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Hindawi Publishing CorporationInternational Journal o Plant GenomicsVolume , Article ID ,pageshttp://dx.doi.org/.//

Review ArticlePlant Domestication and Resistance to Herbivory

Bhupendra Chaudhary

School of Biotechnology, Gautam Buddha University, Greater Noida , India

Correspondence should be addressed to Bhupendra Chaudhary; [email protected]

Received November ; Revised February ; Accepted February

Academic Editor: Peter Langridge

Copyright Bhupendra Chaudhary. Tis is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properlycited.

ransormation o wild species into elite cultivars through domestication entails evolutionary responses in which plantpopulations adapt to selection. Domestication is a process characterized by the occurrence o key mutations in morphological,phenological, or utility genes, which leads to the increased adaptation and use o the plant; however, this process ollowed bymodern plant breeding practices has presumably narrowed the genetic diversity in crop plants. Te reduction o genetic diversitycould result in broad susceptibility to newly emerging herbivores and pathogens, thereby threatening long-term crop retention.Different QLs inuencing herbivore resistance have also been identied, which overlap with other genes o small effect regulatingresistance indicating the presence o pleiotropism or linkage between such genes. However, this reduction in genetic variabilitycould be remunerated by introgression o novel traits rom wild perhaps with antieedant and antinutritional toxic components.Tus it is strongly believed that transgenic technologies may provide a radical and promising solution to combat herbivory as

these avoid linkage drag and also the antieedant angle. Here, important questions related to the temporal dynamics o resistanceto herbivory and intricate genetic phenomenon with their impact on crop evolution are addressed and at times hypothesized oruture validation.

1. Introduction

During speciation in crop plants, many morphologicalchanges evolved in response to continuous selection pres-sure. Such characters are largely governed by genetic andepigenetic changes or are modulated according to ecologicaladaptations. Te transition o wild progenitor species into

modern elite cultivars through domestication entails evolu-tionary responses in which plant populations adapt to humanselection. In response to this selection most plant speciesexhibit marked changes in a variety o phenotypes, mostnoticeably in traits consciously under selection (e.g., ruitsize, yield, and evenness o maturation) []. As Darwin []prooundly recognized long ago, the study o the phenotypic

variation between wild and domesticated plants presents anopportunity to generate insight into general principles oevolution, using the morphologically variable antecedent anddescendant taxa.

An example o how this concept has transormedour understanding is the realization that natural selection

pressure, as well as adaptation under human selection,ofen led to unexpected and unexplained departures rompredicted phenotypes. Tis mainly includes traits such asenhanced yield, enhanced apical dominance, reduced seeddormancy, perennial to annual habit, and relative susceptibil-ity to pathogens, disease, and insect pests [, ]. However, thelatter received the least attention during the process o agri-

cultural evolution. Te term agricultural evolution here,in act, summarizes all o the changes accumulated in anywild plant orm under natural selection, human-mediatedarticial selection (=domestication), and modern breedingpractices (Figure ). From an evolutionary standpoint, thesephenomena may be viewed as novel generators o variationin the tertiary gene pool comprised o domesticated and wildgermplasms (Figure ). Such variations occurred mostly atgenetic level and provide the ability or a given species toevolve in response to the changing environmental conditionsand stress actors [, ]. Notwithstanding the striking dis-coveries o the genetic basis o evolved morphological traitsin crop plants [], relatively little is understood about


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International Journal o Plant Genomics

Modern varieties;molecularplant breeding

(Direct gene

transfer = genetic

transformation)

Primary gene pool

Secondary gene pool

Tertiary gene pool

Wild forms Early cultigens Landraces Domesticates

Plant breeding

(Chromosome-

mediated gene

transfer)

F : An example o cotton (Gossypium) evolution under human selection and contemporary breeding programs. Te modern cropplants are the outcome o recurrent selection on wild orm undergoing through early cultigens and landraces. In conventional and molecularbreeding programs, it is possible to distinguish between primary, secondary, and tertiary gene pools and exchange o hereditary material.Each primary gene pool comprises one domesticated species together with those species with which it readily cross-breeds. Te secondarygene pool includes species that can be cross-bred only with difficulty. Te tertiary gene pool comprises those species which can be cross-bredonly by using advanced techniques such as embryo rescue. (Courtesy Jonathan F. Wendel, ISU). Te horizontal bar shows the reduction ingenetic diversity along with domestication steps with the help o dark to lighter shades.

the manner in which gene networks and biological processesare associated with the more susceptible phenotypes o theelite orms.

Regardless o these rapidly accumulating insights, impor-tant questions remain about every stage o agriculturaldevelopment. How did individual crop plants evolve romwild species and acquire agriculturally important traits? Howdo contemporary plant orms achieve diverse evolutionarytrajectories separate rom those o their progenitor(s)? Howdo recently ormed elite accessions o crop plants becomecompromised o different resistance traits? o what degreehas crop evolution via the process o domestication and con-current breeding practices provided a stimulus or sustainableagriculture? Despite the domestication events ollowed bybreeding practices across plant taxa, we do not know whyagricultural evolution is so prevalent or conversely, whycrop evolution is not universal i it coners some adaptive

advantages and promotes species diversication. Nor do weunderstand the dynamics that underlie the transormation owild orms to domesticated orms in cryptic crops such ascotton and corn.

It has been assumed that several agriculturally importanttraits such as resistance to abiotic and biotic stress conditionsdecreased signicantly during evolution. For example, indomesticated accessions o the genusCajanus, reduced levelso resistance have been reported against herbivores [,],bacterial blight [], and ungal diseases []. Among stressconditions, a reduction in drought tolerance, resistance toherbivory and pathogens, is the major threat to crop plants.It is difficult to understand what are the precise genetic

underpinnings are that make a plant species vulnerable todrought, herbivores, and pathogens afer passing through theevolutionary important mechanism o crop domestication?Surprisingly, what is the extent o reduction in resistancetraits across crop plants, i the reduction in any particularresistance trait is proportional to another resistance trait? Teanswer to these questions may not be consistent across planttaxa but may only hold true or a particular plant lineage.Generally, domestication promotes heterozygosity leading tothe more successul variants under selection pressure eitherthrough xed hybridity or by polysomic inheritance. Couldit be assumed that domesticated accessions are in generalmore successul than their wild progenitors? Tis is anexceedingly difficult question to answer, in large part becausesuccess is an ill-dened term that can reer to anything romshort-term prolieration o individuals to long-term effectson lineage diversication. Te susceptible nature o modern

crop plant varieties in comparison to their wild progenitorscould be one o the most apparent consequences o such amegaevent. Or accelerated mutational activity in coresidentgenomes (in case o polyploid crops) in early generations ledto a downgrade in the pathogenic and herbivore resistanceo domesticated plant species. Answering these and otherquestions will require comparisons o wild and domesticatedorms by researchers rom diverse disciplines such as ecology,population biology, and physiology. Unortunately, theseimportant areas o biology have received ar less attentionthan the genetics and genomics o selection [, ]. Never-theless, even in these better-studied areas much remains to belearned, and it is only by moving beyond the idiosyncrasies o


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Wild

Cultivated

(a)

WildCultivated

(b)

Wild AD1

Cultivated AD1

(c)

F : Difference in wild orms and their respective domesticated orms showing the impact o natural selection during evolution anddomestication on phenotypic traits. (a) Evolution o maize; the domesticated maize (up) and wild teosinte (down). eosinte has many lateralbranches, while todays maize is unbranched. (b) Evolution o tomato; the much larger ruit (right) is rom the domesticated Solanumlycopersicum, and the small tomato ruit (right) is rom wild species Solanum pimpinellifolium; and (c) evolution o cotton (Gossypiumhirsutum); the long ber phenotype is rom domesticated cottonG. hirsutum(AD

1) (lef) and small uzzy phenotype is rom the wild species

(right).

a handul o model crop systems that emergent properties oselection can be detected. Tough crop plants are threatenedby many stress conditions, most o the previous research hasbeen ocused on the study o genetic end o resistance toherbivory at the gene expression level, during the process oselection, and at the phenotypic level. Te aim o this paperis to provide a broad, updated entry to the literature as wellas to highlight the major unanswered questions in the eld ocrop evolutionary genetics.

2. Evolution of Crop Plants

A primary concern o agricultural evolution biology is toinvestigate where, when, and how crop plants originated.Vavilovs center o domestication [] has been a valuablehypothesis as to where crops originated and where oursessile, agrarian cultures began. Since then, we have madegreat strides in pinpointing where contemporary domesti-cated orms have arisen and rom which wild species theyare derived (Figure ). It has been believed that modernelite plant varieties with useul characters (mostly hybrids)or sustainable agriculture have been developed through(i) domestication and (ii) ollowing research and breedingactivities that were implemented by scientists and breedersworldwide (able ) (reviewed by [, ]). However, it is

essential to understand which has been the oremost drivelargely in the phenomenon o agricultural evolution.

Te term domestication is ofen used to describe theprocess by which wild becomes stabilized. From the stand-point o morphological transormation, domesticated ormsare by denition wild species with certain traits highlightedunder human selection (Figure ), showing character mod-ications including novel trait ormation and subsequentsegregation, or example, a reduction in grain shattering andseed dormancyin rice [, , ]; an increase in seed and podsize inVigna[]; an increase in ber length and quality incotton [, ]; changes in ruit size and shape in tomato [];increased apical dominance in maize [, ]; and more. As

Darwin recognized [], the study o the phenotypic variationbetween wild and domesticated plants presents an opportu-nity to generate insight into general principles o evolution,using morphologically variable antecedent and descendantin a comparative ramework. Tis approach provides anintriguing perspective on the molecular genetics o human-mediated articial selection. It is thus assumed that strongarticial selection coupled with introgression (=crossingwiththe respective wild relative) could drive the xation o themost benecial genes and their expression regulation in theprocess o crop domestication.

Te domestication process and introgression under mod-ern breeding programs must have served as effective means


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: Some centers o origin o crop domestication and the trait under selection.

Crop Area o origin raits inuenced under domestication Source

Cereals

Rice China

Reduction in grain shattering and seed dormancy; synchronizationo seed maturation; reduction in tiller number; increase in tiller

erectness; increase in panicle branches; Number o spikelets perpanicle; reduction in hull and pericarp coloration and awn length

[,,]

Barley Fertile crescent, and

Israel-Jordan area Reduction in grain shattering; separation o seeds rom hulls []

Wheat Southwest Asia (ertile crescent) Reduction in shattering o grains (nonbrittle rachis);

ree-threshing trait []

Maize Mesoamerica Increased apical dominance; production o seeds in relatively large

numbers [,]

Brassicas

Cabbage Large number o leaves surrounding the terminal bud []

Cauliower Formation o inorescence meristems []

Legumes

Lentil Mesoamerica Seed dormancy []

Vigna Southeast AsiaIncrease in seed and pod size,

nontwining growth habit, loss o seed dormancy, and seeddispersal ability

[]

Pea Southwest Asia (ertile crescent)Indehiscent pods; lack o dormancy

dwarness; less basal branches; large seeds; good seed qualityday neutral owering

[]

Fibers

Cotton Mexico and Peru Fiber length and quality [,]

Vegetables

omato Mesoamerica Fruits size, shape, and structure [,]

Potato Andes and Amazonia Shorter stolons, larger tubers, (ofen) colored and variously shaped

tubers, and reduction o bitter tuber glycoalkaloids []

Squash Mesoamerica increased seed length and peduncle diameter,change in ruit shape and color

[]

to increase the genetic diversity o elite cultivars especiallyollowing the initial domestication bottleneck, and to pro-duce cultivars adaptive to climatic conditions []. But is ittrue or all domesticated crop plants? Can it be assumed thatcereals with divergent genomic backgrounds experiencedone or more domestication events in their evolutionaryhistory? o test this hypothesis, metagenome studies opopulation genetic structures o cereals, other importantmodern taxa and their wild progenitors o known origin,

are required. Instances o multiple independent domesti-cations in cereals do not provide evidence or their clearancestry (e.g., Oryza, Hordeum), and even i their respec-tive wild progenitors were identied, the multiple originso domesticated orms and their ormation would mostlyremain unknown. It has also been assumed that almost allcrop plants have experienced repeated polyploidization ogenomes in their evolutionary history with multiple-oldduplication o ancestral angiosperm (owering plant) genes[]. Polyploidy has inuenced owering plant diversicationand provides raw material or the evolution o novelty byrelaxing puriying selection on duplicated genes. However,ollowing polyploidization, is the ormation o multiple and

independent domesticated orms a synchronized event acrosstaxa? It still remains unclear whether genetic polyploids suchas wheat, unlike rice and barley, must necessarily undergomutation in orthologous loci simultaneously [,]. In act,many domesticated plant orms appear to undergo one ormore mutations in a single gene, and thus the probability oparallel and independent selection o orthologous chromoso-mal regions responsible or the key domestication transitionis expected to be weak.

Domestication could, thereore, include all responses toplant evolution, including genetic and epigenetic effects,as reviewed recently [, ]. What is the postdomestica-tion impact on the genomic architecture o a plant? Tedomesticated orms are expected to undergo many o thegenome-level megachanges both at structural and unctionallevels, such as sequence loss, structural rearrangements, andchanges in the regulatory sequences, respectively [, ].Recent large-scale microarray studies on the comparison owild and domesticated orms o selective plant species con-rmed that global gene expression had been radically alteredby domestication [, ]. Such changes have certainly playedan important role at the evolutionary scale as domesticated


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plant orms are not always achieved immediately, even inrelatively simpler genomes, as reviewed by [, ]; andinheritable changes can only occur ofen through mutationsat genic and/or regulatory levels. For example, a QL (sh)is responsible or the reduction o grain shattering in thewild rice [] and a loss o unction mutation o Vrs in

six-rowed barley []; and a QL is responsible or ree-thrashing character in wheat []. Accordingly, what is thepreerence or such target genes to undergo mutations duringselection process? It is now evident that the genes involved inimportantdomestication transitions arepreerably regulatorysequences whose mutations can generate substantial phe-notypic modications serving as suitable targets or strongarticial selection in the key steps o crop evolution [,].

Regarding the magnitude o the changes that occurredthroughout crop ormation, it appears that breeding activitieso crop plants are relatively o less radical change than theconversion o wild orms to the domesticated orms. I so,will the modern elite varieties derived through hybridizationo two similar domesticated varieties/orms have less evolu-tionary resolution than those derived through hybridizationwith their wild progenitor species? Tis is denitely anaffirmative assertion and has also been validated across planttaxa with reduced genetic diversity in the breeding programs.Tus, what may be the potential risks involved with suchradical loss in the genetic diversity among elite cultivars?It may also develop the weedy competitors o crop plantsas well as their susceptibility to the diseases, pathogens,and herbivores leading to severe crop losses. But is thereany correlation between operative stress condition and theniche o any plant population? Are there sufficient pieceso evidence or relatively less epidemic o any particularpathogen or pest population? Te bewildering possibilityo such prevalence may destabilize the crop productivityas well as subsequent evolution. For example, despite lowcropdiversity among cereals initially, successul introgressiono resistance to abiotic stress conditions, pathogens, andherbivores was deployed to maintain yield. In this scenario,what is the deadline orsuch incorporation o resistance traitsin cropsor sustainableagriculture? Te answeris still unclearbut it may only be possible i (i) domestication, (ii) changerom traditional landraces to modern breeding varieties, and(iii) their over and above decade eld adaptation can workindenitely; or example, maize hybrids in the United Statesnow have a useul lietime o about years,hal owhat itwas years ago [].

Te advent o genomics has brought a bonade improve-ment to thestudy o such regulatory regions andgenerationomolecular and expression data, knowledge, and tools whichcould be applied in modern breeding programs or exploita-tion o genes rom tertiary gene pool (Figure ). o urtherunderstand the genetic basis o domestication, tremendous

variations have been revealed using molecular markers. Forexample, in tomato, the genetic variation present in wildspecies has beeninvestigated intensively orspecic traitsandis being exploited or tomato breeding []. Using DNAtechnologies, the diversity o domesticated tomato is esti-mated to comprise


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domesticated accessions o allopolyploidG. barbadensewiththeir diploid progenitors (G. arboreumand G. raimondii; B.Chaudhary & J. F. Wendel, unpublished) revealed signicanttranscriptional downregulation o resistance-related genes inthe expression phenotype o the domesticated orm. Tis isa clear indication o reduction in herbivore resistance traits

during the domestication o an allopolyploid crop. Sincecotton allopolyploid species carry A and D genomes,derived rom their diploid progenitors [], it may also beargued that such a reduction in herbivory resistance maybe the cumulative reduction occurred during both polyploidormation and domestication. However, ollowing polyploidormation, many duplicated genes undergo transcriptionalbiases and do not behave as simple additive combinations othe parental genomes [], but instead are maintained at theancestral resistance levels at least in the wild orms. Tus, thepossibility o reduction in resistance levels during polyploidormation appears to be minimal and major reductions inresistance levels may have occurred during the domesticationprocess.

Tis lack o additivity in gene expression levels in mostpolyploid cropplants raises several undamental questions onthe consequences o the evolutionary dynamics o resistancegeneexpression ollowing domestication. From a mechanisticstandpoint, what is responsible or nonadditivity in geneexpression, andwhy does this vary so much among resistancegenes and between different genomic combinations? Why dosuchimportant genesrom two diploid genomes demonstratesuch a large disparity in the degree o suppression o the geneexpression phenotype? Also rom an evolutionary point o

view, how does genomic evolution impact resistance geneexpression variation during agricultural evolution (domes-tication ollowed by the breeding practices), and what arethe potential phenotypic effects o each o these sources o

variation?

.. Genetics of Resistance to Herbivory. One o the mostrecent and spectacular revelations in crop plants is the iden-tication o a number o molecular markers, and how thesemarkers could be applied to identiy and track target genesin a marker-assisted breeding program []. Molecularmarkers have also been applied to increase understandingo the mechanistic and biochemical basis o herbivore resis-tance, as shown thoroughly in maize [], mungbean [],potato [], and in soybean []. What are the putative

regulatory genomic components and pathways providingresistance against herbivores, and at incredibly varied levels?Five QLs have been identied in Arabidopsis known toregulate the glucosinolate-myrosinase system controlling thegeneralist herbivore richoplusia ni than specialist eedinginsect Plutella xylostella [] identiedve QLs inArabidop-sis known to regulate the glucosinolate-myrosinase systemcontrolling the generalist herbivorerichoplusia nithan spe-cialist eeding insect Plutella xylostella. Tis demonstrationo the higher levels o genetic variation or resistance to thegeneralist and specialist herbivores has been urther veriedand expanded in several subsequent studies, including onein which several QLs rom consistent resistance sources

or lea eeding insects SWCB and FAW were mapped onand observed to be located on chromosomes , , and incorn. Given the resistance to both o these insects, candidategenes were identied asmircysteine proteinase gene amily[] and the Glossly gene controlling adult to juveniletransition []. Also in soybean, QLs related to herbivory

resistance were identied through meta-analysis, and thelocations o true QLs were deduced with a condenceinterval o% [, ]. Tus, could it be determinedwhethera genetic variant having a particular QL or haplotype oa polymorphism is associated with the resistant traits? ounderstandthis contention, a number o herbivory-resistanceQLs have been tested or nonrandom associations in thepopulations derived rom a cross between resistant andsusceptible parents determining their proportional contri-bution to the phenotype in wide array o crop species [,]. RFLP-based identication o herbivory-resistance QLsin maize revealed their strong association with antixenosis(=a resistance mechanism employed by a plant to deter orprevent pest colonisation) and antibiosis (=an associationo two organisms in which one is harmed or killed bythe other) resistance to corn earworm [, ], and alsoin soybean []. Te herbivory resistance QLs discoveredby Rector et al. [] accounted or most o the genotypic

variance or corn earworm resistance in the susceptible resistant hybrids; however, with some exceptions those couldprobably be addressed later with the help o soybean insectresistance QL database. Will the contemporary catalogueso genome-sequencing projects across plant systems supportthe identication o important herbivory resistance loci? Inresult, it may denitely be assumed that uture analysesbased on whole-genome sequencing data will emphasizeinsect resistant (IR) QLs/IR genes identied earlier throughmarker-assisted selection. Tis will substantially reduce thetime utilized or their adaptive inheritance through classicalor precision breeding. Until relatively recently, amily-basedQL mapping and association mapping were the primarymeans o searching genes involved in crop evolution [].Considering these studies, different chromosomal regionswere identied harboring corresponding QLs involved inthe herbivory resistance phenotype. Because there is a com-plex correlation among different cellular traits consideredimportant or a resistant phenotype, it becomes enormouslydifficult to identiy such specic biochemical constituents.Tis observation suggests that variation in resistance traitsis controlled by intricate genetic mechanisms, a suggestion

urther bolstered by demonstrations o resistance variation inmaize synthetic hybrids, whose genomes have not undergoneany subsequent selection [,,]. Te mode o resistanceis o great evolutionary interest, as it may ofen sporadi-cally disappear under domestication and ollowing breedingpractices [, , ]. So, what are such vital target genes,their chromosomal positions,and putativestructural changesthose cumulatively have inuenced the loss o resistancepotential? Will any type o stochastic mutations in the codingor noncoding regions lead to the differential loss o resis-tance potential among elite cultivars? From an evolutionaryperspective, it could be hypothesized that divergence inresistance potential at the genomic level may also preserve


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an extensive polymorphism, thus retaining additional rawmaterial or subsequent evolutionary tinkering i exploitedunder breeding programmes.

4. Susceptibility to Herbivory and

Acquired Resistance

.. Resistance Genes: Are Tere Patterns?Te domesticationprocess increased a number o important traits requiredor agricultural innovations, though with ew subsides.For example, the nascent crop-orm (representative romindependent domestication events) is more susceptible toherbivores as a result o having ew important resistance loci,o which most were identied rom their wild progenitorspecies. Is such phenotypic transormation under domesti-cation universally advantageous or has accompanied withthe loss o an additional benet? What is the spectrumo consequences o having a set o important genomic loci

selected under human selection? Are the answers to thesequestions consistent among plant lineages and/or betweenindependent and parallel domestication events within asingle species?

raditional views maintain that domestication ollowedby breeding promoted the xation o resistance loci, reerredto as xed heterozygosity []. It was thus suggestedthat inherited heterozygosity at resistance loci is benecial.Modern views also support that introgression o resistanceloci can be advantageous and provide a primary sourceo genes/alleles with new unctions []. However, theidentication o novel germplasm rom the tertiary gene-pool is an enormously difficult task and it takes time orcharacterization. However, an inventive alternative is tocarry out comprehensive genomic exploration o improvedcultivars, primitive domesticated orms, and their wild pro-genitor species or the identication o candidate genesunderlying resistance traits that show evidence o selectionduring domestication. With the latter approach, could therelationship between identied candidate genes with theirphenotypic effects be envisaged? What are the condencelimits to orbid the possibility o the identied genes as alsepositives? Te use o multiple statistical tests can certainlyreduce such misreadings [].

Analysis o a large number o loci underlying resistanceto herbivory in soybean showed that resistance is an outcomeo a mixture o major and minor gene effects and is not

random. Some loci responsible or acquiring resistance toherbivory were underlying within regions having loci orthe resistance against cyst nematode []. Classication odifferent soybean genotypes showing broad resistance hassuggested important loci contributing to active synthesisand accumulation o products to stop (=antixenosis), deter(=antibiosis), and/or administer (or which mechanism isnot readily established) herbivory [, ]. Tree QLsinuencing resistance to corn borer species in maize havealso been identied as overlapping with other genes o smalleffect in regulating the resistance phenotype, indicating thepresence o pleiotropism or linkage between genes affectingresistance and other agronomic traits []. Recently, one

major and three minor QLs in rice have been identied asshowing resistance against green rice leaopper along withdened microsatellites or marker-assisted selection [].However, at present, relatively little is understood about thetemporal dynamics o resistance to herbivory in differentcropplants, and this requires the study o multiple genomes with

the empirical reality o long-term resistance to herbivory.

.. Modern Cultivars Are More Susceptible Tan Teir WildProgenitor Species. Under classical models, plant resistanceto herbivory and pathogens is proposed to be a primary phe-notype mostly available in the wild ancestors. For instance,plant introductions (PIs) in soybean with low agronomicquality have been demonstrated to be resistant against num-ber o deoliating insects [,]. Such models agree with thetheory predicting that domestication occurred by human-mediated exertion through articial selection on a wildspecies, both positive and negative, over hundreds o gen-

erations resulting in the development o cultivable species.In general, wild plant orms resist attack by herbivores andpathogens mainly through constitutive and inducible deensemechanisms []. Te evolution and maintenance o thelatter are now rmly accepted as an integral component o theplant deense mechanism against herbivores. However, thequestion remains when, where, and how induced resistanceis deployed? Based on differences in the signaling pathwaysand spectra o effectiveness, the induced resistance could becategorized into(i) systemic acquired resistance(SAR) occur-ring in the distal plant parts ollowing localized inectionsand (ii) induced systemic resistance (ISR) stimulated by non-pathogenic organisms and is regulated by jasmonic acid andethylene []. During crop evolution (domestication ollowedby breeding practices), besides all evolutionarily relevantinternal costs (genetic or allocation) o induced resistance,what are the other costs that may also be inuencing theresistance phenotypes? Tere has been rapid progress in thedetection o other important components, such as ecologicalcosts, which are the result o a plants interaction with itsenvironment. Tereore, the conceptual separation o geneticand environmental contributions throughout crop ormationwould help in our understanding o induced resistance [,].

I articial selection prevails all through generations atthe genomic level, is the operation o such selection globalor localized? It may be argued that the evolutionary event

such as domestication can affect the sequence variation atwide-reaching loci within a crop plant. In that scenario,what could be the limiting actors responsible or suchproposed genetic erosion in an elite germplasm? Oneexplanation could be that selection in modern breedingprograms instead acts on selected important loci controllinga variety o traits, concluding that selection in either casewould signicantly reduce species-wide polymorphism andmake it more vulnerable to the stressul conditions [].Besides intensive selection in modern breeding programs, thenarrow genetic base is ofen cited as a contributing actor tolow diversity, at least in soybean. Analysis o ragmentsrom genes in our soybean populations showed evidence


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o a reduction in genetic diversity within and around theselected loci creating genetic bottlenecks []. Te reductiono genetic diversity at different loci could result in broadsusceptibility to newly emerging diseases and herbivores,thereby threatening long-term ood and eed security [].One or multiple domestication events in the evolutionary

history o soybean provide a discernible degree o diversitycompensation that is up to a % reduction, eliminatingalmost % rare alleles present in the wild soybean (G.soja), and even appear to undergo signicant change in theallele requency []. Could it be assumed that the mostsignicant loss o diversity in modern cultivars occurredduring domestication, or due to an unusually low level oinitial genetic variability in the wild progenitor, or both?It seems that the major loss o diversity occurred duringdomestication leading to the bottleneck where there was aloss o rare alleles present in the wild orm and landraces.Contrary to classical predictions that loci under selectionpressure may be relatively ree to acquire heritable changes,it has been shown among subspecies o maize and rice thatsingle nucleotide polymorphisms encode radical changesin the regulatory regions preerentially preserved in thedomesticated orms and evolve conservatively [, , ]. Anysuch change can lead to divergence in subgenomic expressioncomponents, or example, in allopolyploid crop plants [].Tose in result may inuence the quantitatively inheritedtraits such as resistance to herbivory. Since wild plant ormshave large genetic diversity that could be exploited orintrogression o important traits in the modern varieties, itmay be assumed that some sources o resistance have beenlef behind during plant domestication. However, it wouldbe relatively difficult or even unsuccessul to introgress suchtraits into modern cultivars because this may increase thepotential o inerior yield through linkage drag as also shownearlier [, ]. Moreover, it will also be difficult becausecrops with antieedants rom wild may have toxicity and anti-nutritional angle. Here the author has a strong opinion thattransgenic technologies may provide a radical solution to theherbivory as these avoid linkage drag and also the antieedantangle.

5. Transgenic Resistance Mediated bythe Expression of Foreign Proteins

.. ransgenic Crops and Resistance to Herbivory. Introduc-

tion o novel oreign genes into crop plants helps breeders toextend their germplasm with novel phenotypic traits. Suchrequired traits are ofen related to the control o abiotic andbiotic stresses, increasing the crop yield and improving theproduct quality, which were hitherto difficult or not possibleto breed using a conventional approach [,]. Given thetoxicity o chemical pesticides, or the past two decades, amajor emphasis has been on the control o herbivory throughmore rational strategies such as Integrated Pest Management(IPM). A component o IPM is the use o naturally availablepesticides suchas plant secondary metabolites and expressiono heterologous proteins. ransgenic crops with a modiedsingle gene developed or herbivore resistance are immensely

benecial in economic, environmental, and health concerns,as recently reviewed [,], and understood to be secondgeneration resistant crops (detailed in next section). Anumber o genes have been discovered which are toxic orantieedant to herbivores and could be o plant or bacterialorigin. A major contribution o herbivory-proo crops is in

the reduction in application o harmul insecticides spraysand subsequent increase in crop yield [,]. For example,transgenic maize event MON developed using a wildtype gene rom bacteriumBacillus thuringiensis (Bt), resistantto corn rootworm, was rst commercialized in the USA in [] and successully grown until recently. In such ascenario, how do we provide a global perspective o thestatus o biotech crops? Te easiest way is to calculate theglobal adoption rates as a percentage o the global areaso principal crops (i.e., soybean, cotton, maize, and canola)in which biotechnology is utilized. Tough, during lastone decade, herbicide tolerance has consistently been thedominant trait, deployment o multiple genes or other traitssuch as resistance to herbivores is becoming increasinglyimportant and most prevalentor sustainable agriculture. Tebest example o thedynamicso thisvery rapidadoptionis thecontemporary biotech maize or stacked traits []. However,at the eld level evaluation, the best-studied resistance to theherbivory phenomenon in the crops is the Btcotton [],which has a documented reduction in pesticide application omore than % in the developing countries, utmost domesti-cated in India [], though results have been very variable.In , . million small and marginal resource armersplanted and beneted rom. mHa oBtcotton, equivalentto .% o the totalarea under cotton cultivation in India. Tecorresponding adoption rate o biotech cotton has also beenincreased globally rom . mHa to . mHa in theyear []. For soybean, the global hectarage o herbicide toleranttransgenics was . mHa, (up by . mHa in ), whichleads this crop to be the largest GM crop grown worldwide[]. Tese examples illustrate two major contributions othe biotech approach to plant breeding: (i) enlarging thegene pool by including novel genes that breeders could notaccess by crossing techniques and (ii) modiying the genesby recombinant DNA technologies to ne-tune transgeneexpression []. Te latterneeds more emphasisand attentionto achieve success in transgenic technologies or improvedtraits in the crop plants.

What controls the level o a oreign gene expressionin genetically modied plants? Any or all o the molec-

ular mechanisms associated with cellular gene expressionmachinery could be involved. Such a denition encompassesan array o molecular mechanisms at the transcriptionallevel including DNA methylation, mRNA decay, and smallRNA-mediated gene silencing or at translational level havingprotein misolding, degradation or other modication, andnuclear/chromosomal context with respect to genomic loca-tion o transgene ofen reerred to as position effect. It isgenerally assumed that because genes o prokaryotic originare expressed poorly in higher organisms, such as plants[, ], certain modications in such genes are requiredin order to achieve optimal expression. Tis may includemodication in the GC content (as plants are comparatively


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GC rich than bacteria particularlyBacillus spp.), and in codonusage [], afer the introduction o regulatory sequencesand polyadenylation signals. Tis act is well supportedwith a signicant increase in the expression o a codon-modiedBt cryAcgene in comparison to the wild-type generom bacterial origin. Subsequently, by modiying codon

usage, removing polyadenylation sequences [], and othermodications in Btgenes, a number o plants have beentransormed against their target pests [, ]. But isthis trueonly or bacterial genes? Can it be assumed that plant-derivedgenes with insecticidal potential [,] such as protease-inhibitors, alpha-amylase inhibitor, lectins, and hemilectinsdo not require any modication or their optimal efficiencyprior to the delivery into other crop systems?

Under eld conditions, reverse effects o transgenics werealso recorded with (i) harmul effect on nontarget insectsand (ii) target insect to develop resistance against insecticidalgenes used. Te rst risk could be addressed by designingthe synthetic genes to target the hypervariable regions otarget insect genes, thereby avoiding their lethal effects onnontarget insect population. However, in the latter case,the potential hazard could only be equilibrated throughachieving very high transgene expression in the transgenicsthrough the system-specic codon usage modication o agene, use o high strength constitutive promoters, positioneffect- based screening o large transgenic population, andollowing reuge strategy to delay the acquired resistancein the pest population. I transgenic technologies are sopromising and successul over conventional breeding, whatare the major constraints that delayed the worldwide cul-tivation o genetically modied (GM) crops? Here, one othe likely explanations may be the inappropriate resistancemanagement strategies deployed so ar or the commerciallyimportant crop plants. For rice, assessment o agriculturalelds or productivity and health effects in China emphasizedsuch issues and highlighted key concerns on policy imple-mentation and resolution o trade barriers [], which mayalso be true globally. Clearly, much remains to be learnedabout such issues, as how should GM crops or herbivoryresistance be synchronized or sustainable agriculture?

.. Next Generation Herbivory-Resistant Crop Plants. rans-genic technologies are undoubtedly important or plantdeense against stresses, and it has also been argued that theyare useul or the incorporation o novel phenotypes into

crop plants. Existing single gene biotech crop studies may beextrapolated to a hypothetical case where ull coverage o alltarget herbivores and plant diseases would be available in agenetic stock. As mentioned previously, biotech maizein USAis the best example o the deployment o stacked multipletraits including Bt genes (one to control the Europeancorn borer complex and the other to control rootworm)and herbicide tolerance (rst commercialized in ) andcontinued to grow in []. However, hints regardinggene pyramiding, exclusively or herbivory resistance, havealso been emerging rapidly in last decade. In rice (Oryzaindica), incorporation o two Btgenes and one lectin geneshowed the control o three major herbivores: rice lea older

(Cnaphalocrocis medinalis), yellow stemborer (Scirpophagaincertulas), and the brown planthopper (Nilaparvata lugens),respectively []. Tis indicates that, in rice, the long-termeffecto multiple geneexpression is an apparentenhancemento the resistance phenotype established by the synergisticeffects o transgenes. Also, two Bt gene-transgenic cotton

showed enhanced protection against Helicoverpa zea in com-parison to the single gene transgenics with any o the twogenes studied []. Evidence rom our research laboratoryon cotton indicates that transgenic stock with two Btgenestargeting two different lepidopteran insects shows signi-cant improvement in the resistance trait against individualinsects than do the respective single gene transgenics (B.Chaudhary and D. Pental, unpublished data). Tis indicatesthat the gene combinations may have played a strong rolein reserving a durable resistance phenotype. Even withoutknowing the comprehensive specic mechanism(s) involved,there is clearly some association between the observation ohigh levels o protection against herbivores and the presenceo multiple genes.

However, or any particular trait such as resistance toherbivores, can only genes rom similar origin be tagged orsynergistic activity? Canit be assumed that genes rom distantorigin be grouped together or increased resistance pheno-type? Te answer lies with the gut anatomy o phytophagousherbivore, which has different binding sites or toxic proteinsthat determine the spectrum o different lethal protein(s)activity and severity and provide clues or the use o diversetoxic genes to introgress herbivory resistance phenotype.Te use o lectins, or example,Galanthus nivalisagglutinin(GNA), withBtgenes is very promising or increased insectresistance, with the ability o GNA to serve as carrier proteinor the delivery o insecticidal proteins (in most cases Bttoxins)[].

What should be the major selection criteria or insectici-dal proteins when used or gene pyramiding? Tis may entail(i) toxic activity against wide spectrum o herbivores and (ii)nonhomology between or among concurrent toxins used. Awell-studied example in second-generation insect-resistanttransgenic plants is the use o novel vegetative insecticidalproteins (VIPs), which are produced byBacillus thuringiensisduring its vegetative growth along with Btcrystal proteins.Unlike Bt crystal proteins known as -endotoxins, VIPsare not parasporal and are secreted rom the bacterial cellduring vegetative growth. Te ull-length toxin gets activatedproteolytically to a core toxin by proteases in the lepidopteran

gut juice [, ]. Since the mode o action, structure,and binding sites o VIPs are different rom Bt toxins inthe insect gut epithelium, their use as potential insecticidalproteins or gene staking is very promising. ransgenic cottonexpressing two insecticidal proteins VipA and CryAb isestimated to be highly effective against two cotton herbivores,Helicoverpa armigeraand Heliothis virescens[]. Hence, itis assumed that enhanced resistance could be achieved byusing two or more effective analogous insecticidal proteins.Gene combination Bt cryAc and snowdrop lectin GNAwere also tested in cotton and showed resistance againstinsect pests Heliothis armigera and Aphis gossypii [].Also, the results rom a comparison between single Bt


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toxin tobacco transgenics and two gene transgenics havingthe Btgene and the cowpea trypsin inhibitor (Cpi) geneshowed the dominance o two gene products with enhancedinsecticidal efficacy against cotton bollworm (Helicoverpaarmigera) []. Further, an evaluation o Bt-Cpi usionprotein was perormed in Brassica oleracea to study the

insecticidal effect o this usion protein on cabbage worm,which showed high activity o trypsin inhibitor, and theoverall strong resistance to the common cabbage worm[]. Te synergistic activity between unrelated genes seems

very promising. Having distinct binding sites o differentBtgenes in the mid-gut o herbivores, novel combinationso such genes have been considered good to be deployedin delaying the evolution o resistant herbivores []. Sincemost o the activatedBt toxinsshare a common three-domainstructure with a similar mode o action [, ], it is possibleto develop a hybrid toxin through domain swapping [,]. ransgenic cotton and tobacco with a hybrid CryECtoxin developed against polyphagus insectSpodoptera lituraresulted in extreme toxicity to all developmental stages olarval development []. Naimov et al. [] constructed ahybridBtgene using truncatedcryBagene as a scaffold andinserted part o the second domain ocryIIagene conerringresistance to both coleopteran and lepidopteran pests. Tesestudies support the assumption that such a novel strategymay provide new avenues or resistance management studiesinvolving multiple transgenes in crop plants [].

Te pyramiding technology has been noted to provideexcellent control o a broad range o herbivores andreinorcesthe argument that developed resistance in selected herbivoresagainst one toxin will still be ully susceptible to other toxinmolecules present in the plants (reviewed by []). I so,is gene pyramiding an enduring strategy or sustainableresistance? Given the insecticidalactivity, it appears very clearthat single gene transgenics in the eld cannot be sustainedwithout an integrated approach []. Such approach willdenitely delay or, with other components o IPM strategies,preclude the possible adaptation o herbivore-populations toresistant transgenic plants.

.. Endogenous Resistance to Herbivores is Prolonged byransgene Stacking. As mentioned above, one strategy todelay the evolution o resistant herbivores is the stackingo multiple Bt genes [, ]. However, major concernswith this approach are (i) limited insecticidal properties o

Btgenes to the target herbivores due to high specicity oBt toxins, (ii) the potential cross-resistance leading to theevolution o resistant herbivores and (iii) the restricted use opossible novel combinations oBtgenes. A possible solutionto the aorementioned problems may be either pyramiding oBtgenes with another transgene having a different mode oaction, as also discussed earlier [], or by pyramidingthe native herbivory resistance genes with selected Bttrans-genes (reviewed in []). In reerence to the latter, Walkeret al. [] identied that when the SSR-based IR-QL con-ditioning corn earworm resistance in soybean was combinedwithBtcryAc gene, it resulted in detrimental effects on thelarval weights, and with the least oliage consumption. With

these results, can it be assumed that the combined effectso endogenous resistance and transgene-based resistanceare additive while having independent mode o action(s)?Genetic modication o cotton with the BtcryAbtransgenewith high terpenoid levels showed more resistance to tobaccobudworm than transgenics with low terpenoid levels [].

However, transgenics developed in susceptible potato withBtcryA gene against Colorado potato beetle larvae exhibithigher or at least similar mortality in the target herbivoresas in the resistant potato line with leptine glycoalkaloids[]. In the latter scenario, a better strategy may be theidentication o IR-QLs with the help o molecular markers,rather than with specic traits or compounds known tobe associated with the resistance phenotype, as was earlierexampled in soybean, cotton, and potato [,,]. Tenative plant resistance is suggested to be advantageous alsoin the controlling o the resistant herbivore populations, asdemonstrated in the case o tobacco budworm, providingthe lethal dose required or resistance management strategy[]. Tus, staking multiple Btgenes along with the exploita-tion o native resistance through marker-assisted breedingwill comprise complementary additive effects amelioratingthe deployment o resistance management practices in theeld.

6. Conclusions

What are the key evolutionary attributes that make theconversion o wild germplasm to crop such a prevalentphenomenon? Are the most important evolutionary prop-erties o modern crop plants due to contemporary breedingeffortsper se, or is domestication, articial selection, just asimportant? In the opinion o a crop breeder, the end prod-uct is warranted by both. Plant breeding o independentlyselected domesticated orms began almost ten thousand yearsago. Gene mutations occurred during selection, polyploidy,or articial or natural hybridization and brought remarkablegenetic variations. For management o stress conditions incrops, do parallel breeding efforts share similar genomicmodications or is it system/event specic, given the like-lihood that different eatures o human-mediated selectionmay predominate among various lineages?

Very important successes during domestication in termso crop yield and quality with other agronomic aspectshave been achieved, but with compromised resistance to the

herbivores anddiseases. All modern crop plants are protectedagainst herbivores by using synthetic toxic chemicals, ashas been the case or many years, and this ofen leads tothe development o resistance in herbivores against suchrequently used chemicals. o circumvent this problem,introgression o important traits rom the wild gene poolhas been perormed through classical breeding, but hasmet limited success due to incompatibility and numerousgenetic and genomic differences among plant orms. Suchprincipal distinctions may be critical, in that the interactionsestablished by the initial conditions propagate rom the timeo initial origin through periods o stabilization and long-term evolutionary outcome.


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Based on the limited number o available examples, whengene transer occurred in the nascent interspecic crosses,genetic engineering techniques had proven useul to over-come such problems. wo potential benets o genetic mod-ication are precise transer o oreign gene sequences andthe evolution o adaptive transgressive traits. wo potential

benets o genetic modication are precise transer o oreigngene sequences and the evolution o adaptive transgressivetraits. Classic plant breeding programs are reinstated or het-erozygosity and thereore may be more likely to experiencelocus-specic linkage with its evolutionary consequences. Incontrast, a transgenic crop plant possesses a greater insertiono multiple alien genic sequences with immediate phenotypiceffect and genetic novelty. Indeed, experimental analysiso genetically modied crops or multiple traits suggeststhat pyramiding o avorable genes or individual trait mayyield a super-crop with high returns. Tus, the breadth orecurrently selected traits in the domesticated plants and thegenetic transormation system together has a major effect onthe creation and retention o evolutionary novelty in the cropsystem.

Acknowledgments

Te author is thankul to Proessor Jonathan F. Wendel andKara Grupp, Iowa State University, USA, or their suggestionsin the preparation o this paper. Te author also thanks theDepartment o Science and echnology (DS), Council oScientic and Industrial Research (CSIR), and the Depart-ment o Biotechnology (DB), Government o India, or thenancial support to carry out cotton research work in thelaboratory.

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