From Crop Domestication to Super-domestication

Abstract

From Crop Domestication to Super-domestication

D. A. Vaughan1,*, E. Balázs2 and J. S. Heslop-Harrison3

1 National Institute of Agrobiological Sciences, Kannondai 2–1–2, Tsukuba 305-8602, Ibaraki, Japan
2 Agriculture Research Institute, Department of Applied Genomics, Hungarian Academy of Sciences, Brunszvik u2, Martonvasar 2462, Hungary
3 Department of Biology, University of Leicester, Leicester LE1 7RH, UK

 

An open access article from Annals of Botany 2007 100(5):893-901. 

 

Abstract

Research related to crop domestication has been transformedby technologies and discoveries in the genome sciences as wellas information-related sciences that are providing new toolsfor bioinformatics and systems' biology. Rapid progress in archaeobotanyand ethnobotany are also contributing new knowledge to understandingcrop domestication. This sense of rapid progress is encapsulatedin this Special Issue, which contains 18 papers by scientistsin botanical, crop sciences and related disciplines on the topicof crop domestication. One paper focuses on current themes inthe genetics of crop domestication across crops, whereas otherpapers have a crop or geographic focus. One feature of progressin the sciences related to crop domestication is the availabilityof well-characterized germplasm resources in the global networkof genetic resources centres (genebanks). Germplasm in genebanksis providing research materials for understanding domesticationas well as for plant breeding. In this review, we highlightcurrent genetic themes related to crop domestication. Impressiveprogress in this field in recent years is transforming plantbreeding into crop engineering to meet the human need for increasedcrop yield with the minimum environmental impact – weconsider this to be ‘super-domestication’. Whilethe time scale of domestication of 10 000 years or less is avery short evolutionary time span, the details emerging of whathas happened and what is happening provide a window to see wheredomestication might – and can – advance in the future.

 

Key words: Evolution, gene cloning, gene pyramiding, gene duplication, marker assisted selection, QTL, crop wild relatives

 


Introduction

As human societies have evolved so have the plants in the humanenvironment. The transition from gathering wild plants to cultivationinvolved increasing interaction between humans and the plantsthey used. The subsequent genetic changes in these plants resultingin domestication of some of these cultivated species reflectthe genius of early farmers, who were the first plant breeders.The present generation of plant breeders has tools availablethat enable them to be plant engineers. In this article thatoverviews the topic and the range of papers in this SpecialIssue of Annals of Botany on crop domestication, we discusscurrent themes related to the genetics of crop domesticationand crop genepools that are helping to accelerate the transitionfrom plant breeding to plant engineering, from crop domesticationto crop super-domestication.

Cultivated or domesticated plants, when mankind propagates,plants and harvests them, have played significant roles in manyof the advances that pure and applied botanical sciences havemade in the last few centuries. The earliest farmers recognizeduseful genetic variation that could be chosen from the wild,planted, harvested and reselected in order to gradually developimproved populations with a range of desirable traits. The domesticatedforms bore only limited resemblance to their wild ancestorsdue to the selection of domestication genes. Early in the 18thcentury, the first conscious hybridization of plants occurredusing the cultivated ornamental species Dianthus (Phillips, 2006).Knowledge of plant hybridization paved the way for the use byplant breeders of intra- and interspecific hybridization incrop improvement. Mendel's discovery of the laws of genetics,based most famously on his experiments with the domesticatedgarden pea, led to improved understanding of the variation indomesticated and wild species that so impressed Darwin (1859).Subsequently, sophisticated crop breeding programmes were developedthat enabled more efficient introduction of desirable traitsfrom one cultivar to another. Knowledge of the evolutionaryrelationships between crops and their wild progenitors has facilitatedmore efficient exploitation of the genetic resources representedby the wild relatives of domesticated species (for a review,see Hajjar and Hodgkin, 2007). Currently, domesticated cropssuch as rice, maize and tomato are major targets of studiesin molecular genetics. Research on domestication-related traitsis leading to a better understanding of how genetic controlof phenotypic differences is effected. For example, in determiningthe extent to which similar (orthologous) genes are involvedin producing similar phenotypes in distantly related speciesand working out how to transfer desirable genes between speciesthat cannot be hybridized sexually, and then how to controlthe expression of the genes once they are transferred.

Hybridization and selection have both been involved in the originof crops and the process of domestication since early times.Bread wheat, which is a hexaploid (2n = 6x = 42 chromosomes),arose through fortuitous hybridization between tetraploid wheat(Triticum turgidum ssp. dicoccum, 2n = 4x = 28) and diploidgoatgrass (Aegilops tauschii, 2n = 2x = 14), a weed of earlywheat fields. New groups of bananas and plantains developedwhen diploid domesticated bananas (genome AA) spread into therange of wild Musa balbisiana (genome BB), producing the AABand ABB triploids (see Heslop-Harrison and Schwarzacher, 2007).Modern strawberries (Fragaria x ananassa) are a consequenceof hybridization between North American F. virginiana and SouthAmerican F. chiloensis when these hitherto geographically isolatedspecies were cultivated in close proximity in European gardens(Bringhurst and Voth, 1984). Selection, both intentionally byhumans (conscious selection) and as a result of environmentalfactors (natural or automatic selection) has, in most crops,established the traits associated with the domestication syndrome(Hammer, 1984). Weed species have co-evolved with crops andhave been under similarly intense selection pressures. Weedcontrol through agronomy and the better competitive abilityof crops has been continuous over the 10 000 years of agriculture,but weeds still reduce yields and contaminate crops. In rice,changing agricultural practices is leading to the emergenceof new weedy rice forms in the last decade (Cao et al., 2006).Thus, as with the crops, weeds are also evolving rapidly underselection.

Analysis of the genetic, genomic and molecular basis of thetraits selected by early farmers that constitute the domesticationsyndrome in crops, such as loss of seed shattering and increasedorgan size, has been a major focus of much recent research.Profound insights into traits associated with crop domesticationhave resulted from the technologies and discoveries that makeDNA analysis and manipulation possible (for review see Phillips, 2006).These technologies are associated with PCR, development of transgeniccrops and chromosome painting, as well as DNA sequencing andinformation processing. The rapid spread of communication technologiesenable new knowledge to be disseminated at a remarkable speedworldwide and have ushered in global research initiatives relatedto crop genome analysis and related research. These tools havebeen used in various crops for the development of genome maps,QTL analysis, whole-genome sequencing, fine-resolution mappingand gene cloning. These scientific advances have also contributedto crop improvement, with the application of, for example, marker-assistedselection. The use of molecular techniques has provided a rangeof new insights into domestication and its future course.

Fine-resolution mapping and gene cloning of domestication-related genes

Plants have relatively few morphological traits that are controlledby single genes with distinct alleles showing Mendelian segregation– Mendel was fortunate to find seven independent and non-interactinggenes. The development of molecular markers to analyse directlyDNA or gene products has meant that tens of thousands of segregatingpolymorphisms can be analysed in a species. This has made itpossible to locate genes controlling both qualitative and quantitativecharacters very precisely within the genome, understand theirinteractions, and then to study the phenotypic effects of individualgenes or small regions of chromosome in segregating populations(Paterson, 2002; Hancock, 2005; Zhang et al., 2005). In a numberof studies, quantitative trait loci (QTL) affecting differentelements of the domestication syndrome are collocated to thesame locus or the same small chromosomal region, suggestingeither pleiotropy or close linkage of the gene(s) concerned.It can be difficult to distinguish pleiotropy from close linkage(Bomblies and Doebley, 2006) but in this Special Issue, Weeden (2007)gives some examples of pleiotropy in pea; other examples arediscussed below.

Fine mapping of genes has led to the ability to clone domestication-relatedgenes and unravel the molecular basis of domestication-relatedchanges. For example, the two genes that are most importantin relation to spikelet shattering in rice (sh4 and qSH1) havebeen cloned (Konishi et al., 2006; Li et al., 2006; discussedby Sweeney and McCouch, 2007, in this Special Issue). sh4 isthe key shattering gene that distinguishes cultivated from wildrice, while the qSH1 gene controls the difference in the degreeof shattering between some indica and japonica varieties ofrice. sh4 is a transcription regulator and a single amino acidsubstitution results in reduced shattering. For qSH1 a singlenucleotide in the regulatory region of this gene results inthe altered level of seed shattering. sh4 activates the abscissionprocess while qSH1 regulates abscission-layer formation. Sequenceanalysis of sh4 has revealed a single base-pair mutation thatis responsible for non-shattering and this change is the samein both indica and japonica rice varieties (Lin et al., 2007).This result raises doubts about whether Asian rice was domesticatedmore than once, as has been suggested in several recent papers(for a review see Sang and Ge, 2007). In contrast, sequencingand comparing seven loci in wild and landrace barley have providedstrong evidence that barley was domesticated once in the FertileCrescent and a second time between 1500 and 3000 km to the east(Morrell and Clegg, 2007). Analysis of domestication genes acrossdiverse germplasm can resolve questions about where, from whatand how many times a crop was domesticated.

Differences in nucleotide sequence and/or levels of transcriptionof different alleles of transcriptional regulators affect thephenotypes produced by target genes. In wheat, the Q gene ispleiotropic for many domestication traits. The wild-type alleleq is associated with a fragile rachis and grain that does notthresh free of the chaff, whereas the domestication allele Qis associated with a tough rachis and free-threshing grain (Simons et al., 2006).Comparison of the structure and activity of these two allelessuggests that q is transcribed at lower levels than Q and thatthe q protein functions less efficiently than the protein productof Q (Simons et al., 2006). Q is not known in the wild progenitorsof wheat, but human selection post-domestication seems to haveresulted in up-regulation of Q such that Q has more than twicethe effect of q (Simons et al., 2006). Similarly, some of thedifferences in branching and spikelet suppression distinguishingdomesticated maize from wild teosinte and controlled by tb1have been attributed to up-regulation of tb1 in maize (Hubbard et al., 2002).To date, most domestication genes that have been cloned arediverse transcription factors that are usually functional (Doebley et al., 2006;Komatsuda et al., 2007). Thus the role of human selection onwild populations during crop domestication at the gene levelhas been modification rather than elimination of gene function(Consonni et al., 2005; Doebley et al., 2006). This perhapsreflects the relative rarity of mutations leading to new structuralor functional genes and the short time span of crop domestication.

Domestication trait alleles can be found in wild populations


Traits of the domestication syndrome such as loss of seed dispersal,loss of seed dormancy or loss of protection against herbivoresare considered disadvantageous in wild plants (e.g. Crawley and Brown, 1995).These are often recessive alleles so their effects would bemasked in the heterozygotes that make up the bulk of many wildpopulations. However, these recessive alleles become exposedthrough the inbreeding associated with domestication in manycrops.

In maize, pleiotropic effects associated with zfl2 are suchthat selection for increased yield via increases in row numbercontrolled by zfl2 would probably select also for earlier floweringand fewer ears placed lower on the plant (Bomblies and Doebley, 2006).This led Bomblies and Doebley (2006) to suggest that, in general,undesirable secondary effects associated with pleiotropic genescould limit selection for favourable ‘domestication alleles’during early stages of the differentiation of a crop from itswild progenitor. On the other hand, selection for beneficialtraits controlled by pleiotropic genes could result in associatedneutral or even detrimental traits being concurrently selected.This may explain, at least partially, the presence, in wildpopulations, of alleles for traits of the domestication syndromethat apparently evolved prior to domestication and surviveddespite their possibly deleterious effects in the wild. Examplesof this include alleles of the ‘hidden QTL’ fw2·2for increased fruit size in cultivated tomatoes (Solanum lycopersicum)that are also found in the wild cherry tomato (S. lycopersicumvar. cerasiforme; Nesbitt and Tanksley, 2002; Bai and Lindhout, 2007).Alleles of the regulatory locus CAULIFLOWER (BoCAL) in Brassicaoleracea that contribute to, but are insufficient to cause,development of abnormal inflorescence are present in moderatefrequency in wild populations of B. oleracea subsp. oleracea(Purugganan et al., 2000).

A key gene responsible for some differences between maize andits wild progenitor is the teosinte branched 1 (tb1) mutantthat has pleiotropic effects on apical dominance, length oflateral branches, growth of blades of leaves on lateral branches,and development of the pedicillate spikelet in the female inflorescence(Hubbard et al., 2002). In the progenitor of maize, teosinte(Zea mays var. parviglumis ), a tb1 region haplotype with sequencesidentical to that of the major maize tb1 haplotype was found.This result suggested that haplotypes that confer maize-likephenotypes could predate domestication (Clark et al., 2004).Thus, the high-speed evolution represented by crop domesticationcan be the result of strong selection pressures on pre-existingvariation.

Humans caused a major shift in the morphological traits of wildplants by selecting genes of both large effect and small effectto create crops with higher yield of desired product. In azukibean (Vigna angularis) domestication has reduced seed yieldon a per plant basis because farmers have selected determinateplants with larger pods and fewer large seeds per pod than itsprogenitor wild relative (A. Kaga, NIAS, Japan, unpubl. res.).Mathematical analysis of the functional and structural componentsof yield, including harvest index – a systems' biologyapproach – have great potential to indicate future directionsfor selection (Guo et al., 2006). The wild relatives of cropscontinue to be an important reservoir of genes for potentialuse in agriculture. Sometimes, the genes they have furnishedhave had a dramatic effect on yield, as shown by Tanksley and McCouch (1997)and by Cheng et al. (2007) in this Special Issue. Therefore,there is a continued urgency to conserve these wild geneticresources appropriately, both in situ and ex situ, and to characterizethem for future crop improvement.

Orthologues of domestication genes and their action

There are many different families of transcriptional regulatorsin plants and the transcriptional regulators involved in domesticationdiscussed by Doebley et al. (2006) all belong to different families.Within a given family of transcriptional regulators, gene structuremay be sufficiently conserved for similarities to be identifiednot just between genera of the same plant family but betweentaxonomically very distantly related species. Thus, monoculm1in maize shares similarities with LATERAL SUPPRESSOR from Arabidopsisthaliana and tomato (see Doust, 2007, in this Special Issue)and Q in wheat is similar to APETALA2 (AP2) of Arabidopsis (Simons et al., 2006).AP2-like genes appear to have a wide range of roles in plantdevelopment, but Q is so far the only AP2-like gene implicatedin domestication (Simons et al., 2006). One of the genes affectingshattering in rice, qSH1, may be an orthologue of REPLUMLESS(RPL) in Arabidopsis (Konishi et al., 2006). REPLUMLESS is involvedin formation of an abscission layer in the wall of the fruit,whereas qSH1 affects formation of an abscission layer betweenpedicel and spikelet, but Konishi et al. (2006) suggest thatthis difference could be explained by differences in the transcriptionalcontrol of RPL and qSH1. The duplicate genes zfl1 and zfl2 ofmaize are orthologous to the FLORICAULA/LEAFY (FLO/LFY) genesof species of Antirrhinum and Arabidopsis, amongst others (Bomblies and Doebley, 2006).Among the various effects suggested for these genes is the changein phyllotaxy that produces whorled organs during flower development.In maize, zfl2 is the candidate gene for a major effect QTLcontrolling the whorled versus two-ranked arrangement of femalespikelets in maize versus teosinte. FLO/LFY-like genes havenot been reported to affect inflorescence phyllotaxy in anyother species, but Bomblies and Doebley (2006) suggest thata change in expression pattern could have allowed one of theirorthologues to be annexed for a new role in maize.

Rice contains an orthologue of maize tb1, OsTB1, that, likemaize tb1, affects lateral branching (Takeda et al., 2003).Transgenic rice carrying an extra dose of OsTB1 produced manyfewer tillers than normal because of over-expression of OsTB1.A known mutant, fine culm1 (fc1), with enhanced tiller production,mapped to the same locus as OsTB1, suggesting that fc1 is anallele of OsTB1. Sequencing of fc1 showed a deletion generatinga premature stop codon, such that the predicted polypeptideproduct lacked the domain implicated in the DNA binding activityof the class of transcriptional regulators to which tb1 belongs.Takeda et al. (2003) therefore suggest that alterations in theexpression of OsTB1 through dosage effects or use of mutantscould be used to increase or decrease tiller number at willand thereby adapt rice morphology to differing agronomic situations(see also Doust, 2007, in this Special Issue).

In the major oilseed crop canola or oilseed rape (Brassica juncea,B. napus and B. rapa) losses of between 10–50 % of yieldcan occur due to unsynchronized pod shattering (Østergaard et al., 2006)and require extensive management, including spraying with cropdessicants before harvest and windrowing before threshing. Arabidopsishas proved to be a useful model to study the phenomenon, wherea transcriptional regulator, FRUITFUL (FUL), mediates pod dehiscenceby inhibiting expression of genes controlling shattering. Whenthis transcriptional regulator was introduced in B. juncea itwas over-expressed and pods had no shattering. Further fine-tuningof the expression of this gene in canola may enable the requiredlevel of post-harvest shattering to be achieved (Østergaard et al., 2006).Such intentional manipulations to fine-tune gene activity willcertainly constitute super-domestication, where genetics interactswith crop management and agronomy.

Evidently much remains to be learned about the actions of transcriptionalregulators and how they in turn are regulated. Recently, Clark et al. (2006)located a factor or factors controlling the levels of the messageproduced by the transcriptional regulator teosinte branched1 (tb1) in maize, and hence the phenotypic differences betweenmaize and teosinte associated with tb1, to an intergenic regionupstream from tb1. This region consists of a mixture of repetitiveand unique sequences not previously considered to contributeto phenotypic variation. Doebley and Lukens (1998) had earlierproposed that modifications in cis-regulatory regions of transcriptionalregulators would prove a predominant means for the evolutionof novel forms, and the findings of Clark et al. (2006) appearto provide a supporting example. Plant-breeding-related companiesare already looking at the effects of up- and downregulatingall transcription factors in a given genome, aiming to learnmore about the target genes of different transcription factorsand producing a super-domesticate (Doebley et al., 2006), perhapswith more success than gene mutation as a source of Dobzhansky's‘hopeful monsters’.

Effects of selection on domestication genes

Molecular techniques are not just enabling the position of domestication-relatedgenes to be resolved but they can provide information on theeffects of selection and number of generations required fordomestication. By studying nucleotide polymorphism in differentaccessions of a crop upstream and downstream from domestication-relatedgenes, it is possible to determine the extent to which selectionis acting across the genome, the selective sweep (Clark et al., 2004).Positive directional selection leads to reduced variation andlinkage disequilibria in the respective regions (Palaisa et al., 2004).By comparing sequence diversity around a domestication genein the crop and its progenitor, a new view of the processesthat sculptured the formation of the crops species can be attained.By analysis of nucleotide polymorphism around the teosinte branched1 (tb1) gene in a wide variety of maize accessions, it was foundthat human selection acted on the gene's regulatory region andwas not detected in the protein-coding region (Wang et al., 1999;Clark et al., 2004). This was considered to be a consequenceof the high rates of recombination in maize. From the analysisit was estimated that the time taken to domesticate maize wasbetween 315–1023 years (Wang et al., 1999). Studies ofwheat remains at archaeological sites in southern Turkey andSyria, where wheat domestication is believed to have occurred,reveal a gradual change from dehiscent to indehiscent spikelets,suggesting indehiscence took over one millennium to become established(Tanno and Wilcox, 2006). Archaeological remains of rice fromthe lower Yangtze river suggests that rice domestication wasa slow process (see Fuller, 2007, in this Special Issue) andthis is supported by the wild-rice harvesting methods used today,which do not provide a selection pressure for non-shatteringspikelets (Fig. 1). Both molecular and archaeobotanicalstudies suggest a long period of gathering and cultivation precededdomestication for these cereals. While domestication representsrapid change in evolutionary terms, in cereals the transitionin the suite of characters that changed wild populations intodomesticated crops took place over many centuries or millennia.

During domestication, population genetic diversity is reducedas a consequence of selection. Domestication-related genes experiencea more severe genetic bottleneck due to selection than neutralgenes, as discussed by Doebley et al., (2006) and in this SpecialIssue by Yamasaki et al. (2007). Estimates of the severity ofthe genetic bottleneck of domestication based on comparisonof genetic diversity found in their wild ancestors vary considerablyfrom about 80 % in maize (Wright and Gaut, 2005), to 40–50% in sunflower (Liu and Burke, 2006) and as little as 10–20% in rice (Zhu et al., 2007). Polyploid wheats have sufferedtwo bottlenecks associated with the transition from wild wheatand also due to polyploidy. Thus, hexaploid bread wheat hasabout 7 % and 30 % of the nucleotide diversity of its D andA/B genome donors, respectively (Dubcovsky and Dvorak, 2007).Determining how much diversity is lost during the genetic bottleneckof domestication can suggest approaches to future crop improvement,such as tapping high diversity gene sources in wild progenitors(Whitt et al., 2002) or transgenic alteration of expressionof selected genes (see Yamasaki et al., 2007, in this SpecialIssue). Detection of previously undetected domestication-related geneshas become possible using QTL analysis and selective sweepsacross the genome (Yamasaki et al., 2007). This enables hiddendomestication genes to be detected based on the selection profileof comparative sequences. Genomic comparison of crops and theirwild progenitors for hidden domestication-related genomic regionsis a new approach to detecting potentially useful diversityin wild progenitors for crop improvement.


Gene evolution

Genome sequencing has enabled the evolution of domestication-relatedgenes to be elucidated. The wild and domesticated wheat speciesprovide an example. The different domesticated wheat cultigens(cultivated species) evolved from hybridization events betweenwild and cultivated species (to form Triticum aestivum subsp.spelta) or selections from either wild (T. monococcum subsp.monococcum and T. turgidum subsp. dicoccum) or domesticatedspecies (T. aestivum and T. turgidum subsp. durum). In thiswild–domesticated polyploid series the grain-hardnesslocus (Ha) of wheat encodes friabilins that are composed ofthree proteins. The genes Pina, Pinb and Gsp-1 at the Ha locusencode these three proteins. Two of these genes, Pina and Pinb,were eliminated from both the A and B genomes of wheat afterpolyploidization into the tetraploid T. turgidum. In the hexaploid,T. aestivum, Pina and Pinb are present coming from the D genomedonor, Aegilops tauschii. Comparison of the Ha locus in thesame genome in diploid, tetraploid and hexaploid Triticum andAegilops species revealed numerous genomic rearrangements, suchas transposable element insertions, genomic deletions, duplicationsand inversions (Chantret et al., 2005). Genomic rearrangementsat the Ha locus were believed to be mainly caused by illegitimaterecombination, where DNA sequences not originally attached toone another become joined, and this type of recombination isconsidered a major evolutionary mechanism in wheat species (Chantret et al. 2005).The complex evolution of the Ha locus in wheat reflects theremarkably high rate of DNA replacement in wheat genes (Dubcovsky and Dvorak, 2007).

Gene and genome duplication

An area where DNA technologies have had a particular impacton our understanding of domestication has been in relation togene and genome duplication. As well as polyploidy, gene duplicationis a common evolutionary phenomenon in plants (for review seeMoore and Purugganan, 2005). In maize it has been estimatedthat about a third of genes are tandem duplicates due to unequalrecombination or transposition events that have involved genefragments (Emrich et al., 2007). Rondeau et al. (2005) haveshown duplication and subsequent functional specialization ofNADH-MDH genes in some, but not all, grasses with C4 photosynthesis.Among duplicated genes are a class called nearly identical paralogs(NIPs) that appear to be of recent origin. This class of duplicategene shares ≥98 % identity. Many NIPs in maize are differentiallyexpressed. This has lead to the suggestion that the variationin this class of duplicate gene provides new variation thatmay have had a selective advantage during domestication andimprovement of maize (Emrich et al., 2007), and again modellingof plant architecture may suggest routes for crop improvement(Guo et al., 2006).

Reflecting the abundance of polyploids in the plant kingdom,many important crops exhibit both allopolyploidy (e.g. wheat,canola, tobacco, peanut and cotton) and autopolyploidy (e.g.watermelon, strawberries, potato and alfalfa). Allopolyploidyresults in increased allelic diversity while autopolyploidyresults in increased allelic copy number, both of which canlead to novel phenotypes. Since polyploidy is so common in plantsthey must have some selective advantages. Among the presumedmain advantages of polyploidy are fixation of heterosis, duplicationenabling evolution of gene function, and alteration of regulation.

The allopolyploid oilseed crop Brassica napus (canola) providesan example of how heterozygosity resulting from polyploidy canaffect evolutionarily important traits. Brassica napus is thoughtto be derived from crosses between B. oleracea (2n = 18, CCgenome) and B. rapa (2n = 20, AA genome). Using molecular markers,lines in mapping populations were compared at a transpositionsite with QTL for seed yield (Osborn et al. 2003a, Quijada et al., 2006,Udall et al., 2006). When the allelic arrangement was similarto that of the parental genotypes, B. oleracea and B. rapa,seed yields were lower. However, when the arrangement of allelesdiffered from these parental genotypes seed yields were higher.The best explanation for the results of these studies was thatintergenomic heterozygosity increased seed yield in B. napus.

In allopolyploid cotton, an ancient polyploidy, it has beenshown that some homoeologous genes are assigned to different(sub)functions, with gene expression compartmentalized to differenttissue types and gene expression biased between homoeologs (Adams et al., 2003,2004). Thus, between the genomes of cotton, expression of homoeologousgenes is developmentally regulated. It has been suggested thatthis may provide allopolyploids with greater plasticity in responseto stress (Udall and Wendel, 2006). Further understanding ofwhat causes changes in homoeologous gene function may provideavenues to manipulate gene expression.

Gene expression is generally dependent on hierarchically organizednetworks of regulators. The number of these regulators can beincreased several-fold in polyploids and the overall consequencesof polyploidy on gene expression at the end of regulatory networksare difficult to predict (Osborn et al., 2003b). In a genome-wideanalysis of synthetic allotetraploids between Arabidopsis thalianaand A. arenosa, about 5 % of genes showed divergence from themid-parent value, suggesting non-additive gene regulation (Wang et al., 2006b).For example, time of flowering in this synthetic allopolyploidwas later than both parents. This was found to be the resultof the epistatic interactions between two loci, one for floweringfrom A. thaliana (FLC) and the other from A. arenosa (FRI),that enhances FLC expression and inhibits flowering (Wang etal., 2006a). In hexaploid wheat, latitude of breeding has influencedthe selection of genes affecting earliness of flowering, butthere is still much genetic diversity relating to both photoperiodand vernalization requirements of the selections (Goldringer et al., 2006).The rapid reprogramming of biological pathways on polyploidizationleads to novel variation that may be exploited by plant breeders.

Many breeding programmes involve wide and distant hybridization.These procedures cause dramatic genome change, sometimes leadingto unpredictable results. Studies of ancient and modern polyploidsprovide a means of elucidating the effects of dramatic genomechange on gene expression and regulation. Results from suchstudies should enable breeding programs to achieve the desiredresults.

Achieving new levels of crop yield and new uses for crops

The future course of domestication will continue to rely onchanges to the architecture, metabolism and physiology of crops.To reach new levels of crop yield and new uses for crops, acombination of applied and also theoretical approaches involvingcomputer or systems' biology models will be required. To copewith new challenges to crop production, efficient approachesto screen germplasm for genes to both biotic and abiotic stressesin wild and cultivated germplasm are needed. Crops primarilyused for food are now also being used to meet demands for sustainablefuel supply, while the use of plants for construction timbersand fibres in paper, textiles and composite products continuesto increase. To provide value-added crops, new products fromcrops are being developed. Specialized plant products for processing(such as starches, oils, even plastics) for food, pharmaceutical,cosmetic and industrial uses are required for growing markets(Heslop-Harrison, 2002).

As information accumulates on domestication-related traits andtheir genome distribution, new avenues to attain higher yieldand to tailor-make crops are opened up. Analysis of yield andplant height in a cross between two Japanese rice varieties,‘Koshihikari’ and ‘Habataki’, revealedseveral QTLs for each trait. One QTL, Gn1a, increased grainproductivity and acts by altering the production of the enzymecytokinin oxidase/dehydrogenase that degrades the phytohormonecytokinin. By reducing the expression of Gn1a, cytokinin accumulatesin inflorescence meristems, resulting in an increased numberof grains and, hence, a plant with the potential for increasedyield (Ashikari et al., 2005). By accumulating a variety ofyield-related QTLs for increasing both source to produce photosynthateand sink to accept photosynthate, new levels of yield may beachieved.

Throughout history, plants have been subjected to changing climate,and farmers have adopted new species and varieties to meet thechallenges; indeed, post-glacial climate changes may have beenone of the factors leading to the origin of agriculture andplant domestication. Climate change is affecting agriculturein the 21st century; some changes will be met within existingadaptations of plants, but other factors such as increased UVand carbon dioxide levels require new selections based on understandingof plant responses. Hidema and Kumagai (2006) reported considerablevariation in UVB sensitivity of rice cultivars, which was causedby differences of one or two bases in the CPD (cyclobutane pyrimidinedimer) photolyase, altering the activity of the enzyme. Theysuggest that the resistance of rice to UVB radiation can thereforebe increased by selective breeding or bioengineering of thegenes encoding CPD photolyase. Although carbon dioxide enhancementis regularly used to improve glasshouse production, it is notclear how field crops will respond to changes in atmosphericcarbon dioxide concentrations, involving complex interactionsof phytosythesis with light and dark respiration (Bunce, 2005).

There is no naturally occurring waxy wheat variety but in breadwheat there are waxy loci in each of its three different genomes,A, B and D. The waxy locus encodes starch granule protein 1(SGP-1). Different isoforms are encoded by genes in each genome(sgpA1, sgpB1 and sgpD1). In the germplasm collection of breadwheat, cultivars lacking one of the three isoforms were found,two cultivars from Korea lacked SGP-A1, one from Japan lackedSPG-B1 and one from Turkey lacked SPG-D1. By making appropriatecrosses, these genes were combined in a single plant, resultingin the first waxy wheat, which had a null for all three isoformsof SGP-1 (Yamamori et al., 2000), an example of using markersfor identification of alleles and then marker-assisted selectionto find the desired allele combination. The effort to producewaxy wheat in Japan has led to its use as an ingredient forimproved Japanese-style noodles. These examples show the valueof screening germplasm collections with diverse material foruseful genetic variation, but also emphasize that it is notalways necessary to search in exotic material or employ radicaltechniques to make innovative progress in plant breeding.

Super domestication

We are entering a new era in relation to human understandingof and influence on the genetics of crop domestication. Currentresearch on genes related to crop domestication is providingpieces in the complex jigsaw of gene evolution (see also Hancock, 2005),networking, regulation and expression in our most importantplants. Introduction of alien genes through transgenic technologymay be difficult (King et al., 2004), but continued advancesin crop improvement will depend on understanding the genomeand its genes.

Super-domesticates can be constructed with knowledge-led approachesusing the range of current technologies. Here, we use the termsuper-domestication to refer to the processes that lead to adomesticate with dramatically increased yield that could notbe selected in natural environments from naturally occurringvariation without recourse to new technologies. The array ofgenome manipulations that have been developed, mainly sincethe 1980s, enable barriers to gene exchange to be overcome andhave lead to super-domesticates with dramatically increasedyields, resistances to biotic and abiotic stresses, and withnew characters for the marketplace. Hybrid rice (see Cheng et al., 2007,in this Special Issue) can be considered a super-domesticate.

The teams of scientists that support plant breeders are planningand conducting research to change crops radically. For example,changing crops from C3 photosynthesis to C4 photosynthesis isbeing proposed because it is now known that plants with C3 photosynthesishave enzymes for C4 photosynthesis, and even well-developedC4 pathways can be found at certain locations in C3 plants.In addition, C4-enzyme genes have been inserted into and successfullyexpressed in rice (Mitchell and Sheehy, 2006). Conversion ofa crop from C3 to C4 photosynthesis would certainly be a super-domesticate.

It was with this background of rapid progress being made instudies of crop domestication that a meeting was organized inTsukuba, Japan, in October 2006, by the National Institute ofAgrobiological Sciences (NIAS) and the Organisation for EconomicCooperation and Development (OECD) and supported by Annals ofBotany. While the Tsukuba meeting was being planned, a differentmeeting, entitled Plants, People and Evolution, sponsored bythe Linnean Society of London, the Systematics Association andAnnals of Botany was in preparation. This meeting was held inLondon in August 2006. Selected papers from these meetings appearin this Special Issue of Annals of Botany.

Progress in understanding crop domestication, and further advancesthat lead to greater quantities and improved quality of foodcrops, depend increasingly on multidisciplinary team approaches(Zeder et al., 2006; Wuchty et al., 2007). Scientists representinga diversity of botanical and crop-science backgrounds, archaeobotanists,crop evolutionary biologists, geneticists, ethnobotanists, plantbreeders, statisticians and biotechnology specialists contributepapers in this present volume. The papers include both reviewsof topics related to crop domestication and original researcharticles. Two key papers discuss domestication in the New World(Pickersgill, 2007) and the Old World (Fuller, 2007), whilethe papers that follow relate to particular crops or groupsof crops. Included are papers on crops that have been intensivelystudied by molecular methods, e.g. maize (Yamasaki et al., 2007),barley (Azhaguvel and Komatsuda, 2007; Pourkheirandish and Komatsuda, 2007),tomato (Bai and Lindhout, 2007), wheat (Waines and Ehdaie, 2007);some whose genomes have been completely sequenced, e.g. rice(Cheng et al., 2007; Sweeney and McCouch, 2007) and sorghum(Dillon et al., 2007), or where sequencing projects are proceedingactively, e.g. soybean (Liu et al., 2007) and common bean (Phaseolusvulgaris; Papa et al., 2007), and some where domestication isstill at an early stage, e.g. giant cacti (Casas et al., 2007),artichoke (Sonnante et al., 2007) or banana (Heslop-Harrison and Schwarzacher, 2007).Scientists working on minor crops envy the amount of informationbeing rapidly accumulated on model crops, but by extrapolationinformation from model species and model crops is already hasteningadvances in minor crops. This will be particularly true forcurrent genomic initiatives in closely related crops such asthe legumes (Weeden, 2007), where data from common bean andsoybean will benefit the closely related African and Asian Vigna(Isemura et al., 2007). Knowledge of the sorghum genome canbe tapped to make progress in understanding the complex genomeof sugarcane (Dillon et al., 2007) and that of the rice genomefor banana (Heslop-Harrison and Schwarzacher, 2007). Minor crops,by the very fact that less is known about them, provide thepotential of rapidly finding new insights into crop domestication(e.g. Fukunaga et al., 2006).

The papers in this Special Issue are appearing in an area wherethere is currently much scientific progress. It is hoped thatthe papers here will stimulate ideas to help sciences associatedwith crop domestication achieve needed future super-domesticates.

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Figure

 

mcith_mcm22401.gif
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Figure 1   Alternative contemporary ways of harvesting wild rice in India. (A) Beating panicles over a basket, and (B) twisting leaves and stem into bundles that collect shattered grain. These methods, plus swinging a basket over ripening panicles, are used to harvest wild rice in South Asia and West Africa (Oka, 1988).

 


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