Heading date 1 (Hd1), an ortholog of Arabidopsis CONSTANS, is a possible target of human selection during domestication to diversify flowering times of cultivated rice

During the domestication of rice (Oryza sativa L.), diversification of flowering time was important in expanding the areas of cultivation. Rice is a facultative short day (SD) plant and requires certain periods of dark to induce flowering. Heading date 1 (Hd1), a regulator of the florigen gene Hd3a, is one of the main factors used to generate diversity in flowering. Loss-of-function alleles of Hd1 are common in cultivated rice and cause the diversity of flowering time. However, it is unclear how these functional nucleotide polymorphisms of Hd1 accumulated in the course of evolution. Nucleotide polymorphisms within Hd1 and Hd3a were analyzed in 38 accessions of ancestral wild rice Oryza rufipogon and compared with those of cultivated rice. In contrast to cultivated rice, no nucleotide changes affecting Hd1 function were found in 38 accessions of wild rice ancestors. No functional changes were found in Hd3a in either cultivated or ancestral rice. A phylogenetic analysis indicated that evolution of the Hd1 alleles may have occurred independently in cultivars descended from various accessions of ancestral rice. The non-functional Hd1 alleles found in cultivated rice may be selected during domestication, because they were not found or very rare in wild ancestral rice. In contrast with Hd3a, which has been highly conserved, Hd1 may have undergone human selection to diversify the flowering times of rice during domestication or the early stage of the cultivation period.     

Levels and patterns of nucleotide variation in domestication QTL regions on rice chromosome 3 suggest lineage-specific selection

Oryza sativa or Asian cultivated rice is one of the major cereal grass species domesticated for human food use during the Neolithic. Domestication of this species from the wild grass Oryza rufipogon was accompanied by changes in several traits, including seed shattering, percent seed set, tillering, grain weight, and flowering time. Quantitative trait locus (QTL) mapping has identified three genomic regions in chromosome 3 that appear to be associated with these traits. We would like to study whether these regions show signatures of selection and whether the same genetic basis underlies the domestication of different rice varieties. Fragments of 88 genes spanning these three genomic regions were sequenced from multiple accessions of two major varietal groups in O. sativa--indica and tropical japonica--as well as the ancestral wild rice species O. rufipogon. In tropical japonica, the levels of nucleotide variation in these three QTL regions are significantly lower compared to genome-wide levels, and coalescent simulations based on a complex demographic model of rice domestication indicate that these patterns are consistent with selection. In contrast, there is no significant reduction in nucleotide diversity in the homologous regions in indica rice. These results suggest that there are differences in the genetic and selective basis for domestication between these two Asian rice varietal groups.     

Two evolutionary histories in the genome of rice: the roles of domestication genes

Genealogical patterns in different genomic regions may be different due to the joint influence of gene flow and selection. The existence of two subspecies of cultivated rice provides a unique opportunity for analyzing these effects during domestication. We chose 66 accessions from the three rice taxa (about 22 each from Oryza sativa indica, O. sativa japonica, and O. rufipogon) for whole-genome sequencing. In the search for the signature of selection, we focus on low diversity regions (LDRs) shared by both cultivars. We found that the genealogical histories of these overlapping LDRs are distinct from the genomic background. While indica and japonica genomes generally appear to be of independent origin, many overlapping LDRs may have originated only once, as a result of selection and subsequent introgression. Interestingly, many such LDRs contain only one candidate gene of rice domestication, and several known domestication genes have indeed been "rediscovered" by this approach. In summary, we identified 13 additional candidate genes of domestication.     

Population Structure and Domestication Revealed by High-Depth Resequencing of Korean Cultivated and Wild Soybean Genomes

Despite the importance of soybean as a major crop, genome-wide variation and evolution of cultivated soybeans are largely unknown. Here, we catalogued genome variation in an annual soybean population by high-depth resequencing of 10 cultivated and 6 wild accessions and obtained 3.87 million high-quality single-nucleotide polymorphisms (SNPs) after excluding the sites with missing data in any accession. Nuclear genome phylogeny supported a single origin for the cultivated soybeans. We identified 10-fold longer linkage disequilibrium (LD) in the wild soybean relative to wild maize and rice. Despite the small population size, the long LD and large SNP data allowed us to identify 206 candidate domestication regions with significantly lower diversity in the cultivated, but not in the wild, soybeans. Some of the genes in these candidate regions were associated with soybean homologues of canonical domestication genes. However, several examples, which are likely specific to soybean or eudicot crop plants, were also observed. Consequently, the variation data identified in this study should be valuable for breeding and for identifying agronomically important genes in soybeans. However, the long LD of wild soybeans may hinder pinpointing causal gene(s) in the candidate regions.     

Distribution of fertility-restorer genes for wild-abortive and Honglian CMS lines of rice in the AA genome species of genus Oryza

BACKGROUND AND AIMS: Rice (Oryza sativa) is one of the most important cereal plants in the world. Wild-abortive (WA) and Honglian (HL) cytoplasmic male sterility (CMS) have been used extensively in the production of hybrid seeds. Although a variable number of fertility-restorer genes (Rf) for WA and HL-CMS have been identified in various cultivars, information on Rf in Oryza species with the AA-genome is sparse. Therefore the distribution and heredity of Rf for WA and HL-CMS in wild rice species of Oryza with the AA-genome were investigated. METHODS: Fertility-restorer genes for WA and HL-CMS in wild rice species with the AA-genome were investigated by following the fertility of microspores identified by I2-KI staining and by following the seed-setting rate of spikelets. A genetic model of Rf in some selected restorer accessions was analysed based on the fertility segregation of BC1F1 populations. KEY RESULTS: Fertility analysis showed that 21 out of 35 HL-type F1s, and 13 out of 31 WA-type F1s were scored as fertile. The frequency of Rf in wild rice was 60% for HL-CMS and 41.9% for WA-CMS, respectively. The fertility-restorer accessions, especially those with complete restoring ability, aggregated mainly in two species of O. rufipogon and O. nivara. The wild rice accessions with Rf for HL-CMS were distributed in Asia, Oceania, Latin American and Africa, but were centered mainly in Asia, whilst the wild restorer accessions for WA-CMS were limited only to Asia and Africa. Apart from one restorer accession that possessed two pairs of Rf for WA-CMS, all of the other nine tested wild restorer accessions each contained only a single Rf for WA-CMS or HL-CMS. Allele analysis indicated that there existed at least three Rf loci for the WA and HL-CMS systems. CONCLUSIONS: These data support the hypothesis that fertility-restorer genes exist widely in Oryza species with the AA-genome, and that Rf in Oryza sativa originated from the Oryza rufipogon/Oryza nivara complex, the ancestor of cultivated rice in Asia. The origin and evolution of Rf is tightly linked to that of CMS in wild rice, and fertility of a given CMS type is controlled by several Rf alleles in various wild restorer accessions.     

Sequence polymorphisms in wild,weedy, and cultivated rice suggest seed‐shattering locus sh4 played a minor role in Asian rice domestication

The predominant view regarding Asian rice domestication is that the initial origin of nonshattering involved a single gene of large effect, specifically, the sh4 locus via the evolutionary replacement of a dominant allele for shattering with a recessive allele for reduced shattering. Data have accumulated to challenge this hypothesis. Specifically, a few studies have reported occasional seed‐shattering plants from populations of the wild progenitor of cultivated rice (Oryza rufipogon complex) being homozygous for the putative “nonshattering” sh4 alleles. We tested the sh4 hypothesis for the domestication of cultivated rice by obtaining genotypes and phenotypes for a diverse set of samples of wild, weedy, and cultivated rice accessions. The cultivars were fixed for the putative “nonshattering” allele and nonshattering phenotype, but wild rice accessions are highly polymorphic for the putative “nonshattering” allele (frequency ~26%) with shattering phenotype. All weedy rice accessions are the “nonshattering” genotype at the sh4 locus but with shattering phenotype. These data challenge the widely accepted hypothesis that a single nucleotide mutation (“G”/“T”) of the sh4 locus is the major driving force for rice domestication. Instead, we hypothesize that unidentified shattering loci are responsible for the initial domestication of cultivated rice through reduced seed shattering.     

基于线粒体基因片段核苷酸多态性的亚洲栽培稻起源进化研究

亚洲栽培稻的祖先是普通野生稻,已成为世界公认的观点,然而亚洲栽培稻的2个亚种:粳稻和籼稻是一次起源还是二次起源仍存在很大争议,其起源地是国内还是国外依然是国际学者间争论的焦点。本文通过对184份亚洲栽培稻和203份普通野生稻3段基因序列cox3、cox1、orf 224和2段基因间序列ssv-39/178、rps2-trnfM的多样性研究,验证了以下观点:1)粳稻起源于中国,籼稻起源于中国和国外;2)亚洲栽培稻的起源为二次起源,即普通野生稻存在偏籼和偏粳2种类型,亚洲栽培稻的2个亚种籼稻和粳稻在进化过程中分别由偏籼型的普通野生稻和偏粳型的普通野生稻进化而来。     

The complex history of the domestication of rice

BACKGROUND: Rice has been found in archaeological sites dating to 8000 bc, although the date of rice domestication is a matter of continuing debate. Two species of domesticated rice, Oryza sativa (Asian) and Oryza glaberrima (African) are grown globally. Numerous traits separate wild and domesticated rices including changes in: pericarp colour, dormancy, shattering, panicle architecture, tiller number, mating type and number and size of seeds. SCOPE: Genetic studies using diverse methodologies have uncovered a deep population structure within domesticated rice. Two main groups, the indica and japonica subspecies, have been identified with several subpopulations existing within each group. The antiquity of the divide has been estimated at more than 100 000 years ago. This date far precedes domestication, supporting independent domestications of indica and japonica from pre-differentiated pools of the wild ancestor. Crosses between subspecies display sterility and segregate for domestication traits, indicating that different populations are fixed for different networks of alleles conditioning these traits. Numerous domestication QTLs have been identified in crosses between the subspecies and in crosses between wild and domesticated accessions of rice. Many of the QTLs cluster in the same genomic regions, suggesting that a single gene with pleiotropic effects or that closely linked clusters of genes underlie these QTL. Recently, several domestication loci have been cloned from rice, including the gene controlling pericarp colour and two loci for shattering. The distribution and evolutionary history of these genes gives insight into the domestication process and the relationship between the subspecies. CONCLUSIONS: The evolutionary history of rice is complex, but recent work has shed light on the genetics of the transition from wild (O. rufipogon and O. nivara) to domesticated (O. sativa) rice. The types of genes involved and the geographic and genetic distribution of alleles will allow scientists to better understand our ancestors and breed better rice for our descendents.     

Phylogeny and origin of pearl millet (Pennisetum glaucum [L.] R. Br) as revealed by microsatellite loci

During the last 12,000 years, different cultures around the world have domesticated cereal crops. Several studies investigated the evolutionary history and domestication of cereals such as wheat in the Middle East, rice in Asia or maize in America. The domestication process in Africa has led to the emergence of important cereal crops like pearl millet in Sahelian Africa. In this study, we used 27 microsatellite loci to analyze 84 wild accessions and 355 cultivated accessions originating from the whole pearl millet distribution area in Africa and Asia. We found significantly higher diversity in the wild pearl millet group. The cultivated pearl millet sample possessed 81% of the alleles and 83% of the genetic diversity of the wild pearl millet sample. Using Bayesian approaches, we identified intermediate genotypes between the cultivated and wild groups. We then analyzed the phylogenetic relationship among accessions not showing introgression and found that a monophyletic origin of cultivated pearl millet in West Africa is the most likely scenario supported by our data set.     

Quantitative trait loci underlying domestication- and yield-related traits in an Oryza sativa x Oryza rufipogon advanced backcross population

To understand the genetic characteristics of the traits related to differentiation between cultivated rice and its wild progenitor, genetic factors controlling domestication- and yield-related traits were identified using a BC3F2 population derived from an accession of common wild rice (donor, Oryza rufipogon Griff.) collected from Yuanjiang, Yunnan province, China, and an indica cultivar, Teqing (recipient, Oryza sativa L.). A genetic linkage map consisting of 125 simple sequence repeat (SSR) markers was constructed. Based on the phenotypes of the 383 BC3F2 families evaluated in two environments, two domestication-related morphological traits, panicle shape and growth habit, were found to be controlled by single Mendelian factors. This implies that the recessive mutations of single genes controlling some morphological traits could have been easily selected during early domestication. By single-point analysis and interval mapping, 59 putative quantitative trait loci (QTLs) that influence 11 quantitative traits were detected at two sites, and 37.5% of the QTL alleles originating from O. rufipogon had a beneficial effect for yield-related traits in the Teqing background. Regions with significant QTLs for domestication- and yield-related traits were detected on chromosomes 1, 4, 5, 7, 8, and 12. Fine mapping and cloning of these domestication-related genes and QTLs will be useful in elucidating the origin and differentiation of Asian cultivated rice in the future.     

Nucleotide Diversity and Molecular Evolution of the <Emphasis Type="Italic">ALK</Emphasis> Gene in Cultivated Rice and its Wild Relatives

Gelatinization temperature (GT), an important parameter for rice cooking quality, is mainly regulated by the ALK gene encoding starch synthase IIa. Here, we reported the nucleotide diversity of the ALK gene in 122 cultivated accessions and 199 wild rice accessions that were collected around the Pearl River Basin in China. A total of 93 single nucleotide ploymorphisms (SNPs) were identified, with an average of one SNP per 40 bp. Tajima D statistics revealed that the DNA sequences covering the last exon have probably evolved under balancing selection. Based on two functional SNPs (an A to G substitution at 4198 bp and a GC to TT dinucleotide substitution at 4330/4331 bp), three haplotypes, G/GC, G/TT, and A/GC, were identified in both wild and cultivated accessions, with the G/GC haplotype being predominant. Interestingly, the A/GC haplotype was exclusively found in the wild accessions from Guangdong province, while the G/TT haplotype was only present in the wild accessions from Jiangxi province and Hainan Island. This suggests that the G/TT and A/GC variants may have arisen independently and undergone balancing selection on separate haplotypes in multiple populations. Our result supports earlier hypothesis that cultivated rice was independently domesticated from multiple domestication events in China. Our study aids in the understanding of the domestication process that led to the improvement of rice grain quality.     

Genomic analyses provide comprehensive insights into the domestication of bast fiber crop ramie (Boehmeria nivea)

Ramie (Boehmeria nivea) is an economically important natural fiber-producing crop that has been cultivated for thousands of years in China; however, the evolution of this crop remains largely unknown. Here, we report a ramie domestication analysis based on genome assembly and resequencing of cultivated and wild accessions. Two chromosome-level genomes representing wild and cultivated ramie were assembled de novo. Numerous structural variations between two assemblies, together with the genetic variations from population resequencing, constituted a comprehensive genomic variation map for ramie. Domestication analysis identified 71 high-confidence selective sweeps comprising 320 predicted genes, and 29 genes from sweeps were associated with fiber growth in the expression. In addition, we identified seven genetic loci associated with the fiber yield trait in the segregated population derived from the crossing of two assembled accessions, and two of which showed an overlap with the selective sweeps. These findings indicated that bast fiber traits were focused on during the domestication history of ramie. This study sheds light on the domestication of ramie and provides a valuable resource for biological and breeding studies of this important crop.     

Modern elite rice varieties of the 'Green Revolution' have retained a large introgression from wild rice around the Pi33 rice blast resistance locus

During the breeding process of cultivated crops, resistance genes to pests and diseases are commonly introgressed from wild species. The size of these introgressions is predicted by theoretical models but has rarely been measured in cultivated varieties. By combining resistance tests with isogenic strains, genotyping and sequencing of different rice accessions, it was shown that, in the elite rice variety IR64, the resistance conferring allele of the rice blast resistance gene Pi33 was introgressed from the wild rice Oryza rufipogon (accession IRGC101508). Further characterization of this introgression revealed a large introgression at this locus in IR64 and the related variety IR36. The introgressed fragment represents approximately half of the short arm of rice chromosome 8. This is the first report of a large introgression in a cultivated variety of rice. Such a large introgression is likely to have been maintained during backcrossing only if a selection pressure was exerted on this genomic region. The possible traits that were selected are discussed.     

Leveraging natural diversity: back through the bottleneck

Plant breeders have long recognized the existence of useful genetic variation in the wild ancestors of our domesticated crop species. In cultivated rice (Oryza sativa), crosses between high-yielding elite cultivars and low-yielding wild accessions often give rise to superior offspring, with wild alleles conferring increased performance in the context of the elite cultivar genetic background. Because the breeding value of wild germplasm cannot be determined by examining the performance of wild accessions, a phylogenetic approach is recommended to determine which interspecific combinations are most likely to be useful in a breeding program. As we deepen our understanding of how genetic diversity is partitioned within and between cultivated and wild gene pools of Oryza, breeders will have increased power to make predictions about the most efficient strategies for utilizing wild germplasm for rice improvement.     

Selection under domestication: evidence for a sweep in the rice waxy genomic region

Rice (Oryza sativa) was cultivated by Asian Neolithic farmers >11,000 years ago, and different cultures have selected for divergent starch qualities in the rice grain during and after the domestication process. An intron 1 splice donor site mutation of the Waxy gene is responsible for the absence of amylose in glutinous rice varieties. This mutation appears to have also played an important role in the origin of low amylose, nonglutinous temperate japonica rice varieties, which form a primary component of Northeast Asian cuisines. Waxy DNA sequence analyses indicate that the splice donor mutation is prevalent in temperate japonica rice varieties, but rare or absent in tropical japonica, indica, aus, and aromatic varieties. Sequence analysis across a 500-kb genomic region centered on Waxy reveals patterns consistent with a selective sweep in the temperate japonicas associated with the mutation. The size of the selective sweep (>250 kb) indicates very strong selection in this region, with an inferred selection coefficient that is higher than similar estimates from maize domestication genes or wild species. These findings demonstrate that selection pressures associated with crop domestication regimes can exceed by one to two orders of magnitude those observed for genes under even strong selection in natural systems.     

Genetic control of a transition from black to straw-white seed hull in rice domestication

The genetic mechanism involved in a transition from the black-colored seed hull of the ancestral wild rice (Oryza rufipogon and Oryza nivara) to the straw-white seed hull of cultivated rice (Oryza sativa) during grain ripening remains unknown. We report that the black hull of O. rufipogon was controlled by the Black hull4 (Bh4) gene, which was fine-mapped to an 8.8-kb region on rice chromosome 4 using a cross between O. rufipogon W1943 (black hull) and O. sativa indica cv Guangluai 4 (straw-white hull). Bh4 encodes an amino acid transporter. A 22-bp deletion within exon 3 of the bh4 variant disrupted the Bh4 function, leading to the straw-white hull in cultivated rice. Transgenic study indicated that Bh4 could restore the black pigment on hulls in cv Guangluai 4 and Kasalath. Bh4 sequence alignment of all taxa with the outgroup Oryza barthii showed that the wild rice maintained comparable levels of nucleotide diversity that were about 70 times higher than those in the cultivated rice. The results from the maximum likelihood Hudson-Kreitman-Aguade test suggested that the significant reduction in nucleotide diversity in rice cultivars could be caused by artificial selection. We propose that the straw-white hull was selected as an important visual phenotype of nonshattered grains during rice domestication.     

The Puzzle of Rice Domestication

The origin of cultivated rice has puzzled plant biologists for decades. This is due, at least in part, to the complex evolutionary dynamics in rice cultivars and wild progenitors, particularly rapid adaptive differentiation and continuous gene flow within and between cultivated and wild rice. The long-standing controversy over single versus multiple and annual versus perennial origins of cultivated rice has been brought into shaper focus with the rapid accumulation of genetic and phylogenetic data. Molecular phylogenetic analyses revealed ancient genomic differentiation between rice cultivars, suggesting that they were domesticated from divergent wild populations. However, the recently cloned domestication gene sh4, responsible for the reduction of grain shattering from wild to cultivated rice, seems to have originated only once. Herein, we propose two models to reconcile apparently conflicting evidence regarding rice domestication. The snowoballing model considers a single origin of cultivated rice. In this model, a core of critical domestication alleles was fixed in the founding cultivar and then acted to increase the genetic diversity of cultivars through hybridization with wild populations. The combination model considers multiple origins of cultivated rice. In this model, Initial cultivars were domesticated from divergent wild populations and fixed different sets of domestication alleles. Subsequent crosses among these semi-domesticated cultivars resulted in the fixation of a similar set of critical domestication alleles in the contemporary cultivars. In both models, introgression has played an important role in rice domestication. Recent and future introgression of beneficial genes from the wild gene pool through conventional and molecular breeding programs can be viewed as the continuation of domestication.     

Association between nonsynonymous mutations of starch synthase IIa and starch quality in rice (Oryza sativa)

Starch quality is one of the most important agronomic traits in Asian rice, Oryza sativa. Starch synthase IIa (SsIIa) is a major candidate gene for starch quality variation. Within SsIIa, three nonsynonymous mutations in exon 8 have been shown to affect enzyme activity when expressed in Escherichia coli. To search for the variation in SsIIa that is responsible for starch quality variation in rice, we sequenced the SsIIa exon 8 region and measured starch quality as starch disintegration in alkali for 289 accessions of cultivated rice and 57 accessions of its wild ancestor, Oryza rufipogon. A general linear model and nested clade analysis were used to identify the associations between the three nonsynonymous single nucleotide polymorphisms (SNPs) and starch quality. Among the three nonsynonymous SNPs, we found strong evidence of association at one nucleotide site ('SNP 3'), corresponding to a Leu/Phe replacement at codon 781. A second SNP, corresponding to a Val/Met replacement at codon 737, could potentially show an association with increased sample sizes. Variation in SsIIa enzyme activity is associated with the cohesiveness of rice grains when cooked, and our findings are consistent with selection for more cohesive grains during the domestication of tropical japonica rice.