REVIEW

The next green movement:Plant biology for the environmentand sustainabilityJoseph M. Jez,* Soon Goo Lee, Ashley M. Sherp

From domestication and breeding to the genetic engineering of crops, plants providefood, fuel, fibers, and feedstocks for our civilization. New research and discoveries aimto reduce the inputs needed to grow crops and to develop plants for environmental andsustainability applications. Faced with population growth and changing climate, thenext wave of innovation in plant biology integrates technologies and approaches thatspan from molecular to ecosystem scales. Recent efforts to engineer plants for betternitrogen and phosphorus use, enhanced carbon fixation, and environmental remediationand to understand plant-microbiome interactions showcase exciting future directions fortranslational plant biology. These advances promise new strategies for the reduction ofinputs to limit environmental impacts and improve agricultural sustainability.

Our reliance on plants as re-sources is ancient and onlypromises to expand in the fu-ture. Facedwith a growing pop-ulation, estimates suggest the

need for a 70% increase in agriculturalproduction by 2050 and highlightthe parallel challenges of maintain-ing food security, minimizing en-vironmental damage, and managingwater and resource use under shift-ing climate conditions (1). Along withefforts to reduce post-harvest lossesand waste in the food chain, theintensification of agriculture will beessential to increase productivity (2).Precision agriculture, the breedingand genetic engineering of new cropvarieties, and better management ofenergy, fertilizer, field systems, andirrigation inputs will also help tomeet this challenge (2, 3). This growthin global production will come inregions where land and water assetsare either overused or constrained and in de-veloping countries where smallholder farmersdominate (4). Any intensification of agriculturealso risks increased fertilizer use, degradation ofsoil quality, water availability issues, salinization,potential contamination from chemicals, and lossof genetic diversity.The path to increased production requires a

variety of approaches thatminimize inputs, max-imize efficiencies, and limit ecological impact.These goals drive efforts to translate advances infundamental plant biology toward the applica-tion of plants for sustainability. Current agricul-tural technologies require large energy inputs forsoil preparation, irrigation, and the synthesis and

application of fertilizers and pesticides; these pro-cesses also produce greenhouse gases. One routeto reducing those inputs is the development ofplants that more efficiently use fertilizers, removemore carbon from the environment, and main-tain soil and water quality. Are these challengesnew? Not really. The friction between efficientproduction and use of inputs that drive agricul-ture to feed theworld has always been there; thatfriction drove the Green Revolution of the 1960sand continues to motivate innovation and the in-tegration of new technologies to tackle the prob-lem (5, 6). What has changed is the increased rateof population growth and climate change thatwillpush agriculture to the limits in the coming dec-ades, but the tools available to meet these prob-lems have also expanded. Building from a deeperunderstanding of plant genetics, biochemistry,microbiology, chemistry, and systems biology,

plant scientists are working toward the nextgeneration of crops that more efficiently useinputs for growth and mitigate environmentaldamages.

The modern plant engineering toolkit

Since completion of sequencing the first plantgenome in 2000, the increasing amount of dataand the development of new technologies haveaccelerated the discovery and evaluation cycle forplant science (Fig. 1). Cheaper next-generationsequencing and improved computational powerfor data analysis are key for marker-assisted se-lection and quantitative trait locus (QTL)–guidedbreeding (7). The selection of plant traits by usingthese tools accelerates market entry of new vari-eties. These same tools are also essential forstudies of plant-associated microbiomes that areunraveling the interplay between plants, bacteria,and fungi (8). In addition to genomic data, imag-ing technologies now allow large-scale phe-notyping of plant growth and development.

Noninvasive sensors and high-resolution spectroscopy enableimage reconstruction of root andleaf architectures and real-timecapture of mineral and nutrientflow (9). Similarly, monitoringtechnologies, including dronesand satellites, and experimentalsystems, such as free-air concen-tration enrichment facilities thatsimulate altered climate underfield conditions, expand experi-mental trials beyondgrowth cham-bers and greenhouses. Precisionagriculture is also bringing soil,water, and atmospheric chemiststogether with plant scientists tosimulate and anticipate changesacross geographic regions.Along with “big data” that con-

nect genomes, phenotypes, andthe environment, molecular tech-nologies have evolved since thefirst generation of transgeniccrops. A variety of new gene si-lencing andgenomeeditingmeth-

ods offers accuracy not possible with earliermethods (10, 11). Comparative genomics andcomputational modeling of gene and protein net-works are invaluable for mapping control pointsand the fine-tuning of biochemical, signaling,and transcriptional pathways (12, 13). At themolecular level, protein engineering can im-prove activity and generate new functionalitythat extends metabolism. Better techniques forthe introduction of multiple genes and for thetargeting of gene expression to specific tissues,cells, and organelles are also bringing metabolicengineering to new levels of sophistication (14).The pallet of tools withwhich to understand howplants work and interact with their environmentsnow spans from genomes to proteins and metab-olism to agro-ecosystems (Fig. 1). Recent prog-ress highlights how new technologies allowresearch tomove from themolecular to ecosystem

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Department of Biology, Washington University, St. Louis, MO63130, USA.*Corresponding author. Email: jjez@wustl.edu

Organelle, cell, tissue specific expression

Monitoring & field experiment tech

Marker-assisted breeding

Next-gen sequencing

Gene silencing & editing

Protein engineering

Synthetic biology

Pathway/network models

Metabolic engineering

Phenotyping & imaging

Fig. 1. Modern research tools support a cycle of discovery spanningatoms to ecosystems.

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scales to tackle environmental and sustainabilityproblems.

Improving nitrogen use

The success of modern agriculture is largelydue to the availability of fertilizers that pro-vide essential nutrients, such as nitrogen andphosphorus, to plants (Fig. 2). Without nitrogenfertilization, agriculture would support less thanhalf our current population (15). Annually, chem-ical synthesis by means of the Haber-Bosch pro-cess provides ~118 million metric tons of nitrogenvalued at $100 billion, with nearly half of thistonnage applied to wheat, rice, andmaize world-wide (15). TheHaber-Bosch process, which burns3% of the world’s natural gas and contributesthe same percentage to global carbon emissions,mixes nitrogen and hydrogen gas under highpressure (270 atm) and temperature (450°C)with an iron catalyst to generate ammonia, whichis then used in fertilizers. Overuse of nitrogenfertilizers can also disrupt terrestrial and aquaticecosystems. Compared with chemical synthesis,the symbiosis between nitrogen-fixing rhizobialbacteria and legumes, such as soybean, accountsfor <25% of global nitrogen fixation (16). Thedevelopment of plants with improved nitrogenuse would help reduce fertilizer applications,lower energy costs and greenhouse gas emissionsassociated with its synthesis, and help mitigatethe consequences of nitrogen loss into soil andwater sources.Plant nitrogen uptake, assimilation, and stor-

age pathways offer targets for breeding andgenetic engineering of enhanced efficiency (16).For example, transgenic canola overexpressingalanine aminotransferase required 40% less fer-tilizer compared with wild-type plants under low-nitrogen conditions (16). Substantial efforts alsoaim to improve rhizobial colonization of legume

roots (17). This symbiosis provides an oxygen-freeenvironment for nitrogenase, a multisubunit bac-terial metalloenzyme that converts nitrogen intoammonia for the plant (Fig. 2); however, engi-neering nitrogen fixation into nonlegume plantsremains a challenge (18). Introducing nitrogenaseinto plants requires the transfer of the nif genecluster, which encodes multiple nitrogenase sub-units and accessory proteins required for metal-cofactor and subunit assembly and is under highlycoordinated transcriptional control (18). More-over, the oxygen-free environment needed bynitrogenase requires targeted expression in plants.These hurdles have led to investigations of otherplant-microbial interactions that could enhancenitrogen use, such as nonlegume recognitionby Rhizobium, altering plant-mycorrhizal inter-actions, and engineering nitrogen-fixing bacteriathat associate with crops.The signaling pathway required for rhizobial

nodulation in legumes is also involved inmycorrhi-zal fungi associations (19). Because mycorrhizalinteraction is common across plants, dissectingand rewiring the system for nonlegume-Rhizobiumsymbiosis may be possible (19). Likewise, ectomy-corrhizal andarbuscularmycorrhizal associations—in which the extensive fungal hyphae allow forefficient acquisition and delivery of soil nutrients,including nitrogen, in exchange for carbon fromthe plant—are also the focus of intensive research.Ectomycorrhizal fungi associated with plant rootsare critical for overcoming nitrogen limitationand maintaining plant growth (20). Alternatively,nitrogen-fixing endophytic bacteria that formnodule-independent associations with crops andfree-living nitrogen-fixing bacteria, such as Azo-tobacter and Azospirillum, are routinely used asbiofertilizers and could be engineered for en-hanced nitrogen fixation (19). Nitrogen tracerstudies that have used the model grass Setaria

viridis and bacterial inoculants suggest thatthis plant uptakes bacterial nitrogen, but the ef-ficiency and universality of the process is unclear(21). If widespread, engineering of the nif clusterinto bacteria that associate with nonlegume cropsis possible. Experiments demonstrating the trans-fer of nif clusters between bacterial species andsynthetic biology optimization for nitrogenaseexpression have been successful (22). Given thecomplexity of plant-rhizosphere interactions, theapplication of plant-microbe niche engineeringneeds further investigation but could provideways for improving nitrogen use efficiency.There is also the exciting possibility of hybrid

biological-chemical approaches for nitrogen fix-ation. Synthetic nanoparticles as generators offixed nitrogen may be feasible; a cadmium sul-fide nanocrystal/nitrogenase molybdenum-ironprotein hybrid driven by light, instead of ade-nosine triphosphate hydrolysis, was recently de-scribed (23). Whether such nanoparticles can bestable enough to compete with the Haber-Boschprocess or work under field conditions with plantsremains to be explored, but synthesis of ammoniaby using a light-driven catalyst is an intriguingfuture direction that showcases the value of mul-tidisciplinary approaches to sustainability.

Improving phosphorus use

Phosphorus, like nitrogen, is an essential nutri-ent and limits crop growth in nearly 40% of agri-cultural land, but estimates suggest this couldbe as much as 70% (24, 25). Orthophosphate isthe only bioavailable form for plants and is a non-renewable resource obtained frommining. Becauseof its reactivitywith soils rich in ironandaluminumoxides and conversion by soil microbes to formsinaccessible to plants, crops capture <30%of phos-phorus applied as fertilizer. Moreover, phosphateexcesses are a primary contributor to eutrophica-tion. Recent progress toward the development ofplants with improved phosphorus use will helpmaintain supplies of this resource and could limitoveruse (Fig. 2).Traditional breeding and QTL analysis identi-

fied a rice varietywithaproteinkinase [phosphorus-starvation tolerance 1 (PSTOL1)] that acts as anenhancer of early root growth and provides tol-erance to phosphorus deficiency (26). PSTOL1overexpression enhancedgrain yield in phosphorus-deficient soil through altered root architecturethat allows for better nutrient uptake. Variationsin root structure that enhance phosphorusmobi-lization could also be combined with improvedknowledge of key plant-fungal interactions. Forexample, the endophytic fungus Colletotrichumtofieldiae, which associates with Arabidopsisthaliana in the wild, transfers phosphorus toshoots to promoteplant growth and increases plantfertility under phosphorus-limited conditions (27).Complementing these efforts, our molecular

understanding of how phosphorus is sensedwas advanced by the identification of the SPXinositol polyphosphate-binding domain sharedby phosphate transporters, signal transductionproteins, and inorganic polyphosphate polymer-ase (28). This work suggests that association of

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Engineering challenge

Nitrogen fixation

Nitrogen

UptakeAssimilationStorage

Non-legume

Nitrogenase

Nodulation symbiosis

Nodule-free association

Enhanced efficiencyEnhanced root structure

Altered phosphorous form

Signal Nodulation

Rhizobium

Phosphorous

Soil chemistryMicrobes

<30%

Legume

ngha

it

oym

No

Ench

Ni

Nosy

Ec

N

NNodulation

Fig. 2. Improving nitrogen and phosphorus use. (Left) Legume-Rhizobium symbiosis leads to noduleformation and nitrogen fixation. (Right) In nonlegume plants, nitrogen-related pathways are targets forbreeding and genetic engineering. Different strategies for engineering nitrogen fixation are indicated.Most phosphorus is lost, but alterations of root structure and engineered pathways that select forphosphorus forms can enhance efficiency.

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SPX domain proteins with transcription factorsmodulates phosphorus starvation responses. Thereare also efforts to alter the form of phosphorusfertilizer used by plants, with the added benefitof weed control (24). Transgenic plants express-ing a bacterial protein that oxidizes phosphite toorthophosphate can grow with 30 to 50% lessphosphorus input.Moreover, because orthophos-phate does not discriminate between crops andweeds, use of phosphite fertilizer allowed trans-genic plants to grow with up to 10-fold greaterbiomass in competition with weeds than whenprovided with orthophosphate. Deciphering thephosphorus response network in plants prom-ises to reveal new targets for improving nutri-ent use.

Photosynthesis and carbon fixation

As part of terrestrial ecosystems, which sequester~25%of anthropogenic CO2, plants use clean andrenewable processes for removal of this green-house gas: photosynthesis and carbon fixation.The application of modern plant biology ap-proaches toward improving photosynthesisand carbon fixation may provide solutions forcarbon capture and sequestration. Because pho-tosynthesis links sunlight to carbon fixation forthe production of seeds and grains, this will alsoaffect agriculture. Each step—from efficient lightcapture by leaves to the conversion of sunlightinto high-energy compounds to the partitioningof carbon into plant growth and seedproduction—is a target for improvements through breedingand genetic engineering (Fig. 3) (29).Advances in genome data and phenotyping

contribute to understanding how plants adaptto light environment and control leaf anatomyand morphology in sunlight versus shade (30).Such insights can guide the breeding of plantswith improved photosynthesis. Light-capture re-search ranges from themacroscopic to themolec-ular scales. Altering developmental programsthat affect leaf area and geometry would allowlight to penetrate to lower-canopy leaves for max-imizing light-harvesting efficiency (31). Similarly,the discovery of new chlorophylls and strategiesfor altering the structure of light-harvesting anten-na complexes to match photosynthetic efficiencymay extend the spectrum of energy available forphotosynthesis and carbon fixation (32).Ribulose-1,5-bisphosphate carboxylase/oxygenase

(RuBisCO), the entry point for CO2 into theCalvin cycle, is an obstacle for improving carbonfixation. Plant RuBisCO has a slow activation re-sponse and catalyzes an oxygenation reactionthat competes with CO2 fixation. Recent workdescribes the first success in replacing a plantRuBisCO with a more rapid cyanobacterial ho-molog (33). Although the cyanobacterial RuBisCOis faster at CO2 fixation, it is also more reactivewith oxygen. Expression of a subunit from thecyanobacterial carboxysome, a microcompartmentthat excludes oxygen and concentrates CO2, wasrequired for higher fixation rates in transgenicplants (33). Future improvements of photosyn-thetic efficiency by using protein engineeringto reduce RuBisCO oxygenation and to express

carboxysomes and other parts of the cyanobac-terial CO2-concentration machinery are logicalnext steps (33).A more technically demanding approach is

the conversion of plants that use C3 photosyn-thesis to C4 photosynthesis (34). Most plants useC3 photosynthesis with RuBisCO in leaf meso-phyll cells to directly fix CO2. In contrast, C4

plants separate CO2 fixation from the Calvincycle. Making up only 5% of plant species, C4

plants fix ~30% of global CO2. Fixation of CO2

into the C4 acid oxaloacetate occurs in meso-phyll cells, followed by diffusion of oxaloacetateto bundle sheath cells. There, decarboxylation ofoxaloacetate provides CO2 to RuBisCO and theCalvin cycle. The oxygen-free environment en-hances the efficiency of RuBisCO. Evolutionaryhistory suggests that such radical engineering ispossible; C4 plants independently evolved fromC3 plants in 60 different taxa (34). All of the genesand proteins for C4 photosynthesis are known;however, generation of transgenic plants wouldrequire the introduction ofmore than 20 genes—atechnical problem similar to that of engineeringnitrogenase into plants. The more formidablechallenge is how to alter C3 plants for the com-partmentalizationof carbon fixationand theCalvincycle in distinct cell types. As yet, the control of leafcell development and identification of promotersthat target expression to mesophyll versus bundlesheath cells are not well understood.

Water and salinity

Irrigation of agricultural crops accounts for 70%of global fresh water consumption (35). Sustain-able agriculture requires improved plant survivalduring short-term periods without water andmore efficient water use. Although breeding hasaltered flowering time, height, and other traitsthat affect water use, the multigenic nature ofplant drought responses and a lack of naturalvariability for crop drought tolerance have limitedprogress (35). Engineering plants for drought tol-

erance emphasizes the need for systems-levelapproaches that center on molecular controlpoints with broad effects across multiple down-stream targets (Fig. 3).Development of the first commercialized

drought-tolerant plants used a bacterial RNA/cold stress chaperone protein tominimize droughtstress effects on photosynthesis, carbon fixation,and water loss (stomata closure) in early devel-opment of maize (36). Since then, genes andproteins linked to osmoprotectants, the detox-ification of reactive oxygen species producedunder drought stress, and plant hormone systemsthat regulate stomata closure and protein degra-dationhave been engineering targets. For example,expression of trehalose-6-phosphate phosphatase—an enzyme that alters levels of the signalingmolecule trehalose—in maize improved cropyields by 49 and 123% under mild and severedrought conditions, respectively (37). Althoughefforts to improve crop drought tolerance arepromising, the variability of crop cultivars, fieldconditions, and regional weather necessitate con-tinued field studies.In some regions of the world, such as the

tropics, increasingly wetter climates with pro-longed rainfall and severe floods affect farmingwith losses comparable with those from drought(38). In Asia, flooding affects rice with annuallosses of $1 billion in areas dominated by small-holder farms (38). Waterlogged roots and sub-mergence of aerial parts typically kill plants withina week; however, adaptations in certain rice cul-tivars allow for survival up to twice as long. QTLanalysis identified submergence 1 (Sub1) as a me-diator of stress-induced expression of ethylene-responsive transcriptional regulators in rice. Aswith drought, the search for submergence toler-ance traits is identifying key control points inlow-oxygen-sensing and -signaling pathways andregulators of pathways linked to flooding survival(38); however, the extension of such knowledgefrom rice to other crops is just beginning.

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Sunlight Water

Light captureAntenna

Carbon fixationRuBisCO

C3 vs C4 photosynthesis

Plant stress systemsChaperonesOsmoprotectantsHormonesRedox environment

Control point engineeringLeaf architecture

Fig. 3. Improving carbon fixation and water use. Breeding efforts to alter leaves and engineeringof photosynthesis aim to improve the efficiency of carbon fixation. The multigenic nature of water-stress–related pathways requires researchers to target key control points that alter multiple othersteps in various response/protective networks.

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Directly related to crop irrigation and coastalflooding is the problem of soil salinity or sodiumtoxicity. Crop irrigation increases salinity becauseof trace salts in water that accumulate over time.Saline soil conditions affect 7% of land, and nearly30% of irrigated crops suffer from sodium con-tamination (39). The identification of the high-affinity potassium transporters (HKTs), which areselective for sodium and prevent accumulationof this toxic ion in leaves, provides a molecularmechanism for salt tolerance. Natural variationin HKTs is a resource for introducing salt tol-erance into crops. Breeding of a wheat relativewith a HKT gene into durum wheat produces avariety with reduced sodium in leaves and 25%higher grain yield on saline soils (39). Other path-ways involved in salinity tolerance—includingosmoprotectant synthesis, degradation of reactiveoxygen species, and altered signaling systems—are also being explored for the breeding and en-gineering of plants that tolerate growth on salinesoils (40). In addition to excluding contaminantssuch as sodium, plants can serve as environ-mental cleanup tools.

Environmental engineeringfor remediation

All human activity has the potential to createenvironmental contaminants, including organicmolecules from fuel and chemical spills, militaryactivities, agriculture, industry, and forestry andnaturally occurring inorganic contaminants thatare mobilized and concentrated by mining, irri-gation, and geochemical cycles. The use of mi-crobes and plants for remediation dates back tothe Romans and offers noninvasive, cost-effective,and environmentally friendly options to clean upcontamination sites (41). Plants can stabilize, ex-tract, degrade, and/or volatilize organic and in-organic contaminants, and extensive metabolicengineering efforts can improve the remediationefficiency of various pathways (41).Better understanding of plant metabolism is

leading to new approaches for using plants asenvironmental remediation tools. Althoughmanyexplosives, including 2,4,6-trinitrotoluene (TNT),are recalcitrant to degradation, plants can de-toxify TNT to a limited extent (42). Metabolism ofTNT in plants generates a nitro-radical that re-acts with oxygen to form toxic superoxide. Plantswith a knockout of the gene encoding monode-hydroascorbate reductase, which generates thenitro-radical, display enhanced TNT toleranceand may be useful for degradation of explosiveson military sites (42). In addition to knockoutengineering, fine-tuning enzymatic activity canalso tailor plant responses to toxic metals. Di-rected evolution of phytochelatin synthase (PCS),an enzyme that synthesizes heavymetal–bindingpeptides, revealed an unexpected way of improv-ing heavy metal tolerance through the attenua-tion of enzymatic activity (43). A catalyticallyinferior PCS resulted in phenotypic superioritybecause itmaintained cellular redox homeostasiswhile synthesizing peptides for detoxification ofcadmium (43). In addition to remediation ap-plications, plants can also serve as biosensors for

monitoring contamination sites. Introduction ofa fluorescent zinc biosensor into Arabidopsis andpoplar trees demonstrates a useful strategy forthe development of sentinel plants (44). Given thephysical dimensions of many waste sites and theexpense of soil sampling to monitor and definecontamination, improvements in plant-based re-mediation and the development of biosensorscan provide cost-effective tools for environmentalcleanup.

Conclusions

During thepast century, agriculturemovedbeyondthe knowledge of local farmers to become a globalendeavor. Investments in fundamental plant biol-ogy and agriculture revolutionized food produc-tion, but larger problems loom ahead. To meet thechallenges of this century, plant biologists areworking onmany fronts, some highlighted here, tomake sustainability a reality. In this next greenmovement, new technologies and multidiscipli-nary approaches are enabling the translation offundamental plant biology knowledge towardthe reduction of inputs and ecological footprints.Aside from technical hurdles, agro-economics,

the evolutionary constraints of plants, and thepublic perception of plant biotechnology remainissues. Basic science opensmany routes toward asustainable future; however, crops are commod-ities with a narrow profit margin, which cantemper the implementation of new varieties andpractices. Breakthroughs must be useful, makeeconomic sense, and be adaptable to multipleregions and agro-ecosystems worldwide. Morefrequently, the combination of classic breedingand genetic engineering supported by new tech-nologies provides greater options. Natural varia-tion remains essential for plant improvement,but biotechnology can target complicated traitsnot amenable to traditional breeding. This is es-pecially noticeable as efforts shift away from a one-gene-one-trait model toward broader systems-leveltargets, in which key control points that regulatedownstream steps are exploited or combined toregulate multiple pathways. This also highlightsthe potential limits of plant genetics. Moderncrops evolved under “normal” conditions, andthe diversity needed for breeding new traits tomeet changing climate is not always available.Moreover, efforts to improve particular traitsoften ignore combinations of stresses, diseases,and altered inputs. Additional work needs to con-sider multiple simultaneous challenges to plantgrowth and can be aided by the integration oflarge data sets and modeling studies. There isalso substantial progress toward a mechanisticunderstanding of the plant microbiome and howbacteria and fungi work with plants for nutrientmobilization. In particular, recent discoveries onthe relationships between plants and fungi innitrogen (20) and phosphorus (27) may lead toenhancing plant-microbe interactions to mini-mize inputs and environmental impacts. Last,the public perception of plant biotechnology ne-cessitates the continued education of people aboutthe potential, and the limitations, of both breed-ing and genetic engineering.

The coming decades will be an exciting timefor plant biologists with an eye for how to useplants for environmental and sustainability ap-plications. A single look at teosinte and maizeand one sees how adaptable plants can be formeeting our needs. What remains to be seen iswhether we can harness our understanding ofplants to innovate fast enough to meet the chal-lenges poised by 9 billion people in 2050.

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ACKNOWLEDGMENTS

The authors acknowledge support from the NSF (MCB-1157771 toJ.M.J. and DGE-1143954 to A.M.S.). We thank our colleagues forhelpful comments.

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The next green movement: Plant biology for the environment and sustainabilityJoseph M. Jez, Soon Goo Lee and Ashley M. Sherp

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