Malaysian weedy rice shows its true stripes: wild Oryza and elite rice cultivars shape agricultural weed evolution in Southeast Asia

Weedy rice is a close relative of domesticated rice (Oryza sativa) that competes aggressively with the crop and limits rice productivity worldwide. Most genetic studies of weedy rice have focused on populations in regions where no reproductively compatible wild Oryza species occur (North America, Europe and northern Asia). Here, we examined the population genetics of weedy rice in Malaysia, where wild rice (O. rufipogon) can be found growing in close proximity to cultivated and weedy rice. Using 375 accessions and a combined analysis of 24 neutral SSR loci and two rice domestication genes (sh4, controlling seed shattering, and Bh4, controlling hull colour), we addressed the following questions: (i) What is the relationship of Malaysian weedy rice to domesticated and wild rice, and to weedy rice strains in the USA? (ii) To what extent does the presence of O. rufipogon influence the genetic and phenotypic diversity of Malaysian weeds? (iii) What do the distributions of sh4 and Bh4 alleles and associated phenotypes reveal about the origin and contemporary evolution of Malaysian weedy rice? Our results reveal the following: independent evolutionary origins for Malaysian weeds and US strains, despite their very close phenotypic resemblance; wild‐to‐weed gene flow in Malaysian weed populations, including apparent adaptive introgression of seed‐shattering alleles; and a prominent role for modern Malaysian cultivars in the origin and recent proliferation of Malaysian weeds. These findings suggest that the genetic complexity and adaptability of weedy crop relatives can be profoundly influenced by proximity to reproductively compatible wild and domesticated populations.     

Molecular evolution of shattering loci in U.S. weedy rice

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.     

Genome re-sequencing suggested a weedy rice origin from domesticated indica-japonica hybridization: a case study from southern China

Main conclusion

Whole-genome re-sequencing of weedy rice from southern China reveals that weedy rice can originate from hybridization of domesticated indica and japonica rice.

Abstract

Weedy rice (Oryza sativa f. spontanea Rosh.), which harbors phenotypes of both wild and domesticated rice, has become one of the most notorious weeds in rice fields worldwide. While its formation is poorly understood, massive amounts of rice genomic data may provide new insights into this issue. In this study, we determined genomes of three weedy rice samples from the lower Yangtze region, China, and investigated their phylogenetics, population structure and chromosomal admixture patterns. The phylogenetic tree and principle component analysis based on 46,005 SNPs with 126 other Oryza accessions suggested that the three weedy rice accessions were intermediate between japonica and indica rice. An ancestry inference study further demonstrated that weedy rice had two dominant genomic components (temperate japonica and indica). This strongly suggests that weedy rice originated from indica-japonica hybridization. Furthermore, 22,443 novel fixed single nucleotide polymorphisms were detected in the weedy genomes and could have been generated after indica-japonica hybridization for environmental adaptation.     

Single-seeded InDel fingerprints in rice:An effective tool for indica-japonica rice classification and evolutionary studies

Asian cultivated rice(Oryza sativa L.),an important cereal crop worldwide,was domesticated from its wild ancestor 8000 years ago.During its long-term cultivation and evolution under diverse agroecological conditions, Asian cultivated rice has differentiated into indica and japonica subspecies.An effective method is required to identify rice germplasm for its indica and japonica features,which is essential in rice genetic improvements.We developed a protocol that combined DNA extraction from a single rice seed and the insertion/deletion(InDel) molecular fingerprint to determine the indica and japonica features of rice germplasm.We analyzed a set of rice germplasm,including 166 Asian rice varieties,two African rice varieties,30 accessions of wild rice species,and 42 weedy rice accessions,using the single-seeded InDel fingerprints(SSIF).The results show that the SSIF method can efficiently determine the indica and japonica features of the rice germplasm.Further analyses revealed significant indica and japonica differentiation in most Asian rice varieties and weedy rice accessions.In contrast,African rice varieties and nearly all the wild rice accessions did not exhibit such differentiation.The pattern of cultivated and wild rice samples illustrated by the SSIF supports our previous hypothesis that indica and japonica differentiation occurred after rice domestication under different agroecological conditions.In addition,the divergent pattern of rice cultivars and weedy rice accessions suggests the possibility of an endoferal origin(from crop)of the weedy rice included in the present study.     

Cultivated and weedy rice interactions and the domestication process

Examining the targets of selection in crop species and their wild and weedy relatives sheds light on the evolutionary processes underlying differentiation of cultivars from progenitor lineages. On one hand, human‐mediated directional selection in crops favours traits associated with the streamlining of controllable and predictable monoculture practices alongside selection for desired trait values. On the other hand, natural selection in wild and especially weedy relatives presumably favours trait values that increase the probability of escaping eradication. Gene flow between crops and wild species may also counter human‐mediated selection, promoting the evolution and persistence of weedy forms. In this issue, two studies from a group of collaborators examine diversity and divergence patterns of genes underlying two traits associated with red rice (Oryza sp.), the conspecific relative of cultivated rice (Oryza sativa) that is a non‐native weed (see Fig. 1 ). In the first study by Gross et al. (2010) , genetic variation in the major gene underlying the hallmark red pigmentation characterizing most weedy rice (Rc) is found to have a pattern consistent with non‐reversion from U.S. cultivated rice (i.e. the cultivar did not ‘go feral’). This suggests that U.S. weedy rice is not an escaped lineage derived from U.S. cultivated rice populations; weedy rice likely differentiated prior to the selective sweep occurred in this gene within cultivated rice populations. Using the major seed shattering locus sh4 gene and the neighbouring genomic region, Thurber et al. (2010) track the molecular evolutionary history of the high shattering phenotype, a trait contributing dramatically to the success of crop selection in cultivated rice as well as the persistence and expansion of weedy red rice. In this study, the shared fixation of a sh4 mutation in both cultivated rice and weedy rice indicates that weedy rice arose subsequent to the strong selective sweep leading to significant reduction in seed shattering in cultivated rice.

Figure 1 Open in figure viewer PowerPoint A weedy, brown hulled red rice individual with long awns surrounded by a field of cultivated rice (photo by A. Lawton‐Rauh).     

The role of Bh4 in parallel evolution of hull colour in domesticated and weedy rice

The two independent domestication events in the genus Oryza that led to African and Asian rice offer an extremely useful system for studying the genetic basis of parallel evolution. This system is also characterized by parallel de‐domestication events, with two genetically distinct weedy rice biotypes in the US derived from the Asian domesticate. One important trait that has been altered by rice domestication and de‐domestication is hull colour. The wild progenitors of the two cultivated rice species have predominantly black‐coloured hulls, as does one of the two U.S. weed biotypes; both cultivated species and one of the US weedy biotypes are characterized by straw‐coloured hulls. Using Black hull 4 (Bh4) as a hull colour candidate gene, we examined DNA sequence variation at this locus to study the parallel evolution of hull colour variation in the domesticated and weedy rice system. We find that independent Bh4‐coding mutations have arisen in African and Asian rice that are correlated with the straw hull phenotype, suggesting that the same gene is responsible for parallel trait evolution. For the U.S. weeds, Bh4 haplotype sequences support current hypotheses on the phylogenetic relationship between the two biotypes and domesticated Asian rice; straw hull weeds are most similar to indica crops, and black hull weeds are most similar to aus crops. Tests for selection indicate that Asian crops and straw hull weeds deviate from neutrality at this gene, suggesting possible selection on Bh4 during both rice domestication and de‐domestication.     

Diversity and evolution of rice progenitors in Australia

In the thousands of years of rice domestication in Asia, many useful genes have been lost from the gene pool. Wild rice is a key source of diversity for domesticated rice. Genome sequencing has suggested that the wild rice populations in northern Australia may include novel taxa, within the AA genome group of close (interfertile) wild relatives of domesticated rice that have evolved independently due to geographic separation and been isolated from the loss of diversity associated with gene flow from the large populations of domesticated rice in Asia. Australian wild rice was collected from 27 sites from Townsville to the northern tip of Cape York. Whole chloroplast genome sequences and 4,555 nuclear gene sequences (more than 8 Mbp) were used to explore genetic relationships between these populations and other wild and domesticated rices. Analysis of the chloroplast and nuclear data showed very clear evidence of distinctness from other AA genome Oryza species with significant divergence between Australian populations. Phylogenetic analysis suggested the Australian populations represent the earliest‐branching AA genome lineages and may be critical resources for global rice food security. Nuclear genome analysis demonstrated that the diverse O. meridionalis populations were sister to all other AA genome taxa while the Australian O. rufipogon‐like populations were associated with the clade that included domesticated rice. Populations of apparent hybrids between the taxa were also identified suggesting ongoing dynamic evolution of wild rice in Australia. These introgressions model events similar to those likely to have been involved in the domestication of rice.     

Seeing red: the origin of grain pigmentation in US weedy rice

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.     

Conspecific crop-weed introgression influences evolution of weedy rice (Oryza sativa f. spontanea) across a geographical range

Background

Introgression plays an important role in evolution of plant species via its influences on genetic diversity and differentiation. Outcrossing determines the level of introgression but little is known about the relationships of outcrossing rates, genetic diversity, and differentiation particularly in a weedy taxon that coexists with its conspecific crop.

Methodology/Principal Findings

Eleven weedy rice (Oryza sativa f. spontanea) populations from China were analyzed using microsatellite (SSR) fingerprints to study outcrossing rate and its relationship with genetic variability and differentiation. To estimate outcrossing, six highly polymorphic SSR loci were used to analyze >5500 progeny from 216 weedy rice families, applying a mixed mating model; to estimate genetic diversity and differentiation, 22 SSR loci were analyzed based on 301 weedy individuals. Additionally, four weed-crop shared SSR loci were used to estimate the influence of introgression from rice cultivars on weedy rice differentiation. Outcrossing rates varied significantly (0.4∼11.7%) among weedy rice populations showing relatively high overall Nei''s genetic diversity (0.635). The observed heterozygosity was significantly correlated with outcrossing rates among populations (r² = 0.783; P<0.001) although no obvious correlation between outcrossing rates and genetic diversity parameters was observed. Allelic introgression from rice cultivars to their coexisting weedy rice was detected. Weedy rice populations demonstrated considerable genetic differentiation that was correlated with their spatial distribution (r² = 0.734; P<0.001), and possibly also influenced by the introgression from rice cultivars.

Conclusions/Significance

Outcrossing rates can significantly affect heterozygosity of populations, which may shape the evolutionary potential of weedy rice. Introgression from the conspecific crop rice can influence the genetic differentiation and possibly evolution of its coexisting weedy rice populations.     

Fine mapping of a gene causing hybrid pollen sterility between Yunnan weedy rice and cultivated rice (Oryza sativa L.) and phylogenetic analysis of Yunnan weedy rice

Weedy rice represents an important resource for rice improvement. The F₁ hybrid between the japonica wide compatibility rice cultivar 02428 and a weedy rice accession from Yunnan province (SW China) suffered from pollen sterility. Pollen abortion in the hybrid occurred at the early bicellular pollen stage, as a result of mitotic failure in the microspore, although the tapetum developed normally. Genetic mapping in a BC₁F₁ population (02428//Yunnan weedy rice (YWR)/02428) showed that a major QTL for hybrid pollen sterility (qPS-1) was present on chromosome 1. qPS-1 was fine-mapped to a 110 kb region known to contain the hybrid pollen sterility gene Sa, making it likely that qPS-1 is either identical to, or allelic with Sa. Interestingly, F₁ hybrid indicated that Dular and IR36 were assumed to carry the sterility-neutral allele, Sa ⁿ . Re-sequencing SaM and SaF, the two component genes present at Sa, suggested that variation for IR36 and Dular may be responsible for the loss of male sterility, and the qPS-1 sequence might be derived from wild rice or indica cultivars. A phylogenetic analysis based on microsatellite genotyping suggested that the YWR accession is more closely related to wild rice and indica type cultivars than to japonica types. Thus it is probable that the YWR accession evolved from a spontaneous hybrid between wild rice and an ancient cultivated strain of domesticated rice.     

Influence of plant domestication on plant-pollinator interactions: Floral attributes and floral visitor communities in wild and cultivated squash plants

Premise

Domestication of plant species results in phenotypic modifications and changes in biotic interactions. Most studies have compared antagonistic plant-herbivore interactions of domesticated plants and their wild relatives, but little attention has been given to how domestication influences plant-pollinator interactions. Floral attributes and interactions of floral visitors were compared between sister taxa of the genus Cucurbita (Cucurbitaceae), the domesticated C. moschata, C. argyrosperma ssp. argyrosperma and its wild progenitor C. argyrosperma ssp. sororia in the place of origin.

Methods

We conducted univariate and multivariate analyses to compare floral morphological traits and analyzed floral reward (nectar and pollen) quantity and quality between flowers of wild and domesticated Cucurbita taxa. Staminate and pistillate flowers of all three taxa were video recorded, and visitation and behavior of floral visitors were registered and analyzed.

Results

Most floral morphological characteristics of flowers of domesticated taxa were larger in both staminate and pistillate flowers. Staminate and pistillate flowers presented distinct correlations between floral traits and integration indices between domesticated and wild species. Additionally, pollen quantity and protein to lipid ratio were greater in domesticated species. Cucurbit pollen specialists, Eucera spp., had the highest probability of visit for all Cucurbita taxa.

Conclusions

We provide evidence that floral traits of domesticated and wild Cucurbita species experienced different selection pressures. Domesticated Cucurbita species may have more resources invested towards floral traits, thereby increasing attractiveness to pollinators and potentially plant reproductive success. Wild ancestor plant populations should be conserved in their centers of origin to preserve plant-pollinator interactions.     

Genetic variation and possible origins of weedy rice found in California

Control of weeds in cultivated crops is a pivotal component in successful crop production allowing higher yield and higher quality. In rice‐growing regions worldwide, weedy rice (Oryza sativa f. spontanea Rosh.) is a weed related to cultivated rice which infests rice fields. With populations across the globe evolving a suite of phenotypic traits characteristic of weeds and of cultivated rice, varying hypotheses exist on the origin of weedy rice. Here, we investigated the genetic diversity and possible origin of weedy rice in California using 98 simple sequence repeat (SSR) markers and an Rc gene‐specific marker. By employing phylogenetic clustering analysis, we show that four to five genetically distinct biotypes of weedy rice exist in California. Analysis of population structure and genetic distance among individuals reveals diverse evolutionary origins of California weedy rice biotypes, with ancestry derived from indica, aus, and japonica cultivated rice as well as possible contributions from weedy rice from the southern United States and wild rice. Because this diverse parentage primarily consists of weedy, wild, and cultivated rice not found in California, most existing weedy rice biotypes likely originated outside California.     

Origin of mitochondrial DNA diversity of domestic yaks

Background  

The domestication of plants and animals was extremely important anthropologically. Previous studies have revealed a general tendency for populations of livestock species to include deeply divergent maternal lineages, indicating that they were domesticated in multiple, independent events from genetically discrete wild populations. However, in water buffalo, there are suggestions that a similar deep maternal bifurcation may have originated from a single population. These hypotheses have rarely been rigorously tested because of a lack of sufficient wild samples. To investigate the origin of the domestic yak (Poephagus grunnies), we analyzed 637 bp of maternal inherited mtDNA from 13 wild yaks (including eight wild yaks from a small population in west Qinghai) and 250 domesticated yaks from major herding regions.     

All roads lead to weediness: Patterns of genomic divergence reveal extensive recurrent weedy rice origins from South Asian Oryza

Weedy rice (Oryza spp.), a weedy relative of cultivated rice (O. sativa), infests and persists in cultivated rice fields worldwide. Many weedy rice populations have evolved similar adaptive traits, considered part of the ‘agricultural weed syndrome’, making this an ideal model to study the genetic basis of parallel evolution. Understanding parallel evolution hinges on accurate knowledge of the genetic background and origins of existing weedy rice groups. Using population structure analyses of South Asian and US weedy rice, we show that weeds in South Asia have highly heterogeneous genetic backgrounds, with ancestry contributions both from cultivated varieties (aus and indica) and wild rice. Moreover, the two main groups of weedy rice in the USA, which are also related to aus and indica cultivars, constitute a separate origin from that of Asian weeds. Weedy rice populations in South Asia largely converge on presence of red pericarps and awns and on ease of shattering. Genomewide divergence scans between weed groups from the USA and South Asia, and their crop relatives are enriched for loci involved in metabolic processes. Some candidate genes related to iconic weedy traits and competitiveness are highly divergent between some weed‐crop pairs, but are not shared among all weed‐crop comparisons. Our results show that weedy rice is an extreme example of recurrent evolution, and suggest that most populations are evolving their weedy traits through different genetic mechanisms.     

Population genomics identifies the origin and signatures of selection of Korean weedy rice

Weedy rice is the same biological species as cultivated rice (Oryza sativa); it is also a noxious weed infesting rice fields worldwide. Its formation and population‐selective or ‐adaptive signatures are poorly understood. In this study, we investigated the phylogenetics, population structure and signatures of selection of Korean weedy rice by determining the whole genomes of 30 weedy rice, 30 landrace rice and ten wild rice samples. The phylogenetic tree and results of ancestry inference study clearly showed that the genetic distance of Korean weedy rice was far from the wild rice and near with cultivated rice. Furthermore, 537 genes showed evidence of recent positive or divergent selection, consistent with some adaptive traits. This study indicates that Korean weedy rice originated from hybridization of modern indica/indica or japonica/japonica rather than wild rice. Moreover, weedy rice is not only a notorious weed in rice fields, but also contains many untapped valuable traits or haplotypes that may be a useful genetic resource for improving cultivated rice.     

Gene Flow and its Consequences in Sorghum spp.

Gene flow between crops and their weedy or wild relatives can be problematic in modern agricultural systems, especially if it endows novel adaptive genes that confer tolerance to abiotic and biotic stresses. Alternatively, gene flow from weedy relatives to domesticated crops may facilitate ferality through introgression of weedy characteristics in the progeny. Cultivated sorghum (Sorghum bicolor), is particularly vulnerable to the risks associated with gene flow to several weedy relatives, johnsongrass (S. halepense), shattercane (S. bicolor ssp. drummondii) and columbusgrass (S. almum). Johnsongrass and shattercane are common weeds in many sorghum production areas around the world. Sorghum varieties with adaptive traits developed through conventional breeding or novel transgenesis pose agronomic and ecological risks if transferred into weedy/wild relatives. Knowledge of the nature and characteristics of gene flow among different sorghum species is scarce, and existing knowledge is scattered. Here, we review current knowledge of gene flow between cultivated sorghum and its weedy and wild relatives. We further discuss potential avenues for addressing gene flow through genetic, molecular, and field level containment, mitigation and management strategies to facilitate successful deployment of novel traits in this economically important crop species.     

杂草稻叶绿体籼粳分化的多重PCR分析

通过分析籼稻93-11和粳稻培矮64S的叶绿体全基因组,优化和构建了籼粳分化的叶绿体分子标记ORF100和ORF29-TrnC^GCA的多重PCR。应用这个多重PCR对200余份世界各地杂草稻和其它水稻材料进行分析。结果表明:杂草稻中有明显的叶绿体籼粳分化,表现出明显的地域性,且与传统的中国栽培稻的南籼北粳能较好的对应。推测粳型杂草稻可能是栽培稻突变或粳型水稻(作母本)与其它类型水稻材料杂交而形成的。     

Genetic diversity and relationships in mulberry (genusMorus) as revealed by RAPD and ISSR marker assays

Background  

The genus Morus, known as mulberry, is a dioecious and cross-pollinating plant that is the sole food for the domesticated silkworm, Bombyx mori. Traditional methods using morphological traits for classification are largely unsuccessful in establishing the diversity and relationships among different mulberry species because of environmental influence on traits of interest. As a more robust alternative, PCR based marker assays including RAPD and ISSR were employed to study the genetic diversity and interrelationships among twelve domesticated and three wild mulberry species.     

Molecular evolution of the rice blast resistance gene Pi-ta in invasive weedy rice in the USA

The Pi-ta gene in rice has been effectively used to control rice blast disease caused by Magnaporthe oryzae worldwide. Despite a number of studies that reported the Pi-ta gene in domesticated rice and wild species, little is known about how the Pi-ta gene has evolved in US weedy rice, a major weed of rice. To investigate the genome organization of the Pi-ta gene in weedy rice and its relationship to gene flow between cultivated and weedy rice in the US, we analyzed nucleotide sequence variation at the Pi-ta gene and its surrounding 2 Mb region in 156 weedy, domesticated and wild rice relatives. We found that the region at and around the Pi-ta gene shows very low genetic diversity in US weedy rice. The patterns of molecular diversity in weeds are more similar to cultivated rice (indica and aus), which have never been cultivated in the US, rather than the wild rice species, Oryza rufipogon. In addition, the resistant Pi-ta allele (Pi-ta) found in the majority of US weedy rice belongs to the weedy group strawhull awnless (SH), suggesting a single source of origin for Pi-ta. Weeds with Pi-ta were resistant to two M. oryzae races, IC17 and IB49, except for three accessions, suggesting that component(s) required for the Pi-ta mediated resistance may be missing in these accessions. Signatures of flanking sequences of the Pi-ta gene and SSR markers on chromosome 12 suggest that the susceptible pi-ta allele (pi-ta), not Pi-ta, has been introgressed from cultivated to weedy rice by out-crossing.     

Sequencing of Australian wild rice genomes reveals ancestral relationships with domesticated rice

The related A genome species of the Oryza genus are the effective gene pool for rice. Here, we report draft genomes for two Australian wild A genome taxa: O. rufipogon‐like population, referred to as Taxon A, and O. meridionalis‐like population, referred to as Taxon B. These two taxa were sequenced and assembled by integration of short‐ and long‐read next‐generation sequencing (NGS) data to create a genomic platform for a wider rice gene pool. Here, we report that, despite the distinct chloroplast genome, the nuclear genome of the Australian Taxon A has a sequence that is much closer to that of domesticated rice (O. sativa) than to the other Australian wild populations. Analysis of 4643 genes in the A genome clade showed that the Australian annual, O. meridionalis, and related perennial taxa have the most divergent (around 3 million years) genome sequences relative to domesticated rice. A test for admixture showed possible introgression into the Australian Taxon A (diverged around 1.6 million years ago) especially from the wild indica/O. nivara clade in Asia. These results demonstrate that northern Australia may be the centre of diversity of the A genome Oryza and suggest the possibility that this might also be the centre of origin of this group and represent an important resource for rice improvement.