Sequence polymorphisms in wild, weedy, and cultivated rice suggest seed-shattering locus sh4 played a minor role in Asian rice domestication.
ABSTRACT: 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.
Project description:Cultivated rice fields worldwide are plagued with weedy rice, a conspecific weed of cultivated rice (Oryza sativa L.). The persistence of weedy rice has been attributed, in part, to its ability to shatter (disperse) seed prior to crop harvesting. In the United States, separately evolved weedy rice groups have been shown to share genomic identity with exotic domesticated cultivars. Here, we investigate the shattering phenotype in a collection of U.S. weedy rice accessions, as well as wild and cultivated relatives. We find that all U.S. weedy rice groups shatter seeds easily, despite multiple origins, and in contrast to a decrease in shattering ability seen in cultivated groups. We assessed allelic identity and diversity at the major shattering locus, sh4, in weedy rice; we find that all cultivated and weedy rice, regardless of population, share similar haplotypes at sh4, and all contain a single derived mutation associated with decreased seed shattering. Our data constitute the strongest evidence to date of an evolution of weeds from domesticated backgrounds. The combination of a shared cultivar sh4 allele and a highly shattering phenotype, suggests that U.S. weedy rice have re-acquired the shattering trait after divergence from their progenitors through alternative genetic mechanisms.
Project description:BACKGROUND: Seed shattering, or shedding, is an important fitness trait for wild and weedy grasses. U.S. weedy rice (Oryza sativa) is a highly shattering weed, thought to have evolved from non-shattering cultivated ancestors. All U.S. weedy rice individuals examined to date contain a mutation in the sh4 locus associated with loss of shattering during rice domestication. Weedy individuals also share the shattering trait with wild rice, but not the ancestral shattering mutation at sh4; thus, how weedy rice reacquired the shattering phenotype is unknown. To establish the morphological basis of the parallel evolution of seed shattering in weedy rice and wild, we examined the abscission layer at the flower-pedicel junction in weedy individuals in comparison with wild and cultivated relatives. RESULTS: Consistent with previous work, shattering wild rice individuals possess clear, defined abscission layers at flowering, whereas non-shattering cultivated rice individuals do not. Shattering weedy rice from two separately evolved populations in the U.S. (SH and BHA) show patterns of abscission layer formation and degradation distinct from wild rice. Prior to flowering, the abscission layer has formed in all weedy individuals and by flowering it is already degrading. In contrast, wild O. rufipogon abscission layers have been shown not to degrade until after flowering has occurred. CONCLUSIONS: Seed shattering in weedy rice involves the formation and degradation of an abscission layer in the flower-pedicel junction, as in wild Oryza, but is a developmentally different process from shattering in wild rice. Weedy rice abscission layers appear to break down earlier than wild abscission layers. The timing of weedy abscission layer degradation suggests that unidentified regulatory genes may play a critical role in the reacquisition of shattering in weedy rice, and sheds light on the morphological basis of parallel evolution for shattering in weedy and wild rice.
Project description:Weedy rice (Oryza spp.) is a problematic weed of cultivated rice (O. sativa) around the world. Recent studies have established multiple independent evolutionary origins of weedy rice, raising questions about the traits and genes that are essential for the evolution of this weed. Among world regions, South Asia stands out due to the heterogeneity of its weedy rice populations, which can be traced to at least three origins: two through de-domestication from distinct cultivated rice varieties, and one from local wild rice (O. rufipogon/O. nivara). Here we examine five traits considered typical of or advantageous to weedy rice in weedy, cultivated and wild rice samples from South Asia. We establish that convergence among all three weed groups occurs for easy seed shattering, red pericarp color, and compact plant architecture, suggesting that these traits are essential for weed success in the South Asian agricultural environment. A high degree of convergence for black hull color is also seen among weeds with wild ancestors and weeds evolved from the aus cultivated rice group. We also examine polymorphism in five known domestication candidate genes, and find that Rc and Bh4 are associated with weed seed pericarp color and hull color, respectively, and weedy alleles segregate in the ancestral populations, as do alleles for the seed dormancy-linked gene Sdr4 The presence of a domestication related allele at the seed shattering locus, sh4, in weedy rice populations with cultivated ancestry supports a de-domestication origin for these weedy groups, and raises questions about the reacquisition of the shattering trait in these weedy populations. Our characterization of weedy rice phenotypes in South Asia and their associated candidate genes contribute to the emerging understanding of the mechanisms by which weedy rice evolves worldwide, suggesting that standing ancestral variation is often the source of weedy traits in independently evolved groups, and highlighting the reservoir of genetic variation that is present in cultivated varieties as well as in wild rice, and its potential for phenotypic evolution.
Project description:Seed shattering is an important agronomic trait in rice domestication. In this study, using a near-isogenic line (NIL-hs1) from Oryza barthii, we found a hybrid seed shattering phenomenon between the NIL-hs1 and its recurrent parent, a japonica variety Yundao 1. The heterozygotes at hybrid shattering 1 (HS1) exhibited the shattering phenotype, whereas the homozygotes from both parents conferred the non-shattering. The causal HS1 gene for hybrid shattering was located in the region between SSR marker RM17604 and RM8220 on chromosome 4. Sequence verification indicated that HS1 was identical to SH4, and HS1 controlled the hybrid shattering due to harboring the ancestral haplotype, the G allele at G237T site and C allele at C760T site from each parent. Comparative analysis at SH4 showed that all the accessions containing ancestral haplotype, including 78 wild relatives of rice and 8 African cultivated rice, had the shattering phenotype, whereas all the accessions with either of the homozygous domestic haplotypes at one of the two sites, including 17 wild relatives of rice, 111 African cultivated rice and 65 Asian cultivated rice, showed the non-shattering phenotype. Dominant complementation of the G allele at G237T site and the C allele at C760T site in HS1 led to a hybrid shattering phenotype. These results help to shed light on the nature of seed shattering in rice during domestication and improve the moderate shattering varieties adapted to mechanized harvest.
Project description:A number of genes that contribute to the domestication traits of cultivated rice have been identified. These include Sh4, Rc, PROG1 and LABA1, which are associated with non-shattering rachis, white pericarp, erect growth and barbless awns, respectively. The mutations giving rise to the "domestication alleles" of these genes are either invariable in cultivated rice, or have variability that is strictly associated with the phenotypic trait. This observation forms the basis to those current rice domestication models that envisage a single origin for the domesticated phenotype. Such models assume that the domestication alleles are absent or rare in wild rice, emerged under cultivation and spread across all rice groups by introgressive hybridization. We examined whole-genome sequencing datasets for wild and cultivated rice to test the former two assumptions. We found that the rc and laba1 alleles occur in wild rice with broad geographical distribution, and reach frequencies as high as 13 and 15%, respectively. These results are in agreement with previous observations of the prog1 and sh4 domestication alleles in wild populations. We also show that the diversity of the genomic regions surrounding the rc, laba1, prog1 and sh4 alleles in wild accessions is greater than that in cultivated rice, suggesting that these alleles emerged prior to domestication. Our findings indicate that the possibility that independent rice groups obtained identical domestication alleles directly from the wild population needs to be considered.
Project description:De-domestication is a unique evolutionary process by which domesticated crops are converted into 'wild predecessor like' forms. Weedy rice (Oryza sativa f. spontanea) is an excellent model to dissect the molecular processes underlying de-domestication. Here, we analyse the genomes of 155 weedy and 76 locally cultivated rice accessions from four representative regions in China that were sequenced to an average 18.2 × coverage. Phylogenetic and demographic analyses indicate that Chinese weedy rice was de-domesticated independently from cultivated rice and experienced a strong genetic bottleneck. Although evolving from multiple origins, critical genes underlying convergent evolution of different weedy types can be found. Allele frequency analyses suggest that standing variations and new mutations contribute differently to japonica and indica weedy rice. We identify a Mb-scale genomic region present in weedy rice but not cultivated rice genomes that shows evidence of balancing selection, thereby suggesting that there might be more complexity inherent to the process of de-domestication.
Project description:Agricultural weeds pose great challenges to sustainable crop production, owing to their complex origins and abundant genetic diversity. Weedy rice (WD) infests rice fields worldwide causing tremendous losses of rice yield/quality. To explore WD origins and evolution, we analyzed DNA sequence polymorphisms of the seed shattering genes (<i>sh4</i> and <i>qsh1</i>) in weedy, wild, and cultivated rice from a worldwide distribution. We also used microsatellite and insertion/deletion molecular fingerprinting to determine their genetic relationship and structure. Results indicate multiple origins of WD with most samples having evolved from their cultivated progenitors and a few samples from wild rice. WD that evolved from de-domestication showed distinct genetic structures associated with <i>indica</i> and <i>japonica</i> rice differentiation. In addition, the weed-unique haplotypes that were only identified in the WD samples suggest their novel mutations. Findings in this study demonstrate the key role of de-domestication in WD origins, in which <i>indica</i> and <i>japonica</i> cultivars stimulated further evolution and divergence of WD in various agroecosystems. Furthermore, novel mutations promote continued evolution and genetic diversity of WD adapting to different environments. Knowledge generated from this study provides deep insights into the origin and evolution of conspecific weeds, in addition to the design of effective measures to control these weeds.
Project description:Weedy forms of crop species infest agricultural fields worldwide and are a leading cause of crop losses, yet little is known about how these weeds evolve. Red rice (Oryza sativa), a major weed of cultivated rice fields in the US, is recognized by the dark-pigmented grain that gives it its common name. Studies using neutral molecular markers have indicated a close relationship between US red rice and domesticated rice, suggesting that the weed may have originated through reversion of domesticated rice to a feral form. We have tested this reversion hypothesis by examining molecular variation at Rc, the regulatory gene responsible for grain pigmentation differences between domesticated and wild rice. Loss-of-function mutations at Rc account for the absence of proanthocyanidin pigments in cultivated rice grains, and the major rc domestication allele has been shown to be capable of spontaneous reversion to a functional form through additional mutations at the Rc locus. Using a diverse sample of 156 weedy, domesticated and wild Oryzas, we analysed DNA sequence variation at Rc and its surrounding 4 Mb genomic region. We find that reversion of domestication alleles does not account for the pigmented grains of weed accessions; moreover, we find that haplotypes characterizing the weed are either absent or very rare in cultivated rice. Sequences from genomic regions flanking Rc are consistent with a genomic footprint of the rc selective sweep in cultivated rice, and they are compatible with a close relationship of red rice to Asian Oryzas that have never been cultivated in the US.
Project description:Weedy rice is a conspecific form of cultivated rice (Oryza sativa L.) that infests rice fields and results in severe crop losses. Weed strains in different world regions appear to have originated multiple times from different domesticated and/or wild rice progenitors. In the case of Malaysian weedy rice, a multiple-origin model has been proposed based on neutral markers and analyses of domestication genes for hull color and seed shattering. Here, we examined variation in pericarp (bran) color and its molecular basis to address how this trait evolved in Malaysian weeds and its possible role in weed adaptation. Functional alleles of the Rc gene confer proanthocyanidin pigmentation of the pericarp, a trait found in most wild and weedy Oryzas and associated with seed dormancy; nonfunctional rc alleles were strongly favored during rice domestication, and most cultivated varieties have nonpigmented pericarps. Phenotypic characterizations of 52 Malaysian weeds revealed that most strains are characterized by the pigmented pericarp; however, some weeds have white pericarps, suggesting close relationships to cultivated rice. Phylogenetic analyses indicate that the Rc haplotypes present in Malaysian weeds likely have at least three distinct origins: wild O. rufipogon, white-pericarp cultivated rice, and red-pericarp cultivated rice. These diverse origins contribute to high Rc nucleotide diversity in the Malaysian weeds. Comparison of Rc allelic distributions with other rice domestication genes suggests that functional Rc alleles may confer particular fitness benefits in weedy rice populations, for example, by conferring seed dormancy. This may promote functional Rc introgression from local wild Oryza populations.
Project description:Asian cultivated rice Oryza sativa L. was domesticated from its wild ancestor, O. rufipogon. During domestication, the cultivated rice lost its seed-shattering behaviour. Previous studies have shown that two major quantitative trait loci (QTLs; qSH1 and sh4) are responsible for the seed-shattering degree. Here, we produced introgression lines carrying non-functional alleles from O. sativa 'Nipponbare' at the two major QTLs in the genetic background of wild rice O. rufipogon W630, and examined the effects of the two QTLs on seed shattering and abscission layer formation. The introgression lines, with Nipponbare alleles at either or both loci, showed complete or partial abscission layer formation, respectively, indicating that other unknown loci might be involved in enhancing seed shattering in wild rice. We detected a single QTL named qSH3 regulating seed-shattering degree using an F2 population between Nipponbare and the introgression line carrying Nipponbare alleles at the two QTLs. Although we generated an introgression line for qSH3 alone, no effects on seed shattering were observed. However, a significant effect on seed-shattering degree was observed for the introgression line carrying Nipponbare alleles at qSH3 and the two QTLs, suggesting an important role of qSH3 on seed shattering in coordination with the two QTLs.