ORIGINAL PAPER

Stress-adapted extremophiles provide energywithout interference with food production

Ray A. Bressan & Muppala P. Reddy & Suk Ho Chung &

Dae Jin Yun & Lowell S. Hardin & Hans J. Bohnert

Received: 10 November 2010 /Accepted: 30 January 2011 /Published online: 19 February 2011# Springer Science+Business Media B.V. & International Society for Plant Pathology 2011

Abstract How to wean humanity off the use of fossil fuelscontinues to receive much attention but how to replace thesefuels with renewable sources of energy has become acontentious field of debate as well as research, which oftenreflects economic and political factors rather than scientific

good sense. It is clear that not every advertized energy sourcecan lead to a sustainable, humane and environment-friendlypath out of a future energy crisis. Our proposal is based on twoassertions: that the use of food crops for biofuels is immoral,and that for this purpose using land suitable for growing cropsproductively is to be avoided. We advocate a focus on new“extremophile” crops. These would either be wild speciesadapted to extreme environments which express genes,developmental processes and metabolic pathways that distin-guish them from traditional crops or existing crops geneticallymodified to withstand extreme environments. Such extrem-ophile energy crops (EECs), will be less susceptible tostresses in a changing global environment and provide higheryields than existing crops. Moreover, they will grow on landthat has never been valuable for agriculture or is no longer so,owing to centuries or millennia of imprudent exploitation.Such a policy will contribute to striking a balance betweenecosystem protection and human resource management.Beyond that, rather than bulk liquid fuel generation, combus-tion of various biomass sources including extremophiles forgenerating electrical energy, and photovoltaics-based captureof solar energy, are superbly suitable candidates for poweringthe world in the future. Generating electricity and efficientstorage capacity is quite possibly the only way for asustainable post-fossil and, indeed, post-biofuel fuel economy.

Keywords Alternative crops . Bioenergy generation .

Extremophiles . Abiotic stress tolerance . Food or fuel

Introduction

The current massive use and dependence on fossil fuels willeventually lead to their depletion but, more importantly, thepresent applications and uses of fossil energy sources

R. A. BressanDepartment of Horticulture and Landscape Architecture,Purdue University,W. Lafayette, IN 47907-1165, USA

R. A. Bressan :M. P. ReddyPlant Stress Genomics Research Center,King Abdullah University for Science and Technology,Thuwal 23955-6900, Saudi Arabia

S. H. ChungClean Combustion Research Center,King Abdullah University for Science and Technology,Thuwal 23955-6900, Saudi Arabia

D. J. Yun :H. J. BohnertDepartment of Plant Biology and Department of Crop Sciences,University of Illinois at Urbana-Champaign,Urbana, IL 61801, USA

R. A. Bressan (*) :H. J. Bohnert (*)Division of Applied Life Sciences, WCU Program,Gyeongsang National University,Jinju 660-701, South Koreae-mail: bressan@purdue.edu

R. A. Bressane-mail: ray.bressan@kaust.edu.sa

H. J. Bohnerte-mail: hbohnert@illinois.edu

L. S. HardinDepartment of Agricultural Economics, Purdue University,W. Lafayette, IN 47907-1165, USA

Food Sec. (2011) 3:93–105DOI 10.1007/s12571-011-0112-9

contribute significantly to altering the environment.Resource exploitation is accelerating as industrializationreaches all regions of the earth, and as people world-widework to improve their lives. Industrialization, populationincrease and the lack of enforceable standards in mostcountries has also led to widespread abuse of the land andenvironmental degradation. These outcomes are consequen-ces of a near single-minded focus on profit, accompaniedby significant income inequality. Manipulations and subsi-dies have hidden the true cost of energy generation modelsthat have emerged over the last 200 years. Dependency onfossil fuels, leading to environmental degradation and globalchanges, seems to go ahead largely unchecked as developingcountries achieve parity with the more developed countries.Continuing along this path could lead to a global crisis that,without arbitration, has the potential to result in momentouscultural, social and economic tensions.

Growing awareness of the facts and certain consequen-ces of continuing along the same unwise trajectory hasresulted in a number of proposals for possible remediesabout how the world’s craving for energy might besatisfied. Among the options, the production of alternativefuels from biomass has often been put forward as oneimportant component for resolving the energy crisis. Otheravenues point to harnessing wind and wave-power,geothermal or photovoltaic energy capture as possibleremedies. All options are being pursued at present; thefinal outcome will most likely be a mix of differentapproaches. With a still growing human population,judgment about whether we will achieve global energyautarky without damaging the biosphere is not yet possible.

Being renewable in principle, biomass indeed assumes aprominent place among the options that must receiveserious consideration. So far, however, this path forproducing bio-fuels has been sidetracked by players withan economic interest on using food crops for ethanolproduction. There are considerable flaws in the approachand serious detrimental consequences will be the outcomeshould this path be followed, unmodified.

Assigning a significant proportion of the North Americancorn crop to ethanol production in 2007, coupled withenvironment-based failure of rice and other critical crops,and increased demand for high caloric foods in rapidlydeveloping countries drastically increased food prices(Mitchell 2008). Soaring food prices were accompaniedby social unrest leading, in isolated cases, to riots inseveral countries (Brown 2008). This has generated whatmight be termed a “dress rehearsal” for the possibleconsequences of the precarious future of world foodsecurity. Two trends are driving humanity to a seeminglyunavoidable food crisis that is virtually not acknowledgedin its impact and severity. Population increase continues ata pace that will add some 2.5 billion people by the year

2050 to the 6.5 billion already on the planet. Second andcompounding the problem is that people in developingcountries are successfully crossing into a middle classstatus, accompanied by increases in per capita caloric use.Information technology also has provided virtually every-one with the means to appreciate the wealth that hadpreviously been reserved to a few and to now seekparticipation. This almost invisible crisis is greatly over-shadowed by the inevitable energy crisis which isdemanding solutions, even when the detection andexploration of new fossil fuel sources will postpone theunavoidable eventual decline. That it even could beconsidered to use food to produce energy in a worldwhere almost 1 billion people are undernourished speaksof insane, inconsiderate objectives. The lessons of 2007should be heeded, viz, that increased energy supply cannotrely on food biomass (Patzek 2007).

The problem of the first generation ethanol biofuels fromcorn can be readily assessed from the statistics in energyconsumption [Key World Energy Statistics, 2009, Interna-tional Energy Agency]. The energy consumption per capitaper year in developed countries, e.g., USA is 7.75 ton of oilequivalent (TOE), which corresponds to 212,330 Kcal/ca/daybased on 2007 energy consumption statistics. Even mid stagedeveloping countries such as Korea, Taiwan, and SaudiArabia consume 125,700, 131,780, and 170,140 Kcal/ca/day, respectively. Average global everyday food consumptionper person is about 2,400 Kcal/ca/day. This demonstrates thatwe are consuming 50–100 times our capacity for total presentfood energy production as the sum of fuel energy sources.Considering the portion of corn in our foods, even accountingfor the fact that corn is mainly utilized for feeding animals formeat production, the first generation biofuel production fromcorn or, indeed, all food, is not a viable option for solving theenergy predicament.

We shall discuss the following considerations about thegeneration and use of biomass as components of theresolution of this crisis: (1) Non-edible biomass must bethe source of any large scale biofuel production that entersthe global supply system (World Development Report2010). (2) Liquid or alcoholic fuels from bioconversionmechanisms can play important roles in areas not connectedto supply grids, where small scale production systems canbe employed to provide energy. However, for advocatingentry into a global industry from cellulosics there aresufficient data suggesting that liquid fuels from renewablesources cannot be produced in an energy-dense andenvironmentally tolerable way (Patzek 2007). Certainly,liquid fuels will have a future for specific purposes, such askerosene used in airplanes, and production systems basedon algal biomass are promising. (3) Combustion rather thanchemical or biochemical conversion to liquid fuels is themore likely successful route to energy production. The gain

94 R.A. Bressan et al.

of energy in such a way is several-fold more efficient thanethanolic fermentation of starch- or cellulose-based fuels(McKendry 2002; Campbell et al. 2009). (4) Finally, weadvocate the generation of new crops, which can be basedon established crops but which can also be found amongwild species (Bressan et al. 2001; Gutierrez and Ponti 2009;Weyens et al. 2009). Generation of these crops should useone of two strategies: transgenic means or breedingprograms that are based on genome information. Especially,we consider as one important answer for improving thegeneration of biomass the engineering or enhancement ofgenes, processes and metabolic pathways that are used byspecies that are naturally adapted to thrive in extremeenvironments (Office of International Affairs 1990; Bressanet al. 2001; Amtmann et al. 2005).

Non-food biomass

In principle, there are two major sources of non-ediblebiomass. One is made up of the non-edible portions ofmajor crop plants, e.g. wheat and rice straw or cornstover (Graham et al. 2007). This practice may, overtime, lead to soils that become depleted in carbon. Thesecond non-food source of biomass, which is substantialand most likely to provide an economically advanta-geous route, are specialty crops with large biomassyields in environments less suitable for extant crops.Whereas we foremost consider land areas here, generat-ing biomass or useful chemical compounds, such aslipids, from aquatic systems is another option. Harness-ing the productivity of the sea may be of importance inthe future. For example, unicellular algae in ponds, orocean-based macroalgal farms, have been proposed asviable biomass/energy sources and pharmaceutical pro-duction areas (Beer et al. 2009).

An important resource is also the biomass that mayconceivably be produced from the vast areas of land that isagriculturally of low quality because it is characterized bystressful environments to which our crops have never beenadapted through breeding. When we point to the potentialproductivity of marginal lands, we are not picturing theextension of agriculture to untouched valuable ecosystemsbut to areas that have been degraded by agriculture in thepast. Areas in this category can be found in sub-tropical andtropical climate zones across the globe, in the African Sahelzone, central Asia, and indeed also in the Americas northand south. Such degraded, low productivity land isincreasing world-wide. In this sense we are advocating therecovery of degraded ecosystems using species that arenaturally capable of succeeding in such environments.There are many regions world-wide where extremophilesmay be grown: in a general sense these would be areas

where subsistence farming is practiced with minimal gainsand high frequency of disastrous harvests that requireinternational support efforts. A world with nine-billionhumans will have to organize the globalization of how togrow energy crops while providing food to those who growthese crops. While irrigation is not strictly excluded, weenvision non irrigation as the environmentally prudentproduction scheme that optimizes greening of degradedlands in a sustainable way.

This potentially useful biomass has received littleattention. Only recently, attempts have been initiated byorganizations such as CIMMYT to generate from high-yielding lines of maize the progeny that may be useful indrought-prone areas of Africa (Messmer et al. 2009). Ratherthan adapting existing crops, generating alternative cropsthat could be used strictly for biomass production onmarginal soils in stressful environments has been proposedbefore with, for various reasons, little resonance (e.g.,Odum 1974; O’Leary 1984; Glenn and O’Leary 1985;Mizrahi and Pasternak 1985; Hendricks and Bushnell2008). It is time to reconsider. Table 1 lists species growingwell under highly stressful conditions and includes data onbiomass or seed/fruit yields, although in many cases thedepth of the information is not sufficient. Conditions, forexample salinity or aridity, under which these species weregrown were often not recorded in sufficient detail. Unlikethe well known fresh water crop species from tropic ortemperate zones these species have not or have onlymarginally been improved by selection or breeding. Giventhe plant breeder’s toolbox, now fortified by genomics,such species should be targeted for improvement to convertthem into genuine new crops.

Non-food crops will gain particular importance as theyield of crops for human consumption must be increased,which will probably be achieved by breeding, adaptationand growth of traditional crops on less productive land.Also, the diversion of corn starch to biofuel production willlead to price increases as food or fuel destinations compete.This will generate incentives to grow food crops ongenerally unsuitable, marginal land that promises at leastsome return for farmers, although the potential forincreased destruction to environments exists. Such areasrepresent prime regions for non-food crops, in particular forspecies, as we shall outline below, that are adapted totolerate abiotic stresses in areas that are often nutrient-pooras well as because scarce coverage by plants has notenriched the soil.

Liquid fuels for transportation and energy

We find it remarkable that liquid biofuels should bepromoted as the most desirable portable fuels by present

Stress-adapted extremophiles provide energy without interference 95

research strategies (National Academy of Sciences 2008).An examination of the energy conversion efficiencies castsserious doubt on the benefits claimed (McKendry 2002).Comparing the combustion of biomass in power plants withthe production of ethanol or other liquid energy reveals astrikingly greater efficiency in favor of combustion inelectric power generation (McKendry 2002; Patzek 2007;Campbell et al. 2009). Stored electric power, for examplewhere depleted batteries may be exchanged for charged

ones at “gas” stations, is as portable as the advertisedalcohols in almost all transportation uses.

We point out the advantage of combustion now in thecontext of allowing much greater advantage to the use ofstressful environments for biofuel production. In addition,biomass “waste” accumulating in production agriculturescenarios, for example the fraction of corn stover that is notbetter returned to the soil, or various cellulosic materialsand even household wastes, may be utilized with no or little

Species Yield References

Biomass species mt .ha−1 year−1

1 Acacia spp. 13.00–14.00 Singh and Toky 1995

2 Agave spp. 38.00–45.00 Nobel 1991a

3 Albizia lebbek 5.30–20.20 Kawahara et al. 1981

4 Arundo donax 45.00–51.00 Williams et al. 2008

5 Atriplex spp. 12.60–20.90 Aronson et al. 1988

6 Batis spp. 13.60–17.90 Glenn and O’Leary 1985

7 Beta spp. 42.00–55.60 Kaffka and Hills 1992

8 Casuarina spp. 17.42 Goel and Behl 2005

9 Distichlis spp. 30.00–40.00 Dakheel et al. 2008

10 Eucalyptus spp. 21.00–29.00 Singh and Toky 1995

11 Juncus spp. 0.96–44.00 Cleark and Jacoby 1994

12 Leucaena spp. 25.00–33.00 Singh and Toky 1995

13 Miscanthus spp 18.00–48.00 Petyr et al. 2008

14 Opuntia spp. 31.00–41.00 Nobel 1991b

15 Panicum virgatum 11.00–22 .00 Lemus et al. 2008

16 Pennisetum spp. 35.00–45.00 Woodard and Sollenberger 2008

17 Populus spp. 2.80–11.40 Laureysens et al. 2004

18 Prosopis spp. 4.00–39.00 El Fadl 1997

19 Salicornia spp. 12.70–24.60 Glenn et al. 1991

20 Sarcocornia spp. 2.02–47.76 Palomo and Niell 2009

21 Sesbania spp. 8.00–21.00 Evans and Rotar 1987

22 Spartina spp. 40.00 Odum 1974

23 Sporobolus spp. 30.00–40.00 Dakheel et al. 2008

24 Tamarix spp. 5.00–20.00 Biosaline Biomass 2004

Seed/oil yield by species Mg .ha−1year−1 (oil, seed* or fruit)

25 Azadiracta indica 2.67 Azam et al. 2005

26 Balanites spp. 1.60 Deshmukh and Bhuyar 2009

27 Calyophyllum spp. 4.68 Azam et al. 2005

28 Citrullus spp. 1.50–2.10*(seed) Yaniv et al. 1999

29 Elaeis guineensis. 4.00–5.00 Yusoff and Hansen 2007

30 Jatropha spp. 1.50–7.80*(seed) Jongschaap et al. 2007

31 Kosteletzkya spp 1.46 * (seed) Gallagher 1985

32 Moringa spp. 3.50* (seed) Morton 1991

33 Phoenix spp. 12.00 *(fruit) Samarawira 1983

34 Pongamia spp. 0.22–2.25 Karmee and Chadha 2005

35 Salvadora spp. 3.500*(seed) NEDFCL 2002

36 Simarouba glauca 0.90–1.20 Dash et al. 2008

37 Simmondsia chinensis 1.12–2.25 Duke 1983

Table 1 Extremophile species—bioenergy production potential

96 R.A. Bressan et al.

new infrastructure development. It is to be noted that thetechnology of combustion of biomass through whichelectricity can be generated is relatively mature, based onthe current technologies of waste incineration and coalcombustion. In such cases, the significant energy lossduring the process of the conversion of biomass to biofuelcan be minimized. The strategy will have the add-on benefitof being applicable at different scales of power generatingunits. Scaling can also be achieved by using differentenergy production platforms that utilize the biomass, withsmall-scale, local fermentation and biogas production as anoption alongside combustion or solar energy collection inrural areas that are not, or not yet, connected to country-wide electricity grids. Our arguments here include theapproximately one half of crop biomass that is not annuallyconverted into fiber, fruit or seed, and may lead to increasedproductivity and yield when more is returned to the soil.

Novel crops can be found among existing species thatcan provide biomass on marginal land in stressful con-ditions where our favorite crops will not be productive ordie. These species offer several opportunities. First, it is notnecessary that we change these specialists in the evolution-ary race to colonize resource-poor niches into new energycrops. In the combustion model, they are highly suitablebiomass sources already. By using them for energy we alsocan avoid the difficult and time consuming geneticmanipulations needed that would convert them into newagronomically and culturally accepted food or specializedliquid fuel crops. Beyond plant research, what is needed isrelatively modest infrastructure modification and thegeneration of incentives to allow the market to utilize theseEECs. The largest cost, once the infrastructure is in place,both economically and energetically will be for collectingand delivering the non-edible biomass to combustioncenters connected to the electrical grid. Once biomassgenerates electricity, the cost related to the distribution ofelectricity to consumers can be much smaller as comparedto the cost associated with the distribution of biofuels toconsumers.

A second option, which would establish energy cropfarms on marginal land with naturally adapted species, canbe viewed as an extension of the first, albeit on a longertimescale. Selecting and breeding from among the manyspecies that could be used has in the past been viewed aswasteful, as agriculturists have opined that the “useful”species have already been domesticated. The ease withwhich we can now obtain genetic information about wildspecies, and then begin to select for traits that in manycases have already been defined at the gene level, seems toargue for a change. Conventional wisdom about breeding isin need of a revision.

The third option, most important for bioenergy croputilization in a more distant future, will be the design of

transgenic crops. By this, we suggest that species with highbiomass potential be genetically modified to becomeadapted to stressful environments without losing theirvigor. A requirement for the transfer of multiple geneswith precisely structured control regions for tissue- andcondition-specific expression and transcript and proteinstability is within present technological capabilities. Theimplementation of such projects must, however, beremoved from the short-time focus of companies and thewhims of agencies that operate in funding cycles, and bestructured more like the engineering programs of NASA.

Extremophile new crops

Most crops originated from sub-tropical wild species thathave been genetically modified over more than 8,000 yearsby selection for increased yield under favorable environ-mental conditions. Inadvertently, the emphasis on yield hasalso generated lines with moderate stress adaptationcapacity in particular environments but none of our majorcrops can tolerate extreme environmental stresses. Here wewill briefly discuss plants that have evolved to colonizehabitats characterized by the extreme environmental con-ditions of water scarcity, high and fluctuating soil salinityand extreme temperatures (see Table 1). EEC species withhigh productivity in stressful environments exist andprovide vast potential for further improvement becausethey have not been used in breeding and the genesunderlying their extremophile lifestyles have not beenexploited by genetic engineering. They can be productiveeven on marginal soils, with low fertilizer input and littlemanagement intervention. Sustainability and preservationof soil and water resources is an intrinsic advantage ofsuch new bioenergy crops. Species that carry thesecharacteristics in their genetic makeup exist in essentiallyall plant families. However, previous attempts at propa-gating species in this category have focused on generatingharvestable seeds or fruits (O’Leary 1984; Glenn andO’Leary 1985; Glenn et al. 1991; USDA 2002). In contrast,extremophiles have not previously been selected forenhanced total biomass.

Appropriately modified and managed, extremophileplant species that are naturally adapted to grow on marginalland under stress conditions can be exploited. Thecombustible energy obtainable from extremophile species,which additionally would stabilize soils and mitigateclimate degradation, is comparable to that for crop plantson a weight basis. Some wild grasses, some halophyticspecies and xerophytic agaves, for example, generatebiomass comparable to the dry biomass of corn stover(Bogdan 1977; Glenn et al. 1991; Nobel 1991a; Spatari etal. 2005).

Stress-adapted extremophiles provide energy without interference 97

The major problem of irrigated agriculture—salinity

A third problem arises in irrigated agriculture. Irriga-tion is practiced not only in arid and semi-arid landsbut is—depending on water availability and cost—alsoused to increase yields in general. All too oftenirrigation relies on non-renewable (fossil) undergroundwater supplies. Prolonged irrigation and intense agri-culture use lead to increases in soil salinity. This is aninevitable consequence of adding water at the surfacewhile there is no connection to the groundwater table.Erosion, desertification and loss of soil follow. Theworld’s approximately 160 million hectares of irrigatedland, representing about 15% of the farmed area onearth, produce approximately one third of all food. Onethird of that is affected by increasing salinity, requiringcostly intervention to reverse the damage or at leastslow down its progression (Pitman and Laeuchli 2002).Continued use of irrigated farming in places like thesouthwestern U.S. is practiced because financial incen-tives exist in the form of subsidized, artificially low costof water and energy, but rising costs have already led toareas of cropland being abandoned (Global Climate andEnergy Project 2010). Arid lands cannot sustain con-ventional agriculture without jeopardizing food supplyand climate.

Currently, the water used for irrigated agriculture isabout 3000 km3/year. It is estimated that 1000 km3/yearwould be required to produce enough biofuel throughirrigated agriculture to cover 10% of current worldenergy consumption. Clearly, biofuel productionthrough irrigated agriculture does not present itself as aviable option (Falkenmark et al. 2009; Kinzelbach 2009.It appears to us that the only long-term sustainablesolution is to radically change our current agriculturalpractices and grow crops adapted to extreme anddegraded environments. In a more general sense, a largecomponent of energy and food security will require theuse of stress tolerant EECs. These species can becomenew crop species not requiring irrigation, able to grow indegraded soils, such as those with high salinity,tolerating temperature extremes, and thriving underresource-poor edaphic conditions with low inputrequirements.

These will be the future bioenergy crops; chosen fortheir adaptation to inhabit niches that have not beenpreviously in the focus of agriculture. Their modificationand management for highly productive growth on land thattraditional crops cannot use will avoid competition andsupport food security. Many stress-adapted species showhigh photosynthetic conversion efficiency during parts ofthe growing season, and have biochemical adaptations thatincrease water use efficiency (WUE) without compromising

growth. In many regions that are typically viewed as arid,sodic, or nutrient poor, plant species exist that are able toproduce surprisingly high biomass. Altogether theseregions equal or slightly exceed the total area of the world’scultivated regions. To provide some yardstick, regions withhigh productivity numbers have been recorded for temper-ate and tropical aquatic—including moderately brackish—swamps at ~40 metric tons/ha per year (mt/ha x a) withcultivated annual plants at 10–25 mt/ha x a. This comparisoncan be applied to the productivity of the most productivetropical perennial plants and a few crops [e.g. sweet potato] at50–80mt/ha x a, whereas tropical annuals attain 25–35mt/ha xa (Westlake 2008).

Naturally stress-tolerant plants—the untapped biofuelresource

True extremophiles are species that grow on inhospitable,marginal lands where they have to cope with abioticstresses such as drought, temperature extremes or salinityand often combinations of these factors (Bressan et al.2001; Amtmann et al. 2005). Such plants are also expert inwithstanding high irradiation under abiotic stress conditionsthat preclude growth. Extremophiles are efficient scav-engers for nutrients from soils that are degraded or poor(Kant et al. 2008; Vincour & Altman 2005; Wong et al.2006) and should require minimal inputs thus minimizingenvironmental collateral damage, an often cited drawbackof the green revolution (Pimentel et al. 1973; Huang et al.2002).

Extremophile species typically grow slowly, a strategythat provides survival while hedging bets for reproductivesuccess. This yield penalty for growth under stressconditions is often cited as the major obstacle for attemptsto grow desert-adapted species. However, the slow growthphenotype is not a constraining genetic character becausemany extremophiles are able to exhibit rapid and surprisinglysubstantial growth spurts as conditions improve from deadlyfor normal crops to merely stressful. Examples of suchbehavior are legions; some desert plants, for example, achievebiomass productivity under well-watered conditions thatapproach those of currently studied biomass crops (Nobel1991a). A recent documentation of growth habits ofextremophiles compared salt tolerance and growth in theabsence and presence of salt stress in 11 relatives ofArabidopsis (Orsini et al. 2010). Some extremophiles amongthese species, exhibited more rapid growth than Arabidopsisin both stressed and control conditions.

As one example, Nobel (1991a) explored productivityof agaves and cacti grown under cultivation. Theyobserved aboveground biomass productivity of 38 t.ha−1

year−1 under non-irrigated and 45 t.ha−1 year−1 with

98 R.A. Bressan et al.

irrigation for agave species, with the corresponding figures forOpuntia sp. being 31 and 47 t. ha−1 year−1, respectively.These values approximate to 30% of the dry biomass that isgenerated by Miscanthus under well-watered largely stress-free growth conditions (Heaton et al. 2008). Likewise,Salicornia (glasswort), Suaeda (seablite), and Atriplex(saltbush) can provide yields similar to alfalfa grown withfreshwater irrigation. However, comparisons of productivitybetween monocultures and multispecies communities andtheir contribution to future global energy supply haveresulted in widely differing conclusions (Garnier et al.1997; Berndes et al. 2003). Salicornia species, for example,are to some degree already used as crops (Fig. 1) even in theabsence of major breeding efforts.

These and many other examples paraphrase the funda-mental distinction between growth, growth potential, andthe ability to sustain life under stress. Whether by selection,genetic engineering or adapting appropriate changes toagricultural practices, the number of extremophile speciesalready known can provide sufficient genetic material thatcan be harnessed for biomass production, and someextremophile species are already suitable for cultivation.Identification of mechanisms employed by variousextremophiles opens the prospect of using moleculargenetics to merge their tolerance characteristics withengineered or breeding-dependent increases in low-inputbiomass production.

A number of biomass “crops”, potential EECs, arepresently promoted as biofuel raw materials, such asPoplar (Populus sp.; Laureysens et al. 2004), Miscanthus(Miscanthus giganteus, Petyr et al. 2008; Heaton et al.2008), switchgrass (Panicum virgatum, Lemus et al. 2008)or prickly pear (Opuntia sp., Nobel 1991b) and agaves(Agave americana, Nobel 1991a) and, in the tropics,

elephant grass (Pennisetum purpureum, Woodard andSollenberger 2008). To some degree it has been shown thatthese species can be reasonably productive on land that is toopoor for agronomic profitablility or even suitability forsubsistence farming, forcing farmers to migrate, typicallyjoining the urban poor. In addition, some species such aspalms (Elaeis guineensis, Lam et al. 2009) and physic nut(Jatropha curcas, Achten et al. 2007) are productive on lessfertile land producing oil suitable for conversion intobiodiesel (Fig. 2). Oil palm monocultures in southeast Asiaare profitable and have improved living conditions, althoughthe cultivation is already seriously encroaching on bothnatural ecosystems and land that was previoulsy used forgrowing food crops. Such practices are not sustainable in thelong term.

The yield penalty conundrum is also suspect for anotherreason because yield or greater EEC biomass is geneticallycontrolled and can be engineered. Many attempts have, inthe past, been directed towards engineering photosynthesis,viewed as the most basic determinant of “productivity”.There have been only few, if any, yield improvements bythis route. More promising, it seems, will be that we focuson the structure of gene systems in plants with differentlifestyles and, especially, the interaction of genes with theenvironment. Here we point to new data and insights thatindicate how environmental factors can alter gene expres-sion (Jablonka and Raz 2007). Recently a number ofstudies have shown that growth can be altered bycontrolling hormone synthesis, distribution and, especially,the ratios among plant hormones (Bögre et al. 2008). Inessence, the perception by a plant of what is a stressfulcondition and what constitutes tolerable stress that may bealtered without incurring a yield penalty by an environ-mentally imposed factor has no theoretical barrier (Bressan

Fig. 1 Salicornia brachiatacultivation. Plants are grown onsaline soils irrigated withseawater (CSMCR, Bhavnagar,India). The insert shows fruitingplants

Stress-adapted extremophiles provide energy without interference 99

et al. 2001). Such approaches are currently being applied totraditional crops (Bänziger et al. 2006) and to species thatare being promoted as bioenergy crops for biomass-derivedethanol or biodiesel production, such as Miscanthus,switchgrass or Jatropha, when grown under less than idealconditions (Heaton et al. 2008; Petyr et al. 2008).

There are two cardinal issues that demonstrate theunderlying necessity for an extremophile approach tobiomass and energy production. First, utilizing agriculturalland on which food can be grown productively interfereswith the imperative that we must produce enough food for agrowing human population. Second, land not covered byforests and not useful for traditional crops without irrigationamounts, astonishingly, to approximately one third of theplanet’s land mass. These savannahs, dry grasslands,chaparrals and dry deserts, and likewise nutrient-poortropical forests, are increasingly under assault for agricul-tural use. Rapidly increasing demands for food or industrialmaterials from plants continues to increase pressure toconvert these marginally productive regions into areas forcrop production. Without political and technologicallysound alternatives this will happen because human pop-ulations with no alternatives but to rely on subsistencefarming will be forced to take this route. The consequencesof intense individualized farming for food production withcrops that are not truly suitable in these areas are not onlydiscouraging but are potentially environmentally cata-strophic, whether we focus on farming in the rainforestsof Indonesia, southeast Asia, the Amazon, or central Africa.Clearly, a switch to bioenergy crops can free these humanpopulations from poverty and substantially help avoid thedanger of environmental collapse. Likewise, the arid zonesof sub-Saharan Africa, Australia, the southwestern UnitedStates, western China, or the cold and dry vast regions ofcentral Asia and Siberia with their traditionally low

productivity become increasingly endangered by ourinsistence on their use to alleviate inadequate agriculturalproduction in the present arable areas.

Conclusions

The world’s approximately 13 billion ha of land includejust over 10% that are highly suitable for agriculture.However, the area suitable for marginal farming is maybethree times that acreage (Food and Agriculture Organiza-tion of the United Nations 2003). This less suitable farmland, and to some variable degree all land, experiencesabiotic stresses that may become more pronounced, andwill likely become more erratic, in the wake of globalclimate change. Deviation from the long-term mean oftemperature, wind and moisture for a particular area,especially frequent and inconsistent variations, generatesmost certainly the most serious challenge to sustaining cropyield. As early as 1982, Boyer pointed to the high yieldreductions caused by abiotic stresses, and newer studieshave provided evidence that crop yields are still less thanone third of what could be achieved under ideal growthconditions (Boyer 1982; Evans and Fischer 1999). A luciddocumentation of the constraints on productivity in Africanand Asian farming systems documented the problems anew(Waddington et al. 2010). These problems will persist atleast until extant crop species have been optimized topresent and new climates and only if we can add or uncovergenetic resources supporting higher and more stableproduction in variable climates and tolerance of otherabiotic stresses within the genomes of our crops. Thereis near universal consensus that drought is the mostdamaging of the abiotic stresses that requires immediateand determined attention.

Fig. 2 Jatropha curcas planta-tion. Plants are grown on wasteland under semi-arid conditions(CSMCRI, Bhavnagar, India).The insert shows a cluster offruits taken at the location

100 R.A. Bressan et al.

Increasing irrigation, the remedy for combating droughtin past millennia, will not be practical or possible becausewater is either not available or will become too energycostly. Water will become less available for agriculture asurbanization increases. Also, access to fresh water in desertand semi-desert areas of the world is developing into apolitical issue that could become explosive. Water scarcitywill also affect irrigation already in place and using lesswater out of necessity will then accelerate soil salinization. Asthe climate changes, additional challenges for agriculture willfocus on temperature extremes. Although some success inprotecting plants from drought and temperature damage haverecently been reported (Nelson et al. 2007; Rivero et al.2007), overly optimistic predictions seem inappropriatebecause the results so far indicate that fundamental solutionsto the drought problem are not yet at the implementationstage.

“No country is immune to climate change, but thedeveloping world will bear the brunt of the effects,including some 75–80% of the costs of the anticipateddamage” (World Development Report 2010). As theconsequences of the likely changes come into clearer focus,the results of inaction become equally clear, yet still themost apparently efficient remedies are hotly debated. Itseems extremely important and prudent that food cropproductivity must be improved and that should not bediminished by allocating arable land to biomass crops. Inlight of this, crop improvement, whether by transgenicmeans or based on molecular breeding advances, is finallybeginning to attach importance to crops that are betterprotected against the influence of changing environmentalconditions (Nelson et al. 2007; Edmeades et al. 1999;Bänziger et al. 2006; Moose and Mumm 2008; Messmer etal. 2009; Tester and Langridge 2010).

The future we envision assumes that the immediateuse of wild, extremophile plants in small scale applica-tions should go hand in hand with efforts to developagronomically a number of evolutionarily stress-adaptedspecies. These will strictly be reserved for energyproduction on marginal soils, already degraded by“desperation” agriculturists, with minimal impact onimportant ecosystems. It will be essential that the ill-adapted crop species presently used in such areas aregradually replaced. Massive breeding efforts should bedevoted to develop EECs. Also, breakthroughs of therecent past in genomics and improved understanding ofthe regulation of gene and protein expression—includingepigenetic mechanisms that allow plants to respond in aflexible way to environmental challenges (Chinnusamyand Zhu 2009)—must be employed. Genomics-basedselection approaches and transgenic modifications thatallow transfer of mechanisms from EECs into species withhigh biomass productivity will be required.

Solar efficiencies will have the final word on theproblem. Solar energy irradiation of the earth’s surfaceamounts to approximately 5.7×1024 J on an annual basis.Photosynthetic organisms as a group utilize this energy infixing CO2 at ~2×1011 t/year (3×1021 J/year), whereasamounts consumed by humans are ~3×1020 J/year (Hall1979), representing only 10% of the energy convertedduring photosynthesis. The typical photosynthesis efficien-cy of plants is well below 1%. Compared to that value, theefficiency of advance solar photovoltaic (PV) cellsapproaches or exceeds 40%. Even the emerging PV cellssuch as dye-sensitized or organic cells that could reason-ably compete economically with current electricity produc-tion show efficiencies higher than 6% at least for researchcells (Best Research-Cell Efficiencies, National RenewableEnergy Laboratory 2007). It seems clear that in the longterm utilization for primary energy production will moveaway from bioconversions. We advocate that ethanolproduction should be the first to find replacement, whereasother bioenergies such as localized biogas generation canbe sustained. More efficient physical-chemical processesand more direct solar energy-based sources will eventuallybe required.

Biofuels have served as the primary energy source fromantiquity. All advances of human civilization have beenbased on biofuels, as new sources were found and newmethods were developed for utilization. Non-biologicalsources, such as photovoltaics, wind, wave, or geothermaland other technological solutions are becoming competi-tive. As a consequence, better engineered, efficient biofuelresources will become integrated and adapted to particularlocations and conditions on a local scale. Bio-methane,even bio-alcohols, will find their proper role in a futureeconomy designed to place prime importance on environ-mental sustainability. In such a scenario the use of EECscan provide significant input in a way that contributes tofood security and also protects important natural ecosys-tems. However, implementation of these approaches shouldbe carefully restricted so as not to contribute or generateadditional population pressure, poverty or further incomeimbalances, food shortage and excess, and land use andabuse. This energy crop production should be viewed asreplacing poorly adapted cash crops or even subsistencecropping where economically viable supply and marketinginfrastructures are available. Otherwise extremophiles thatprovide specialty products such as high value oils, otherhigh energy products and localized bio-energy should begrown. Increased water use and energy requirements alsorequire global economic and political adjustments; asdiscussed by the ‘tragedy of the commons’ parable,solutions have no strictly scientific remedy (Hardin 1986).Even for those who see the future with respect to energyand food with less certainty, and perhaps with more

Stress-adapted extremophiles provide energy without interference 101

optimism, than our analysis suggests, a focus not just on theimmediate future but on the long run is of paramountimportance.

Epilogue

by a cherished friend and colleague, Lowell S. Hardin,economist and architect in the debate leading to theoriginal green revolution (Meetings that changed theworld—Bellagio 1969: The green revolution. Hardin2008).

“In the 1960s when the thrust to increase food cropproductivity in Asia was launched, serious scholars heldthat famine was inevitable. They were wrong. Theproduction acceleration campaign succeeded. By 1975India and Pakistan had increased food crop production sogreatly that they were self- sufficient. This unpredicted andunprecedented phenomenon came to be known as the greenrevolution. It was based on the application of strategies andtactics that had earlier brought about the agriculturalrevolution in the United States and Europe. While plantbreeding, and improved production technologies includingirrigation were involved, the green revolution had anotheressential but little recognized component. That was incen-tive policies formulated and administered by supportivegovernments. These often included subsidies on inputs(seed, fertilizer, irrigation water) and guaranteed prices forthe product (price supports, public acquisition programs).

Given today’s even more complicated food and energysecurity situation than existed during the food crisis of the1960s, it is apparent that the strategies and tactics employedto generate the green revolution are not in themselves equalto the challenge. They need to be employed to their fullproductive potential. But given the looming possibility (ifnot probability) that the world may face a very tight supplyof crop land and water with an ever-tightening food andenergy situation, additional strategies such as the one setforth here command accelerated investment in research andtesting. Determining the technological and economicpotential of generating energy from biomass produced withstress-adapted extremophiles is an insurance strategyhelping make the future less insecure. For this to occur, aswith the green revolution, incentive policies (long-termresearch support, public-private partnerships) must beformulated, adopted and implemented.”

The outline provided here points towards the use ofmarginal lands and lands destroyed by irrigation over manycenturies for the “cultivation” of naturally stress-adaptedspecies, which could over time be converted into energycrops. While the policies for such an undertaking aremissing, developing such policies, and their implementation

through long-term support by international organizationsand/or foundations can be imagined.

Acknowledgments Our work has been supported by funds fromKing-Abdullah-University for Science and Technology of SaudiArabia, by the World Class University Program (Korea, R32–10148), by the Biogreen 21 Project of the Rural DevelopmentAdministration (Korea, 20070301034030), and by University ofIllinois and Purdue University institutional support.

References

Achten, W. M. J., Mathijs, E., Verchot, L., Singh, V. P., Aerts, R., &Muys, B. (2007). Jatropha biodiesel fueling sustainability.Biofuels, Bioproducts and Biorefining, 1, 283–291.

Amtmann, A., Bohnert, H. J., & Bressan, R. A. (2005). Abiotic stressand plant genome evolution. Search for new models. PlantPhysiology, 138, 127–130.

Aronson, J. A., Pasternak, D., & Danon, A. (1988). Introduction andfirst evaluation of 120 halophytes under seawater irrigation. In E.E. Whitehead, C. F. Hutchinson, B. N. Timmerman, & R. G.Varady (Eds.), Arid lands today and tomorrow: Proceedings ofan international research and development conference (pp. 737–746). Boulder: Westview.

Azam, M. M., Waris, A., & Nahar, N. M. (2005). Prospects andpotential of fatty acid methyl esters of some non-traditional seedoils for use as biodiesel in India. Biomass and Bioenergy, 29,293–302.

Bänziger, M., Setimela, P. S., Hodson, D., & Vivek, B. (2006).Breeding for improved abiotic stress tolerance in maize insouthern Africa. Agric Water Management, 80, 212–224.

Beer, L. L., Boyd, E. S., Peters, J. W., & Posewitz, M. C. (2009).Engineering algae for biohydrogen and biofuel production.Current Opinion in Biotechnology, 20, 264–271.

Berndes, G., Hoogwijk, M., & van den Broek, R. (2003). Thecontribution of biomass in the future global energy supply: areview of 17 studies. Biomass and Bioenergy, 25, 1–28.

Best Research-Cell Efficiencies. National Renewable energy Labora-tory, 2007.

Biosaline Biomass; Energy for the Netherlands in 2040 (2004) Reportto SenterNovem. J. Hoek (eds.), Ocean Desert Enterprises.

Bogdan, A. V. (1977). Tropical pasture and fodder plants. London:Longman.

Bögre, L., Magyar, Z., & Lopez-Juez, E. (2008). New clues to organsize control in plants. Genome Biology, 9, 226.

Boyer, J. S. (1982). Plant productivity and environment. Science, 218,443–448.

Bressan, R. A., Zhang, C., Zhang, H., Hasegawa, P. M., Bohnert, H.J., & Zhu, J. K. (2001). Learning from the Arabidopsisexperience. The next gene search paradigm. Plant Physiology,127, 1354–1360.

Brown, L. R. (2008). Plan B 3.0: Mobilizing to save civilization. NewYork: W.W. Norton & Company.

Campbell, J. E., Lobell, D. B., & Field, C. B. (2009). Greatertransportation energy and GHG offsets from bioelectricity thanethanol. Science, 324, 1055–1057.

Chinnusamy, V., & Zhu, J. K. (2009). Epigenetic regulation of stressresponses in plants.Current Opinion in Plant Biology, 12, 133–139.

Cleark, P. J., & Jacoby, C. A. (1994). Biomass and above groundproductivity of salt marsh plants in south eastern Australia.Australian Journal of Marine & Freshwater Research, 45, 1521–1528.

102 R.A. Bressan et al.

Dakheel, A. A., Hadrami, G. A., Shoraby, S. A., Shabbir, G. (2008). Thepotential of salt tolerant plants and marginal resources in developingan integrated forage-live stock production system. 2nd InternationalSalinity forum. Salinity, water and society- global issues, localaction. [http://www.internationalsalinityforum.org/].

Dash, A. K., Pradhan, R. C., Das, L. M., & Naik, S. N. (2008). Somephysical properties of Simarouba fruit and kernel. InternationalAgrophysics, 22, 111–116.

Deshmukh, S. J., & Bhuyar, L. B. (2009). Transesterified hingan(Balanites) oil as a fuel for compression ignition engines.Biomass and Bioenergy, 33, 108–112.

Duke, J. A. (1983). Handbook of energy crops (unpublished)Available from: URL: http://www.hort.purdue.edu/newcrop/dukeenergy/dukeindex.

Edmeades, G. O., Bolaños, J., Chapman, S. C., Lafitte, H. R., &Bänziger, M. (1999). Selection improves drought tolerance intropical maize populations. Crop Science, 39, 1306–1315.

El Fadl, M. A. (1997). Management of Prosopis juliflora for use inagroforestry systems in the Sudan. University of HelsinkiTropical Forestry Reports, 16, 107.

Evans, L. T., & Fischer, R. A. (1999). Yield potential: it’s definition,measurement, and significance. Crop Science, 39, 1544–1551.

Evans, D. O., & Rotar, P. P. (1987). Productivity of Sesbania species.Tropical Agriculture, 64, 193–200.

Falkenmark,M., Rockström, J., & Karlberg, L. (2009). Present and futurewater requirements for feeding humanity. Food Security, 1, 59–69.

Food and Agriculture Organization of the United Nations. (2003).Application of molecular biology and genomics to geneticenhancement of crop tolerance to abiotic stress. http://www.fao.org/WAIRDOCS/TAC/Y5198E/y5198e00.htm.

Gallagher, J. L. (1985). Halophytic crops for cultivation at seawatersalinity. Plant and Soil, 89, 323–336.

Garnier, E., Navas, M.-L., Austin, M. P., Lilley, J. M., & Gifford, R.M. (1997). A problem for biodiversity-productivity studies: howto compare the productivity of multispecific plant mixtures tothat of monocultures? Acta Oecologica, 18, 657–670.

Glenn, E. P., & O’Leary, J. W. (1985). Productivity and irrigationrequirements of halophytes grown with seawater in the SonoranDesert. Journal of Arid Environments, 9, 81–91.

Glenn, E. P., O’Leary, J. W., Watson, M. C., Thompson, T. L., &Kuehl, R. O. (1991). Salicornia bigelovii Torr.: an oilseedhalophyte for seawater irrigation. Science, 251, 1065–1067.

Global Climate and Energy Project. (2010). Stanford University,http://gcep.stanford.edu/.

Goel, V. L., & Behl, H. M. (2005). Growth and productivityassessment of Casuarina glauca Sieb. ex.Spreng on sodic soilsites. Bioresource Technology, 96, 1399–1404.

Graham, R. L., Nelson, R., Sheehan, J., Perlack, R. D., & Wright, L.L. (2007). Current and potential U.S. corn stover supplies.Agronomy Journal, 99, 1–11.

Gutierrez, A. P., & Ponti, L. (2009). Bio-economic sustainability ofcellulosic biofuel production on marginal lands. Bulletin ofScience Technology and Society, 29, 213–225.

Hall, D. O. (1979). In D. O. Hall (Ed.), Biomass for energy (pp. 1–18).London: UK Section of the International Solar Energy Society.

Hardin, G. (1986). The tragedy of the commons. Science, 162, 1243–1248.

Hardin, L. S. (2008). Meetings that changed the world—Bellagio1969: the green revolution. Nature, 455, 470–471.

Heaton, E. A., Dohleman, F. G., & Long, S. P. (2008). Meeting USbiofuel goals with less land: the potential of Miscanthus. GlobalChange Biology, 14, 2000–2014.

Hendricks, R. C. & Bushnell, D. M. (2008). Halophyte energyfeedstocks: back to our roots. 12th International Symposium onTransport Phenomena and Dynamics of rotating Machinery,Honolulu, Hawaii, 2008.

Huang, J., Pray, C., & Rozelle, S. (2002). Enhancing the crops to feedthe poor. Nature, 418, 678–684.

Jablonka, E., & Raz, G. (2007). Transgenerational epigeneticinheritance: prevalence, mechanisms, and implications for thestudy of heredity and evolution. Quarterly Reviews of Biology,84, 131–176.

Jongschaap, R. E. E., Corre, W. J., Bindraban, P. S., Brandenburg, & W.A. (2007). Claims and facts on Jatropha curcas L. Wageningen,The Netherlands: Plant Research International B.V; < http://www.factfuels.org/media_en/Claims_and_Facts_on_Jatropha.

Kaffka, S. R., & Hills, F. J. (1992). Can feedstock production forbiofuels be sustainable in California? California Agriculture, 63,202–207.

Kant, S., Bi, Y. M., Weretilnyk, E., Barak, S., & Rothstein, S. J.(2008). The Arabidopsis halophytic relative Thellungiella hal-ophila tolerates nitrogen-limiting conditions by maintaininggrowth, nitrogen uptake, and assimilation. Plant Physiology,147, 1168–1180.

Karmee, S. K., & Chadha, A. (2005). Preparation of biodiesel fromcrude oil of Pongamia pinnata. Bioresource Technology, 96,1425–1429.

Kawahara, T., Kanazawa, Y., & Sakurai, S. (1981). Biomass and netproduction of man-made forests in the Philippines. Journal ofJapanese Forest Society, 63, 320–327.

Kinzelbach, W. (2009). Water and Sustainability in a GlobalPerspective. KAUST Inauguration Symposium: Sustainability ina Changing Climate, Thuwal, Saudi Arabia, Sept. 24, 2009

Lam, M. K., Tan, K. T., Lee, K. T., & Mohamed, A. R. (2009).Malaysian palm oil: surviving the food versus fuel dispute for asustainable future. Renewable & Sustainable Energy Reviews, 13,1456–1465.

Laureysens, I., Bogaert, J., Bluest, R., & Ceulemans, R. (2004).Biomass production of 17 poplar clones in a short rotationcoppice culture on a waste disposal site and its relation to soilcharacteristics. Forest Ecology and Management, 187, 295–309.

Lemus, R., Oldham, L., & Crouse, K. (2008). Soil nutrientrecommendations for switchgrass production in Mississippi. In:Annual Meeting Abstracts [CD-ROM]. Southern Plant NutrientManagement Conference State Report, 4–5 November 2008,Olive Branch, MS.

Marris, E. (2008). Water: more crop per drop. Nature, 452, 273–277.McKendry, P. (2002). Energy production from biomass (part 3):

gasification technologies. Bioresource Technology, 83, 55–63.Messmer, R., Fracheboud, Y., Bänziger, M., Vargas, M., Stamp, P., &

Ribaut, J. M. (2009). Drought stress and tropical maize: QTL-by-environment interactions and stability of QTLs across environ-ments for yield components and secondary traits. Theoretical andApplied Genetics, 119, 913–930.

Mitchell, D. (2008). A note on rising food prizes. Policy ResearchWorking Paper 4682, The World Bank, Development ProspectsGroup.

Mizrahi, Y., & Pasternak, D. (1985). Effect of salinity on variousagricultural crops. In D. Pasternak & A. San-Pietro (Eds.),Biosalinity in action: Bioproduction with saline water (pp. 301–307). Dordrecht: Martinus Nijhoff.

Moose, S. P., & Mumm, R. H. (2008). Molecular plant breeding as thefoundation for 21st century crop improvement. Plant Physiology,147, 969–977.

Morton, J. F. (1991). The horseradish tree Moringa pterygosperma(Moringaceae)—A boon to arid lands? Economic Botany, 45, 18–333.

Nelson, D. E., Repetti, P. P., Adams, T. R., Creelman, R. A., Wu, J., etal. (2007). Plant nuclear factor Y (NF-Y) B subunits conferdrought tolerance and lead to improved corn yields on water-limited acres. Proceedings of the National Academy of Sciencesof the United States of America, 104, 16450–16455.

Stress-adapted extremophiles provide energy without interference 103

NEDFCL (Northeast Development Finance Corporation Limited).(2002). http://www.nerdatabank.nic.in/csireconomic.hmt.

Nobel, P. S. (1991a). Achievable productivities of certain CAMplants: basis for high values compared with C3 and C4 plants.The New Phytologist, 119, 183–205.

Nobel, P. S. (1991b). Environmental productivity indices and productiv-ity forOpuntia ficus-indica under current and elevated atmosphericCO2 levels. Plant Cell and Environment, 14, 637–646.

Odum, E. P. (1974). Halophytes, energetics and ecosystems. In R. J.Reimold & W. H. Queen (Eds.), Ecology of halophytes (pp. 599–602). New York: Academic.

Office of International Affairs [OIA]. (1990). Saline agriculture: Salt-tolerant plants for developing countries. Washington DC:National Academy.

O’Leary, J. W. (1984). The role of halophytes in irrigated agriculture.In R. C. Staples & G. H. Toennissen (Eds.), Salinity tolerance inplants (pp. 285–300). New York: Wiley.

Orsini, F., Paino D’Urzo, M., Inan, G., Serra, S., Oh, D. -H., Mickelbart,M. V., et al. (2010) A comparative study of salt tolerance parametersin eleven wild relatives of Arabidopsis thaliana. Journal ofExperimental Botany, 61, 3787–3798.

Palomo, L., & Niell, F. X. (2009). Primary production and nutrientbudgets of Sarcocornia perennis spp. Alpine (Lag).castroviejo inthe salt marsh of Palmones river estuary (Southern Spain).Aquatic Botany, 91, 130–136.

Patzek, T. W. (2007). How can we outlive our way of life? 20th roundtable on sustainable development of biofuels: Is the cure worsethan the disease? Château de la Muette: OECD Headquarters.

Petyr, R., Voigt, T., Heaton, E., Dohleman, F., & Long, S. P. (2008).Growing giant Miscanthus in Illinois. http:/miscanthus.illinois.edu/wpcontent/uploads/growersguide.pdf.

Pimentel, D., Hurd, L. E., Bellotti, A. C., Forster, M. J., Oka, I. N.,Sholes, O. D., et al. (1973). Food production and the energycrisis. Science, 182, 443–449.

Pitman, M. G., & Laeuchli, A. (2002). Global impact of salinity andagricultural ecosystems. In A. Läuchli & U. Lüttge (Eds.), Salinity:Environment—Plants—Molecules. The Netherlands: Kluwer.

Rivero,R.M.,Kojima,M.,Gepstein,A.,Sakakibara,H.,Mittler,R.,Gepstein,S., et al. (2007). Delayed leaf senescence induces extreme droughttolerance ina floweringplant.Proceedings of the National Academy ofSciences of the United States of America, 104, 19631–19636.

Samarawira, V. (1983). Date palm—potential source for refined sugar.Economic Botany, 37, 181–186.

Schmer, M. R., Vogel, K. P., Mitchell, R. B., & Perrin, R. K. (2008).Net energy of cellulosic ethanol from Switchgrass. Procedings ofNational Academy of Science, 105, 464–469.

Singh, V., & Toky, O. P. (1995). Biomass and net primary productivity inLeucaena, Acacia and Eucalyptus, short rotation, high density(energy) plantations in arid India. J Arid Environments, 31, 301–30.

Spatari, S., Zhang, Y., & Maclean, H. L. (2005). Life cycle assessmentof switchgrass- and corn stover-derived ethanol-fueled automo-biles. Environmental Science & Technology, 39, 9750–9758.

Tester, M., & Langridge, P. (2010). Breeding technologies to increasecrop production in a changing world. Science, 327, 818–822.

USDA, NRCS. (2002). Plant Profile for Distichlis spicata (L.) Greene.The PLANTS Database, Version 3.5 (http://plants.usda.gov/).National Plant Data Center, Baton Rouge, LA 70874-4490 USA.

Vincour, B., & Altman, A. (2005). Recent advances in engineeringplant tolerance to abiotic stress: Achievements and limitations.Current Opinion in Biotechnology, 16, 123–132.

Waddington, S.R., Li, X.,Dixon, J., Hyman,G.,&deVicente,M.C. (2010).Getting the focus right: production constraints for six major food cropsin Asian and African farming systems. Food Security, 2, 27–48.

Westlake, D. F. (2008). Comparisons of plant productivity. BiologicalReviews, 38, 385–425.

Weyens, N., van der Lelie, D., Taghavi, S., Newman, L., &Vangronsveld, J.(2009). Exploiting Plant-microbe partnerships to improve biomassproduction and remediation. Trends in Biotechnology, 27, 591–598.

Williams, C.M. J., Biswas, T. K., Black, I., & Heading, S. (2008). Pathwaysto prosperity: second generation biomass crops for biofuels using salinelands and wastewater. Agricultural Science, 21, 28–34.

Wong, C. E., Li, Y., Labbe, A., Guevara, D., Nuin, P., Whitty, B., et al.(2006). Transcriptional profiling implicates novel interactionsbetween abiotic stress and hormonal responses in Thellungiella, aclose relative of Arabidopsis. Plant Physiology, 140, 1437–1450.

Woodard, K. R., & Sollenberger, L. E. (2008). Production of biofuelcrops in Florida: Elephant grass. Gainesvlle: Institute of Foodand Agricultural Sciences, The University of Florida .SS-AGR-297. (http://edis.ifas.ufl.edu).

World Development Report. (2010). Development and climatechange, UNDP-Worldbank, www.worldbank.org/wdr2010.

Yaniv,Z., Shabelsky,E.,&Schafferman,D. (1999).Colocynth: Potential aridlandoilseed fromanancient cucurbit. In J. Janick (Ed.),Prospectives onnew crops and new uses (pp. 257–261). Alexandria: ASHS.

Yusoff, S., & Hansen, S. B. (2007). Feasibility study of performing alife cycle assessment on crude palm oil production in Malaysia.International J Life Cycle Assessment, 12, 50–58.

Ray A. Bressan received aPh.D. in 1975 from ColoradoState University. After a Fellow-ship appointment at the MSU/DOE Plant Research Laboratoryat Michigan State University, hejoined Purdue in 1978 as aprofessor of plant physiology inthe Department of Horticulture.He is now working as a profes-sor and co-director of the PlantStress Genomics Research Cen-ter, King Abdullah University ofSc ience and Technology,Thuwal, Saudi Arabia. He is a

visiting professor at Gyeongsang National University, Jinju, Korea. Heis working on moving academic knowledge into application, with afocus on the mechanisms of abiotic stress tolerance in plants.

Muppala P. Reddy received hisPh.D. degree in Botany fromGujarat University, Ahmadabad,India, in 1985. He worked as ascientist at the Central Salt andMarine Chemicals Research Insti-tute (CSIR) Bhavnagar, India,1987-2009, focusing on improv-ing stress tolerance and produc-tivity in crops and wild species,with emphasis on biofuel plants.He was a visiting scientist in theDepartment of Horticulture, Pur-due University, USA, 1996-97and 1999-2000. He serves now

as Director of Greenhouses, Plant Stress Genomics Research Center,King Abdullah University of Science and Technology. His interest is cropand plant improvement for abiotic stress tolerance and productivity.

104 R.A. Bressan et al.

Suk Ho Chung received hisB.S. degree in MechanicalEngineering in 1976 from SeoulNational University and hisPh.D. degree in MechanicalEngineering in 1983 fromNorthwestern University. Heworked as a professor in theSchool of Mechanical and Aero-space Engineering, Seoul Na-tional University during 1984-2009. He is now a professor inMechanical Engineering in KingAbdullah University of Scienceand Technology, and Director of

the Clean Combustion Research Center. His research interests covercombustion, pollutant formation, and laser diagnostics.

Dae-Jin Yun received his Ph.D.degree in Agricultural Chemis-try from Kyoto University,Japan, in 1994. He worked as ascientist at the Center for PlantEnvironmental Stress Physiolo-gy, Purdue University, USA,1994-1998, focusing on stresstolerance mechanisms in plant.He has worked as a professor inthe Department of Biochemistry,Gyeongsang National Universi-ty since 1998. He serves now asthe Director of World ClassUniversity program supported

by the Ministry of Education, Science and Technology, Korea. Hismain research topic is to develop Plant Environmental Biotechnologyfor Climate Change.

Lowell S. Hardin received hisPh.D. from Cornell University,USA, in 1943. During a longcareer at Purdue, he has been ateacher of farm management andHead, Department of Agricultur-al Economics professor, and isnow an emeritus in this depart-ment. From 1965 to 1981 heserved as senior agriculturistwith the Ford Foundation. Dur-ing his tenure there he became aprincipal architect of the world-wide system of thirteen interna-tional agricultural research cen-

ters. His name is also associated with the discussions that initiated thefirst green revolution in agriculture. He is a Fellow of the AmericanAgricultural Economics Association for which he has served assecretary-treasurer, vice president and president.

Hans J. Bohnert received aPh.D. degree in General Biol-ogy from the University ofHeidelberg, Germany, in 1972.After working at the University ofDüsseldorf, Germany, CSIROPlant Industries, Australia, EMBLHeidelberg and Max-Planck-Institute for Plant Breeding, Ger-many, he joined the Department ofBiochemistry, The University ofArizona, USA, in 1983. In 2001he moved to the University ofIllinois, Departments of Plant Bi-ology and of Crop Sciences,

Urbana-Champaign, USA. He also serves as the director of theCenter for Comparative and Evolutionary Genomics. He is avisiting professor at Gyeongsang National University, Jinju,Korea. His interests center on understanding mechanisms confer-ring abiotic stress tolerance in plants.

Stress-adapted extremophiles provide energy without interference 105