cultivated quinoa but also in

wild species that grow more or less associated with the cultivated crop. There are

indications that wild species such as C. hircinum, C. nuttalliae, C. petiolare, C. album, and

C. ambrosioides harbor downy mildew resistance genes. These sources may be useful for

incorporating resistance into commercial varieties, by traditional hybridization techniques

or by genetic transformation. At present, a large part of the genetic diversity of the genus

Chenopodium, mainly C. quinoa, is stored in germplasm collections in Bolivia, Peru, and

Ecuador (,5000 accessions). Many of these accessions have been characterized for

agronomic traits, including susceptibility to downy mildew, but a complete evaluation of

plant material for resistance to downy mildew has not been conducted with enough

continuity to allow for actual genetic improvement.

Screening for Resistance

Current knowledge is limited by the lack of experiments to identify the pathogen–

host interactions under controlled conditions. Therefore, it is not known whether the

variation in downy mildew incidence under different geographic conditions is due to

variation in environmental conditions or to variation within the pathogen populations.

Existing data on susceptibility and resistance of quinoa cultivars originates almost

exclusively from experiments based on natural infection. This creates uncertainty about

the inoculum level, the possible presence of focal infection points, and the composition of

the pathogen population. Screening for resistance in the field based on natural infection is

time-consuming and laborious. It should only be done in highly conducive areas, with

known pathogen populations and consistently high disease pressure, in order to ensure

reliable and reproducible results. Such “hot spot” areas have yet to be identified for the

quinoa/downy mildew system.

Screening methods based on artificial inoculation of seedlings or detached leaves

under controlled conditions may be a useful tool for quinoa breeders. A large amount of

literature is available on screening for resistance against downy mildew in several crops.

In pea and cabbage, cotyledons or seedlings with a few true leaves can be used in rapid

screening assays for breeding purposes; leaves are inoculated with a known concentration

of sporangia and incubated for 7 days under controlled conditions (Coelho et al., 1998;

Grontoft, 1993; Jensen et al., 1999a; Klodt-Bussmann and Paul, 1995; Nashaat and

Awasthi, 1995; Natti, 1958; Stegmark, 1991; Taylor et al., 1989). A detached leaf assay is

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currently being used at the International Potato Center (CIP) to evaluate resistance against

Phytophthora infestans in potato (Goth and Keane, 1997; Mizubuti and Fry, 1998). Such

screening systems offer many advantages, as they are quick and do not require much

space. A good correlation between seedling and adult plant resistance has been found

(Grontoft, 1993; Jensen et al., 1999b; Natti, 1958; Stegmark, 1991), although some

contradictions have been noted (Dickson and Petzoldt, 1993).

Ochoa et al. (1999) have established a seedling assay to identify virulence and

resistance factors in the quinoa/downy mildew system. Eighteen-day-old seedlings are

inoculated with a spore suspension (105 spores/mL) and incubated for 7 days under fixed

temperature and light regimes. The disease reaction is scored according to a 0–5 scale

(Table 2).

A similar assay is being used at the International Potato Center to characterize disease

reaction. Detached quinoa leaves from 4- to 6-week-old seedlings are placed upside down

on water agar plates moistened with 1 mL of spore suspension (105 spores/mL). After 1

week of incubation under controlled conditions, the degree of sporulation is scored

according to the scale shown in Fig. 2 (Danielsen and Ames, 2000).

These assays may be appropriate for large-scale screening of quinoa germplasm and

for studies of downy mildew populations. The method of choice would depend on the

availability of equipment and space.

Leaf Spot

Leaf spot of quinoa is a seed-borne disease caused by Ascochyta hyalospora (Cooke

and Ellis). Typical leaf spot symptoms include light-colored, circular spots (0.5–1.0 cm)

with a light-brown edge. The spots eventually turn necrotic, and black pycnidia can be

seen with the naked eye (Alandia et al., 1979; Boerema et al., 1977). Heavy infection leads

to leaf loss. In studies of Bolivian quinoa seed samples, observed levels of infection by the

Table 2. Scale for scoring disease reactions of downy mildew (Peronospora farinosa f.sp.

chenopodii) in primary leaves of quinoa (Chenopodium quinoa).

Reaction type Classification Symptoms

0 Resistant No evidence of symptoms, no perceptible necrosis

1 Resistant Small chlorotic-necrotic lesions (2–5 mm) with truncated

mycelium in the mesophyl of the leaf

2 Resistant Small chlorotic lesions (4–8 mm) with a little sporulation

3 Susceptible Medium-sized, confined chlorotic lesions with sporulation;

sporulation mainly on the lower-leaf surface

4 Susceptible Large, not clearly confined chlorotic lesions with sporulation;

sporulation mainly on the lower-leaf surface

5 Susceptible Mild chlorosis with abundant sporulation on upper and lower

leaf surfaces

Source: Ochoa et al., 1999.

Diseases of Quinoa 53

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leaf spot pathogen ranged from 7.8–26.3% (Boerema et al., 1977). Germination testing in

the same study showed that the fungus produces mild to severe browning in the root and

hypocotyl; some of the most severely infected seedlings died.

During the growth season 1999–2000, leaf spot was observed in several quinoa

fields in Puno, Peru, mainly on cv. Kanccolla (data not shown). The geographic

distribution and economic importance of leaf spot are not known. The disease is

frequently reported from fields in the highlands of Peru, but it is not considered a major

constraint to production.

Brown Stalk Rot

Brown stalk rot caused by Phoma exigua var. foveata (Foister) Boerema was observed

for the first time in Puno in 1974–1975 (Otazu and Salas, 1977). Since then, the disease

has been reported frequently from the Andean highlands (Alandia et al., 1979). Initial

symptoms are small, humid spots on the upper-third part of the stalk. The lesions grow to

cover most of the stalk, and inflorescence and pycnidia become visible. The foliage

becomes chlorotic, and the stalk bends downward and tends to break easily.

Phoma exigua is a soil-borne pathogen that is seen in areas with low temperatures and

high humidity, common conditions in the Andean highlands during the growing season.

Pathogenicity tests have shown that mechanical injury of the plant is a prerequisite for

infection. In the Andean highlands, hailstorms frequently cause such mechanical damage

to plants (Otazu and Salas, 1977).

Figure 2. Sporulation index for determination of downy mildew (Peronospora farinosa f.sp.

chenopodii) susceptibility/resistance of quinoa genotypes in a detached leaf assay. The black dots

represent downy mildew sporangia. 0 ¼ no sporulation; 1 ¼ one to few single sporangiophores,

sporulation barely visible; 2 ¼ a few sporangiophores, scattered or in a small, dense group,

sporulation visible; 3 ¼ diffuse sporulation on the whole leaf, or dense sporulation on less than 50%

of the leaf; 4 ¼ moderate sporulation on the whole leaf, or dense sporulation on 50–90% of the leaf;

and 5 ¼ dense sporulation on more than 90% of the leaf. 0–2 ¼ resistant; 3–5 ¼ susceptible.

Danielsen, Bonifacio, and Ames54

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Cross-inoculations showed that P. exigua var. foveata, which causes brown stalk

rot in quinoa, is the same pathogen that causes gangrene in potato (Logan, 1974; Otazu

and Salas, 1977). The frequent use of quinoa–potato crop rotations in the Andean

highlands may be a possible factor in the buildup of inoculum in the soil, which

increases disease pressure. However, neither of these diseases occurs at a level beyond

sporadic incidence.

ROOT AND SEEDLING DISEASES

Rhizoctonia Damping Off and Fusarium Wilt

Root and seedling diseases in quinoa caused by Rhizoctonia and Fusarium were

not mentioned in the literature. However, during the 1998 growing season, Rhizoctonia

solani and Fusarium spp. were isolated from a field of quinoa at the International

Potato Center (Barboza et al., 2000). In pathogenicity tests performed under

greenhouse conditions, R. solani produced symptoms similar to those observed in the

field caused by damping off: failure in seed germination and sunken lesions in the main

stems of old plants at ground level. None of the R. solani isolates anastomosed with

AG 1–7 tester strains, but they did anastomose with each other. Fusarium spp.

reproduced wilting and root rot in old plants.

Because both fungi are soil-borne pathogens that also affect several other hosts,

causing similar symptoms, the inoculum potential in the soil could be an important factor

in enabling the disease to cause damage.

Seed Rot and Damping Off

Seed rot and damping off of quinoa caused by Sclerotium rolfsii Sacc. was first

reported in California in 1980 (Beckman and Finch, 1980), when pre- and post-emergent

damping off of seedlings was observed in a quinoa field. Diseased seedlings showed stem

girdling, and collapse appeared in patchy areas in the field. Sclerotium rolfsii was

consistently isolated from diseased seedlings, and subsequent pathogenicity tests

confirmed that the isolated fungus was the causal agent of the disease.

Another potential constraint to quinoa is damping off caused by Pythium zingiberum,

a pathogen that causes rhizome rot in ginger (Ikeda and Ichitani, 1985). Inoculation of the

soil with P. zingiberum oospores caused damping off of quinoa seedlings within 10 days of

incubation at 308C; C. quinoa proved more susceptible than C. amaranticolor. In a

greenhouse experiment, an unidentified Pythium species killed emerging Amaranthus

seedlings, particularly at high moisture levels, whereas quinoa seedlings remained healthy

(Aufhammer et al., 1994). In both studies, however, differences in cultivar susceptibility

were not considered.

Seed rot and damping off caused by Sclerotium and Pythium have not yet been

reported in South America but should be considered potential production constraints when

quinoa is introduced into areas outside its traditional growing regions.

Diseases of Quinoa 55

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ACKNOWLEDGMENTS

We thank John Hockenhull and Abigail Hollister for their valuable comments on the

manuscript. The research project on downy mildew of quinoa was supported by the Danish

government, Ministry of Foreign Affairs (RUF grant no. 90929).

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