Molecular evidence for a single evolutionary origin of domesticated rice

Asian rice, Oryza sativa, is one of world's oldest and most important crop species. Rice is believed to have been domesticated ～9,000 y ago, although debate on its origin remains contentious. A single-origin model suggests that two main subspecies of Asian rice, indica and japonica, were domesticated from the wild rice O. rufipogon. In contrast, the multiple independent domestication model proposes that these two major rice types were domesticated separately and in different parts of the species range of wild rice. This latter view has gained much support from the observation of strong genetic differentiation between indica and japonica as well as several phylogenetic studies of rice domestication. We reexamine the evolutionary history of domesticated rice by resequencing 630 gene fragments on chromosomes 8, 10, and 12 from a diverse set of wild and domesticated rice accessions. Using patterns of SNPs, we identify 20 putative selective sweeps on these chromosomes in cultivated rice. Demographic modeling based on these SNP data and a diffusion-based approach provide the strongest support for a single domestication origin of rice. Bayesian phylogenetic analyses implementing the multispecies coalescent and using previously published phylogenetic sequence datasets also point to a single origin of Asian domesticated rice. Finally, we date the origin of domestication at ～8,200-13,500 y ago, depending on the molecular clock estimate that is used, which is consistent with known archaeological data that suggests rice was first cultivated at around this time in the Yangtze Valley of China.     

Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa

Cultivated rice, Oryza sativa L., represents the world's most important staple food crop, feeding more than half of the human population. Despite this essential role in world agriculture, the history of cultivated rice's domestication from its wild ancestor, Oryza rufipogon, remains unclear. In this study, DNA sequence variation in three gene regions is examined in a phylogeographic approach to investigate the domestication of cultivated rice. Results indicate that India and Indochina may represent the ancestral center of diversity for O. rufipogon. Additionally, the data suggest that cultivated rice was domesticated at least twice from different O. rufipogon populations and that the products of these two independent domestication events are the two major rice varieties, Oryza sativa indica and Oryza sativa japonica. Based on this geographical analysis, O. sativa indica was domesticated within a region south of the Himalaya mountain range, likely eastern India, Myanmar, and Thailand, whereas O. sativa japonica was domesticated from wild rice in southern China.     

Dissecting yield-associated loci in super hybrid rice by resequencing recombinant inbred lines and improving parental genome sequences

The growing world population and shrinkage of arable land demand yield improvement of rice, one of the most important staple crops. To elucidate the genetic basis of yield and uncover its associated loci in rice, we resequenced the core recombinant inbred lines of Liang–You–Pei–Jiu, the widely cultivated super hybrid rice, and constructed a high-resolution linkage map. We detected 43 yield-associated quantitative trait loci, of which 20 are unique. Based on the high-density physical map, the genome sequences of paternal variety 93–11 and maternal cultivar PA64s of Liang–You–Pei–Jiu were significantly improved. The large recombinant inbred line population combined with plentiful high-quality single nucleotide polymorphisms and insertions/deletions between parental genomes allowed us to fine-map two quantitative trait loci, qSN8 and qSPB1, and to identify days to heading8 and lax panicle1 as candidate genes, respectively. The quantitative trait locus qSN8 was further confirmed to be days to heading8 by a complementation test. Our study provided an ideal platform for molecular breeding by targeting and dissecting yield-associated loci in rice.Rice is one of the most important staple crops in the world and serves as a model for monocots (1). Currently, rice breeding faces the challenge of overcoming the yield plateau. All important agronomic traits would ultimately need to consider their impacts on the yield, which is linked to various growth and developmental components, such as tiller number, seed number and set, and grain weight, to name a few. A number of quantitative trait loci (QTLs) have been reported to control these components, including those revealed by map-based cloning studies, such as IPA1/WFP for tiller and spikelet numbers (2, 3); days to heading8 (DTH8)/Ghd8 and Ghd7 for heading date, plant height, and spikelet number (4, 5); Gn1 for spikelet number (6); GIF1 for seed set (7); and grain size3 (GS3) and GW5 for grain size and weight (8, 9). Although a series of QTLs for yield components have been cloned, elucidation of the genetic mechanisms underlying the inheritance of superior yield in super hybrid rice still has a long way to go.Hybrid rice has a notable contribution to yield improvement. Various commercialized hybrids are derived by crossing different varieties within or between two subspecies, Oryza sativa ssp. indica and ssp. japonica (10, 11). As a pioneer super hybrid rice, Liang–You–Pei–Jiu (LYP9) realized the target of 10.5 tons/ha in 2000 (12). LYP9 was developed by a cross of the paternal 93–11, an indica variety widely grown in China (13), and the maternal PA64s cultivar with a mixed genetic background of indica and javanica. To date, it has been widely cultivated for commercial production in China. Such a feature was thought to make LYP9 recombinant inbred lines (RILs) ideal materials for exploring molecular mechanisms underlying rice yield.Here, we constructed a high-density linkage map by resequencing the parents of LYP9 and 132 core RILs. As a result, we finished the chromosome-scale genome sequence of PA64s and updated the 93–11 genome sequence by anchoring to chromosomes, filling up gaps, and correcting single-base errors. Twenty-five unique QTLs related to rice production were identified. One QTL, qSN8 for spikelet number, was fine-mapped with a large RIL population and confirmed as DTH8 by a complementation test.     

Genetic structure and isolation by distance in a landrace of Thai rice

Rice is among the 3 most important crops worldwide. While much of the world''s rice harvest is based on modern high-yield varieties, traditional varieties of rice grown by indigenous groups have great importance as a resource for future crop improvement. These local landraces represent an intermediate stage of domestication between a wild ancestor and modern varieties and they serve as reservoirs of genetic variation. Such genetic variation is influenced both by natural processes such as selection and drift, and by the agriculture practices of local farmers. How these processes interact to shape and change the population genetics of landrace rice is unknown. Here, we determine the population genetic structure of a single variety of landrace rice, Bue Chomee, cultivated by Karen people of Thailand. Microsatellite markers reveal high level of genetic variation despite predominant inbreeding in the crop. Bue Chomee rice shows slight but significant genetic differentiation among Karen villages. Moreover, genetically determined traits such as flowering time can vary significantly among villages. An unanticipated result was the overall pattern of genetic differentiation across villages which conforms to an isolation by distance model of differentiation. Isolation by distance is observed in natural plant species where the likelihood of gene flow is inversely related to distance. In Karen rice, gene flow is the result of farmers'' seed sharing networks. Taken together, these data suggest that landrace rice is a dynamic genetic system that responds to evolutionary forces, both natural and those imposed by humans.     

Genomewide SNP variation reveals relationships among landraces and modern varieties of rice

Rice, the primary source of dietary calories for half of humanity, is the first crop plant for which a high-quality reference genome sequence from a single variety was produced. We used resequencing microarrays to interrogate 100 Mb of the unique fraction of the reference genome for 20 diverse varieties and landraces that capture the impressive genotypic and phenotypic diversity of domesticated rice. Here, we report the distribution of 160,000 nonredundant SNPs. Introgression patterns of shared SNPs revealed the breeding history and relationships among the 20 varieties; some introgressed regions are associated with agronomic traits that mark major milestones in rice improvement. These comprehensive SNP data provide a foundation for deep exploration of rice diversity and gene–trait relationships and their use for future rice improvement.     

NAL1 allele from a rice landrace greatly increases yield in modern indica cultivars

Increasing crop production is essential for securing the future food supply in developing countries in Asia and Africa as economies and populations grow. However, although the Green Revolution led to increased grain production in the 1960s, no major advances have been made in increasing yield potential in rice since then. In this study, we identified a gene, SPIKELET NUMBER (SPIKE), from a tropical japonica rice landrace that enhances the grain productivity of indica cultivars through pleiotropic effects on plant architecture. Map-based cloning revealed that SPIKE was identical to NARROW LEAF1 (NAL1), which has been reported to control vein pattern in leaf. Phenotypic analyses of a near-isogenic line of a popular indica cultivar, IR64, and overexpressor lines revealed increases in spikelet number, leaf size, root system, and the number of vascular bundles, indicating the enhancement of source size and translocation capacity as well as sink size. The near-isogenic line achieved 13–36% yield increase without any negative effect on grain appearance. Expression analysis revealed that the gene was expressed in all cell types: panicles, leaves, roots, and culms supporting the pleiotropic effects on plant architecture. Furthermore, SPIKE increased grain yield by 18% in the recently released indica cultivar IRRI146, and increased spikelet number in the genetic background of other popular indica cultivars. The use of SPIKE in rice breeding could contribute to food security in indica-growing regions such as South and Southeast Asia.The world’s population is expected to surpass 9 billion in 2050 (http://esa.un.org/unpd/ppp/index.htm). Most of this increase will occur in the developing countries of Asia and Africa. By 2035, a 26% increase in rice production will be essential to feed the rising population (1, 2). Rice (Oryza sativa L.) is a staple food of more than 3 billion people, mainly in Asia. Predominantly, indica cultivars are grown in southern China, Southeast Asia, and South Asia, occupying approximately 70% of the rice-producing area in the world, whereas japonica cultivars are grown mainly in East Asia (3, 4). Because of urbanization and industrialization, an increase in the yield of indica cultivars is a pressing need in Southeast and South Asia (5). Additionally, good grain quality (influencing market value) and high yield are essential for the adoption of new cultivars in local areas (6).The grain yield of rice is determined by spikelet number per panicle, panicle number per plant, grain weight, and spikelet fertility. Although many quantitative trait loci (QTLs) for yield components have been identified (www.gramene.org), few have so far been isolated. To date, at least nine genes or loci for yield-related traits in rice have been isolated from natural variation: Gn1a and APO1 for number of grains (7–9); GS3, GW2, and qSW5 for grain size (10–12); DEP1 and WFP for panicle architecture (13, 14); SCM2 for strong culm (15); and Ghd7 for late heading and number of grains (16). APO1, SCM2, and DEP1 increased grain yield in a japonica genetic background in field experiments (9, 13, 15). However, no novel cloned gene has been reported to increase grain yield in indica cultivars (17). Here, we identified a gene in a tropical japonica landrace and used the allele to increase the grain yield of modern indica cultivars at the crop level through a breeding concept developed by International Rice Research Institute (IRRI) breeders more than 20 y ago.In 1989, a breeding program for New Plant Type (NPT) rice was launched at IRRI to increase the yields of modern indica cultivars by using genetic material from tropical japonica landraces (18). Several Indonesian tropical japonica landraces—which are characterized by large panicles, large leaves, a vigorous root system, thick stems, and few unproductive tillers—have been used in international breeding programs. However, despite these features, the NPT cultivars yield less than modern indica cultivars, mainly because of low grain fertility and low panicle number (19, 20). To genetically dissect and elicit the valuable traits of NPT cultivars, we backcrossed the NPT cultivars including YP9 (IR68522-10-2-2) against modern indica cultivar IR64 to develop introgression lines (ILs) (Fig. S1). BC₃-derived ILs, which had favorable yield-related traits and few undesirable traits, were selected by field observation (21). Using the ILs, we identified 21 QTLs for yield components such as total spikelet number per panicle (TSN), grain weight, and panicle number. Among the QTLs, qTSN4, for high TSN, was commonly detected on the long arm of chromosome 4 in five NPT lines derived from different tropical japonica cultivars (22). Additionally, a near-isogenic line (NIL) for qTSN4 from YP9, derived from tropical japonica landrace Daringan with an IR64 genetic background, had more spikelets per panicle and more branches than IR64.In this study, we isolated the gene for qTSN4 through map-based cloning to facilitate its use in breeding. The phenotypic effects of the gene were validated in transgenic plants and by expression analysis. To confirm the effect on practical grain yield in the field, we evaluated yield and related traits by using NILs with genetic backgrounds of popular indica cultivars.     

Ancient mitochondrial DNA analysis reveals complexity of indigenous North American turkey domestication

Although the cultural and nutritive importance of the turkey (Meleagris gallopavo) to precontact Native Americans and contemporary people worldwide is clear, little is known about the domestication of this bird compared to other domesticates. Mitochondrial DNA analysis of 149 turkey bones and 29 coprolites from 38 archaeological sites (200 BC–AD 1800) reveals a unique domesticated breed in the precontact Southwestern United States. Phylogeographic analyses indicate that this domestic breed originated from outside the region, but rules out the South Mexican domestic turkey (Meleagris gallopavo gallopavo) as a progenitor. A strong genetic bottleneck within the Southwest turkeys also reflects intensive human selection and breeding. This study points to at least two occurrences of turkey domestication in precontact North America and illuminates the intensity and sophistication of New World animal breeding practices.     

A conserved molecular basis for photoperiod adaptation in two temperate legumes

Legumes were among the first plant species to be domesticated, and accompanied cereals in expansion of agriculture from the Fertile Crescent into diverse environments across the Mediterranean basin, Europe, Central Asia, and the Indian subcontinent. Although several recent studies have outlined the molecular basis for domestication and eco-geographic adaptation in the two main cereals from this region, wheat and barley, similar questions remain largely unexplored in their legume counterparts. Here we identify two major loci controlling differences in photoperiod response between wild and domesticated pea, and show that one of these, HIGH RESPONSE TO PHOTOPERIOD (HR), is an ortholog of EARLY FLOWERING 3 (ELF3), a gene involved in circadian clock function. We found that a significant proportion of flowering time variation in global pea germplasm is controlled by HR, with a single, widespread functional variant conferring altered circadian rhythms and the reduced photoperiod response associated with the spring habit. We also present evidence that ELF3 has a similar role in lentil, another major legume crop, with a distinct functional variant contributing to reduced photoperiod response in cultivars widely deployed in short-season environments. Our results identify the factor likely to have permitted the successful prehistoric expansion of legume cultivation to Northern Europe, and define a conserved genetic basis for major adaptive changes in flowering phenology and growth habit in an important crop group.     

Beyond the single gene: How epistasis and gene-by-environment effects influence crop domestication

Domestication is a multifaceted evolutionary process, involving changes in individual genes, genetic interactions, and emergent phenotypes. There has been extensive discussion of the phenotypic characteristics of plant domestication, and recent research has started to identify the specific genes and mutational mechanisms that control domestication traits. However, there is an apparent disconnect between the simple genetic architecture described for many crop domestication traits, which should facilitate rapid phenotypic change under selection, and the slow rate of change reported from the archeobotanical record. A possible explanation involves the middle ground between individual genetic changes and their expression during development, where gene-by-gene (epistatic) and gene-by-environment interactions can modify the expression of phenotypes and opportunities for selection. These aspects of genetic architecture have the potential to significantly slow the speed of phenotypic evolution during crop domestication and improvement. Here we examine whether epistatic and gene-by-environment interactions have shaped how domestication traits have evolved. We review available evidence from the literature, and we analyze two domestication-related traits, shattering and flowering time, in a mapping population derived from a cross between domesticated foxtail millet and its wild progenitor. We find that compared with wild progenitor alleles, those favored during domestication often have large phenotypic effects and are relatively insensitive to genetic background and environmental effects. Consistent selection should thus be able to rapidly change traits during domestication. We conclude that if phenotypic evolution was slow during crop domestication, this is more likely due to cultural or historical factors than epistatic or environmental constraints.Domestication is a process of evolutionary change that leads to increased dependence and associated phenotypic modifications in both domesticator and domesticated. Much is known about the phenotypes that change during plant domestication, including the so-called domestication syndrome described from annual crops, which emphasizes retention of seed on the seed head, reduction in lateral branching, reduction in seed dormancy, and increase in seed size (1). Other phenotypic changes occurring during domestication and improvement, such as shifts in flowering time and grain composition, have also been extensively studied (2–4). Recent molecular research has begun to identify and functionally characterize a growing number of the major-effect domestication and crop improvement genes (5–8). However, there is disagreement over the speed of phenotypic evolution during domestication, with an apparent disconnect between the relatively simple genetic architecture of many domestication-related traits, which should facilitate rapid change, and the protracted length of time seen in the archeobotanical record for some domestication phenotypes to become widespread (9–12).The genetics of domestication traits generally suggest that phenotypic changes during crop domestication could potentially occur rapidly. Many domestication alleles segregate as Mendelian loci with large effects (7), and the rate of self-pollination in many crops is high, allowing for the expression of both recessive and dominant domestication alleles even when initially at low frequencies in populations. However, archeobotanical evidence from the major cereal crops rice and wheat (10, 13) and some population genetic simulations (9, 14) suggest that genetic modifications underlying phenotypic change may only slowly be translated into geographically widespread domestication phenotypes. Scenarios to explain this apparent discrepancy have focused on the strength of selection during domestication, mediated by the ability of early farmers to recognize and use favorable mutations, as well as population genetic processes such as introgression from wild populations (15). It is also possible that the vagaries of human history, including wars, epidemics, and other interruptions to food production (16), may have led to protracted domestication rates. There has been much debate as to whether the slow increase in domesticated phenotypes is real or a preservation artifact and what assumptions can be made about the botanical knowledge of early farmers (9–12, 17). Here we explore whether background effects such as gene-by-gene interactions (epistasis) and gene-by-environment (G × E) effects can affect the efficacy of selection on domestication alleles. In theory, this middle ground between molecular genetic change and its expression during development could have significantly slowed the process of phenotypic evolution during crop domestication.Epistasis refers to genetic interactions between loci, which may be either biallelic or higher order in nature. The term has been defined in a number of different ways [reviewed by Phillips (18)]; here we restrict our use to describe the phenomenon whereby the phenotypic effects of a given allele at a gene can vary depending on the allelic composition of the other loci that make up an individual’s genotype. This definition has been described as “compositional epistasis” (18) and is synonymous with “physiological epistasis” as used by Cheverud and Routman (19) and “functional epistasis” as used by Carter et al. (20). Epistasis has been shown to contribute to additive genetic variances and covariances, thereby affecting the response to selection; depending on the direction of these effects in morphospace, it may dramatically change the response to selection in only a few generations (20). In the context of domestication genetics, various outcomes are possible for any pair of loci, from complete lack of gene interaction, with only additive effects explaining the phenotype (Fig. 1A), to the effects of wild and domestication alleles differing across genetic backgrounds (Fig. 1 B and C).Open in a separate windowFig. 1.Three sets of phenotypic outcomes that could result from biallelic epistatic interactions between two loci. Circles and stars represent genotypes homozygous for alleles that affect a domestication trait, where higher trait values are selectively favored during domestication. Pink genotypes have alleles from the domesticated population. Blue genotypes have alleles drawn from a population of close wild relatives. (A) No interaction. Additive effects of alleles explain all of the phenotypic variation. (B) Interaction such that domestication alleles at one or the other locus give trait values close to the domesticate double homozygote. (C) Less than additive interaction such that the wild–domesticate gene pair combinations have genotypic values lower than wild or domesticate double homozygotes.The geographical distribution and population structure of many crops and their wild relatives may predispose these species to epistatic effects. Both crop species and their wild progenitors are often characterized by substantial population genetic structure, with distinct genetic subpopulations that are geographically separated and evolutionarily diverged (21, 22). This is especially true for inbreeding species, where local adaptation is not easily homogenized by introgression from other populations and where local variants can readily become established and persist through time. If adaptive differentiation among populations has led to evolutionary divergence in gene regulatory networks, a domestication allele that was initially selected upon in one population could, in theory, have very different phenotypic effects when introgressed into a population growing in a different region.G × E interactions refer to situations in which the relative effects of alleles change across environments. The visible morphological traits selected during domestication, such as branching, inflorescence development, and seed size, are strongly affected by the environment (23), and the phenotypic effects of favorable domestication alleles may have been difficult for early farmers to consistently detect. If we assume that early agriculturalists, like those today, sought to reduce the impacts of both predictable and unpredictable environmental variation on crops, a resulting expectation is that domestication alleles would be less sensitive to environmental changes than predomestication, ancestral alleles. Such phenotypic stability would facilitate selection, enabling the spread of domesticated crops away from their native environments into other climates and latitudes (24).Here we investigate whether epistasis and/or G × E interactions could help explain the apparent contradiction between the genetic simplicity of many domestication-related traits (both domestication and improvement traits) and the slow rate of phenotypic progress observed for some crops in the archeobotanical record. We review studies of epistasis and show that a number of genes affecting domestication-related traits are epistatic in segregating populations containing wild and domestication alleles. In many cases, domestication alleles have more stable effects in diverse genetic backgrounds than do ancestral alleles, suggesting that selection for these “robust” alleles would be effective in creating rapid phenotypic change. Similarly, the effects of domestication alleles differ across environments but are often less sensitive to environmental variation than wild (predomestication) alleles. As a complement to the literature review, we also examine the effects of epistasis on shattering and the effects of epistasis and G × E on flowering time in a cross between domesticated foxtail millet (Setaria italica) and its wild progenitor, green millet (Setaria viridis). We find loci of major-effect and epistatic and G × E interactions that significantly explain phenotypic variation. Major-effect loci appear to be less influenced by genetic background than are minor-effect loci. We suggest that for many domestication-related traits, wild populations segregate for alleles that are sensitive to genetic background and environment but that the process of domestication has favored relatively insensitive loci that have large effects on traits and are highly responsive to selection. Thus, the simple genetic architecture observed for many domestication-related traits may be the evolutionary outcome of successful selection for alleles that are relatively insensitive to background effects.     

Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice

Grain size and shape are important components determining rice grain yield, and they are controlled by quantitative trait loci (QTLs). Here, we report the cloning and functional characterization of a major grain length QTL, qGL3, which encodes a putative protein phosphatase with Kelch-like repeat domain (OsPPKL1). We found a rare allele qgl3 that leads to a long grain phenotype by an aspartate-to-glutamate transition in a conserved AVLDT motif of the second Kelch domain in OsPPKL1. The rice genome has other two OsPPKL1 homologs, OsPPKL2 and OsPPKL3. Transgenic studies showed that OsPPKL1 and OsPPKL3 function as negative regulators of grain length, whereas OsPPKL2 as a positive regulator. The Kelch domains are essential for the OsPPKL1 biological function. Field trials showed that the application of the qgl3 allele could significantly increase grain yield in both inbred and hybrid rice varieties, due to its favorable effect on grain length, filling, and weight.     

Sunflower domestication alleles support single domestication center in eastern North America

Phylogenetic analyses of genes with demonstrated involvement in evolutionary transitions can be an important means of resolving conflicting hypotheses about evolutionary history or process. In sunflower, two genes have previously been shown to have experienced selective sweeps during its early domestication. In the present study, we identified a third candidate early domestication gene and conducted haplotype analyses of all three genes to address a recent, controversial hypothesis about the origin of cultivated sunflower. Although the scientific consensus had long been that sunflower was domesticated once in eastern North America, the discovery of pre-Columbian sunflower remains at archaeological sites in Mexico led to the proposal of a second domestication center in southern Mexico. Previous molecular studies with neutral markers were consistent with the former hypothesis. However, only two indigenous Mexican cultivars were included in these studies, and their provenance and genetic purity have been questioned. Therefore, we sequenced regions of the three candidate domestication genes containing SNPs diagnostic for domestication from large, newly collected samples of Mexican sunflower landraces and Mexican wild populations from a broad geographic range. The new germplasm also was genotyped for 12 microsatellite loci. Our evidence from multiple evolutionarily important loci and from neutral markers supports a single domestication event for extant cultivated sunflower in eastern North America.     

Earliest domestication of common millet (Panicum miliaceum) in East Asia extended to 10,000 years ago

The origin of millet from Neolithic China has generally been accepted, but it remains unknown whether common millet (Panicum miliaceum) or foxtail millet (Setaria italica) was the first species domesticated. Nor do we know the timing of their domestication and their routes of dispersal. Here, we report the discovery of husk phytoliths and biomolecular components identifiable solely as common millet from newly excavated storage pits at the Neolithic Cishan site, China, dated to between ca. 10,300 and ca. 8,700 calibrated years before present (cal yr BP). After ca. 8,700 cal yr BP, the grain crops began to contain a small quantity of foxtail millet. Our research reveals that the common millet was the earliest dry farming crop in East Asia, which is probably attributed to its excellent resistance to drought.