Genes and Mutations Underlying Domestication Transitions in Grasses

Over the past several years, our understanding of plant domestication has advanced substantially at the gene and genome levels. This is due largely to the rapid accumulation of genomic resources that provided genome-wide markers for population and molecular genetic analyses of crops and their wild relatives. A number of recent reviews captured some general aspects of these advances (Doebley et al., 2006; Ross-Ibarra et al., 2007; Vaughan et al., 2007; Burger et al., 2008). The primary goal of this article is to update the recent progress made in the grass family (Poaceae). Grass domestication had a unique importance in the history of human civilization. Cereal crops, domesticated from wild grasses thousands of years ago, have provided food security for the human society. Of the modern cereals, maize (Zea mays), rice (Oryza sativa), and wheat (Triticum spp.), domesticated in different regions of the world 7,000 to 10,000 years ago, are the top three food crops with much higher annual production than others. Barley (Hordeum vulgare), arguably the fourth important cereal crop used as human food, animal feed, and brewing grains, is also among the earliest domesticated cereals. Sorghum ranks next in the annual cereal production, followed by oat (Avena sativa), rye (Secale cereale), and millets (http://faostat.fao.org/). The number of studies published on cereal domestication appears to be correlated with the agronomic importance of the crops, with especially a wealth of data generated for maize, rice, wheat, and barley. The amount of genomic resources that became available over the past several years also seemed to have an impact on publications. The completion of rice genome sequencing (International Rice Genome Sequencing Project, 2005) has greatly accelerated the progress of studying rice domestication, resulting in a number of recent reviews on this subject (Kovach et al., 2007; Sang and Ge, 2007a, 2007b; Sweeney and McCouch, 2007; Vaughan et al., 2008). Of the four top cereals, maize represents a rather unique case. It differs from barley, rice, and wheat by having undergone much more drastic morphological modifications during domestication. Considerable effort undertaken to investigate maize domestication has yielded classic literatures on the molecular basis of morphological evolution, which was thoroughly reviewed recently (Doebley, 2004; Doebley et al., 2006). For these reasons I will focus on updating recent progress made in barley, rice, and wheat, in which the studies of phenotypic transitions that allowed effective harvesting, such as reduction in shattering and improvement of threshing, will be the main theme of the article. One of the recent advances in understanding rice domestication was the finding that the two major types of rice cultivars, rice subspecies indica and subspecies japonica, had distinct genomic backgrounds. Molecular clock dating with various markers suggested that the genomes of indica and japonica rice came from wild populations that diverged 0.4 to 0.2 million years ago, considerably preceding the time of rice domestication (Ma and Bennetzen, 2004; Vitte et al., 2004; Zhu and Ge, 2005). This lends support to the hypothesis of independent domestication of indica and japonica rice. The geographic locations for the domestication of indica and japonica cultivars were traced to south of the Himalayans and southern China, respectively (Londo et al., 2006). Another line of advances was achieved through genetic analyses of morphological and physiological changes from the wild progenitors, Oryza nivara and Oryza rufipogon, to the cultivated rice. The number and chromosomal locations of quantitative trait loci (QTL) underlying important domestication traits have been estimated. These included the reduction in grain shattering and seed dormancy, synchronization of seed maturation, reduction in tiller number, increase in tiller erectness, increase in panicle branches, and the number of spikelets per panicle, and reduction in hull and pericarp coloration and awn length (Xiong et al., 1999; Cai and Morishima, 2002; Thomson et al., 2003; Li et al., 2006a; Onishi et al., 2007a). Of these changes often known as the domestication syndrome of cereals (Harlan, 1992), reduction in grain shattering is critical to effective harvesting and has been viewed as the hallmark of cereal domestication. A major QTL, sh4, responsible for the reduction of grain shattering from the wild progenitors to cultivated rice was recently cloned (Li et al., 2006b). The gene encodes a transcription factor with a Myb3 DNA-binding domain. The mutation selected by early farmers to develop nonshattering cultivars was a single nucleotide substitution leading to an amino acid substitution from Lys to Asn in the DNA-binding domain. The substitution of the neutral for the positively charged amino acid, which weakened but did not knock out the gene function, caused the incomplete development and partial function of the abscission zone where a mature grain detaches from the pedicle. This disables the natural detachment of grains necessary for seed dispersal in the wild species, but allows manual separation of grains and pedicles at the abscission zone in cultivars. The fine tuning of the gene function is critical for maximizing the harvest efficiency because it prevents excessive grain loss during the first stage of harvest when tillers with mature panicles are cut and gathered. Equally important is the ability to subsequently remove and recover grains from the straws using simple threshing techniques such as beating against a wood tub. Comparative sequence analyses further indicated that sh4 had a single origin and are now fixed in all rice cultivars (Li et al., 2006b; Lin et al., 2007; Onishi et al., 2007b). This finding was, however, somewhat surprising given the strong phylogenetic evidence for the independent domestications of indica and japonica rice. Two theoretical models were proposed to reconcile these apparently conflicting genetic and phylogenetic data (Sang and Ge, 2007a, 2007b). The snowballing model considers that the earliest domesticated rice had fixed a set of critical domestication alleles such as sh4, which then spread into the populations of the wild progenitors, O. nivara and O. rufipogon, through introgression. One or both of the modern cultivars, indica and japonica, were derived from the hybrids that maintained the original set of domestication alleles and captured genomic background of wild populations best adapted to the local conditions. The core of the domestication alleles fixed in the founding cultivar thus acted to facilitate cultivar diversification as it rolled through the wild gene pool. The combination model assumes that early rice cultivars were domesticated independently from wild populations with distinct genomic backgrounds at different locations. They initially fixed different sets of domestication alleles to make cultivation feasible and worthwhile. Subsequent crosses among these early cultivars followed by artificial selection for the best domestication alleles, including sh4, drove the fixation of the same set of alleles of different origins in nearly all modern cultivars. Perhaps not in the strict sense, the snowballing model is more consistent with the conventional view of a single domestication, whereas the combination model leans toward the scenario of multiple domestications. In either case, introgression coupled with both artificial and natural selections played an important role in rice domestication. It served as an effective means to increase the genetic diversity of cultivars especially following the initial domestication bottleneck, and to produce cultivars adaptive to various climatic conditions in different geographic regions. Other domestication-related genes cloned so far are not fixed in all rice cultivars. qSH1 is a homeobox gene responsible for the further reduction of grain shattering in some of the temperate japonica cultivars (Konishi et al., 2006). The causal mutation was a nucleotide substitution in the regulatory element located approximately 12 kb upstream of the coding region of qSH1, which substantially changed the level and pattern of gene expression and disrupted the development of the abscission zone between grains and pedicles. For japonica cultivars with both qSH1 and sh4, the two genes contribute similar magnitude of phenotypic effect (Xiong et al., 1999; Cai and Morishima, 2002; Onishi et al., 2007a). The reasons why they have such different frequencies in rice cultivars can be speculated as follows. First, qSH1 was selected during the domestication of japonica rice, but was subsequently selected against and eliminated from most of the japonica cultivars after sh4 was introduced from cultivars of different origins, such as indica. The combination of qSH1 and sh4 could have made threshing too difficult and laborious at the time. Second, qSH1 was derived in the japonica cultivars that already had sh4 to further reduce shattering when the requirement for stronger threshing force was no longer a problem. Another gene, Rc, encoding a bHLH protein that presumably regulates anthocyanin biosynthesis in the seed coat, was involved in the origin of white-seed cultivars from the red-seed wild progenitors (Sweeney et al., 2006). Two independent mutations in exon 6 of the gene could each be responsible for the loss of red pigment in the pericarps. A 14-bp deletion was found in nearly 98% of white rice and a nucleotide substitution resulting in a premature stop codon was found in the rest of white rice. Phylogenetic analyses indicated that the predominant 14-bp deletion originated in the japonica cultivar and spread into the indica cultivar through introgression (Sweeney et al., 2007). Although the reasons why white rice was favored over red rice thousands of years ago was not entirely clear, the selection for white seeds apparently was strong enough to spread the 14-bp deletion into the vast majority of modern cultivars. Studies of barley domestication have progressed rapidly over the past few years (Pourkheirandish and Komatsuda, 2007). The phylogenetic relationships and population genetic structures of barley and its wild progenitor Hordeum spontaneum were analyzed using various types of molecular markers. Genes controlling key domestication traits were fine mapped or cloned. Similar to rice, the findings were brought on questions of whether barley was domesticated once or multiple times and to what extent introgression has influenced the domestication process. Molecular phylogenetic analysis initially based on AFLP markers supported the hypothesis of a single origin of cultivated barley in the Fertile Crescent, and traced the location of barley domestication to the Israel-Jordan area (Badr et al., 2000). The conclusion, however, was soon called into question as the subsequent phylogenetic studies using different types of molecular markers favored the alternative hypotheses of multiple independent domestications. The analysis of chloroplast microsatellites suggested that there were additional centers of domestication west of the Fertile Crescent, including Ethiopia and western Mediterranean (Molina-Cano et al., 2005). A population genetic study based on sequences of seven nuclear loci also argued for the multiple origins of barley, and suggested that there were two centers of domestication, one in the Fertile Crescent and the other 1,500 to 3,000 km farther east (Morrell and Clegg, 2007). It further indicated that wild barley from the Fertile Crescent served as the primary genome donor for the modern cultivars in Europe and North America, while the wild populations from the eastern center contributed most of the genetic diversity of Asian cultivars. Despite a growing body of evidence supporting multiple origins of barley, the phylogenetic analysis alone could not rule out the possibility that barley was domesticated once in the Fertile Crescent and spread to other regions of the world where it hybridized with the wild species (Badr et al., 2000; Kilian et al., 2006b). Crosses between the early cultivars and wild populations followed by artificial selection for domestication traits and natural selection for better adaptation to local climates could have given rise to cultivars with highly divergent genomic backgrounds. This scenario is similar to the snowballing model of rice domestication. analyses of domestication traits have recently yielded into the of barley domestication. The domestication transitions that have been to genetic studies in barley the reduction in grain shattering of the separation of seeds from of and the from to barley each as a seed dispersal of three of which the two are with to the dispersal of the in the wild This trait did not during the initial domestication of the barley. In the more advanced barley, the two spikelets so that the number of of grains is The gene, that the development of the spikelets has been cloned et al., 2007). In the barley, encodes an transcription factor that is in the and the development of the The mutation of allowed the further development of the and rise to barley. different mutations have been in the barley, the multiple independent origins of the trait et al., 2007). In wild barley, are to the seed and seeds from and et al., 2008). This trait is in a of barley cultivars known as barley, which it the modern cereal crop with and barley is used as animal or brewing For the of as a in the separation of during The of barley in which seeds are from the was a of selection for human rice where grains are at first from straws through threshing and seeds are subsequently from during the seeds of barley and wheat can be from that on the This an of grains from but additional mutations that allowed of seeds from The gene, by this selection was recently cloned in barley et al., 2008). In the barley, the gene encodes an factor that regulates biosynthesis in the seed coat, which between seed and the A deletion in the region was in the barley. The of sequences indicated that the deletion mutation was selected that the trait of seeds had a single of barley, to grain shattering in rice, was found to be by two and The at one of the or the from the western of the world have the while most of eastern cultivars have the Although has been phylogenetic analysis of sequences to these loci that eastern and western cultivars their the independent origins of from the eastern and western regions and Komatsuda, 2007). This the recent phylogenetic studies with multiple genes in supporting the independent domestications of barley. The however, has not been found in barley cultivars, due to the of the two loci et al., Of the three traits in the earliest barley cultivars approximately 10,000 years ago and is now fixed in all cultivars. and seeds more than a and are fixed in the modern cultivars. independently several times from various mutations of seeds by originated once and is found in all and barley for human et al., 2008). introgression between cultivars of either the same or different origins, coupled with strong artificial selection for threshing, has allowed the of in rice and barley where domestication at the the of genomes played an important role in wheat domestication and 2007). The wheat (Triticum and wheat (Triticum were domesticated independently in the Fertile Crescent approximately 10,000 years ago and served as important crops et al., Molecular phylogenetic studies that wheat was domesticated from a wild species with the genome of et al., wheat was domesticated from a wild species, with the genome that derived from the between an species, and a of the species, et al., 2002; Kilian et al., or wheat, now the most modern was derived from the between a cultivar with the genome and a wild species, with the genome of phylogenetic et al., 2002; et al., 2006). wheat has the genome of Similar to rice and barley, selection for cultivars with nonshattering grains or was a critical early of wheat domestication. For wheat of the was by alleles at two and located in the regions of and respectively et al., they are the loci between the and genomes from the For wheat, there was an additional also mapped to the location of of the genome et al., 2006; et al., 2006). that this chromosomal region of wheat be to that of barley two loci for and et al., 2006; and Komatsuda, 2007; but Li and 2006). The however, is not to either of the rice shattering genes sh4 and after the domestication of wheat with the trait in This to the development of the two most modern cultivars, the wheat of the genome and the or wheat (Triticum a of the The was achieved through the of and that were and in the wild species as as in cultivars such as and of the cultivars could to seeds force such as beating or during analysis between wheat and the wild progenitor of wheat, four responsible for the origin of the et al., Of the four QTL, two with each for approximately of phenotypic were mapped to the locations where two major loci were These were on the of of the and on the of of the The alleles, and were and at these two the of the wheat with the genome is as wheat with such a was with the of the wheat, the was not threshing due to the of the at the of the genome and an additional mutation at the of the genome was for the development of the in the wheat, which rise to the of et al., 2004; et al., 2007). The recent molecular of that it was a gene to the family of transcription et al., 2003; et al., 2006). The had a higher level of transcription than the in and The coding region of differs from that of by an amino acid which was responsible for an of of protein when in This mutation in the coding with regulatory mutations including a substitution at the et al., to the mutation of that the In to threshing, had effect on several other domestication-related such as plant and and resulting in and higher Comparative sequence analyses indicated that had a single origin in wheat et al., 2006). One hypothesis the of wheat is that the was in the wheat with the of which then served as the of In this an additional mutation at of the genome was et al., 2006). This be similar to the development of in the wheat, where a of presumably to and of the was selected following the it is why was not found in the genome of the the was threshing, with the of at the time of was selected in the wheat at first and then spread into wheat through introgression. These recent findings a general question of genes and mutations were for a critical domestication In the where the causal mutations have been a single mutation nonshattering in all rice cultivars, threshing or seeds in barley, and grains of maize et al., 2005). One gene with different mutations for the origin of white seeds of rice and of barley. In maize, that encodes a transcription factor was responsible for the reduction of of the wild progenitor (Doebley et al., the causal have been located in the region approximately to kb upstream of the coding it was not entirely whether a single mutation or multiple mutations of independent origins were involved in this domestication et al., 1999; et al., 2006). The next of in wheat and barley, where the major have been located on but not cloned. The responsible for in wheat were mapped to the chromosomal between the different genomes in the and wheat, that genes could have been the of In barley, it was proposed based on genetic analyses that two and the has been in crosses and the has been found in This to the possibility that and could be different mutations of the same One can the hypothesis that the with the same mutation and the but alleles with different mutations are to that the same function of the protein as in the wild It is that in Rc, and of the seven where an important domestication has been at the gene one gene one Of where causal mutations are three and the scenario of one mutation for one for of barley and wheat where the major have not been there is a that each was by the same or One to the scenario of one gene for one trait was threshing of wheat, which was by two major loci of similar magnitude of phenotypic however, the two loci are different in other aspects of their is over for the or and other domestication-related traits in to It is thus that a of threshing, was selected at first during wheat domestication and was then selected and to fixation in both and cultivars because it was such a with effect on it is to based on these findings that in most a single gene played a role in the population over the of a key domestication of effect or genes played but necessary in the of a domestication This given that there are multiple in a that could be by domestication Equally is the question of among the the of domestication selection are Comparative suggested that the be for key domestication traits in the grass family et al., The recent findings from fine and of domestication of cereals an to this hypothesis at a genomic The evidence so far to that the has a more phylogenetic than The best is the of genetic basis of the nonshattering trait among rice, barley, and the responsible for nonshattering were mapped to the chromosomal regions in barley and wheat that to the same of the these regions are not to shattering sh4 and qSH1, in rice that to a but different for barley and wheat, the trait is by different for barley and for is the of one gene controlling a domestication in crops but not between crops especially as they more to each of it has been that genes involved in the important domestication transitions are regulatory genes mutations can phenotypic modifications that as for strong artificial selection in the key of crop (Doebley and Doebley et al., 2006). one further from this one can that out or the function of a regulatory gene effect not be an genetic to It is thus not surprising to that selection independently by early farmers at the same the origins of white rice and barley, where the same phenotypic in each was through independent selection for the mutations of the same This that there was the number of in the for the artificial selection that at the most for this is as the divergent between more crop genes and domestication with and backgrounds independently domesticated cultivars of a gene between during the of domestication. in the top represents the single origin of a domestication The is subsequently fixed in this cultivar and and also fixed in the other for this scenario in barley and sh4 in rice qSH1 was derived in some japonica cultivars after the fixation of sh4 for in the top represents the independent origin of at the same as the red Two alleles and have the similar function and in the modern cultivars. for this scenario the alleles of in barley and in rice. at two different by a red and a are selected during the independent domestications. The red is more than the and there is between selection the red gene in both cultivars with a of the cultivar the The the of sh4 and qSH1 in some japonica cultivars in the that qSH1 originated in japonica the introgression of In the of two domestication loci initially the red gene is more than the gene there is a between the gene is eliminated from the cultivars and the red gene the domestication gene fixed in the modern cultivars. This is a more for scenario A that there had been gene by artificial selection at the initial stage of the the reviewed one gene responsible for a critical domestication as a This could be to strong artificial selection on the number of genes for phenotypic changes that a wild species into a among cultivars of different origins greatly the spread of the most Although further have to on additional domestication genes from a number of crops, what has been so far to that a drastic phenotypic for an crop or a crop can be achieved by or mutations of one it not be to or such a mutation because the number of genes can be I and for on the of the