A Killer-Protector System Regulates Both Hybrid Sterility and Segregation Distortion in Rice

Yang, Jiangyi; Zhao, Xiaobo; Cheng, Ke; Du, Hongyi; Ouyang, Yidan; Chen, Jiongjiong; Qiu, Shuqing; Huang, Jianyan; Jiang, Yunhe; Jiang, Liwen; Ding, Jiajia; Wang, Jia; Xu, Caiguo; Li, Xianghua; Zhang, Qifa

doi:10.1126/science.1223702

Cited by 252 publications

(262 citation statements)

References 38 publications

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“…Kubo et al (2008) showed that hybrid male sterility is caused by epistasis between two novel genes, S24 and S35, on rice chromosomes 5 and 1. Similar results have also been found in Drosophila (Chang and Noor, 2010), alfalfa (Li et al, 2011), rice (Xie and Chen, 2012;Yang et al, 2012) and Arabidopsis lyrata (Leppälä et al, 2013). Thus, the Dobzhansky-Muller model, in which hybrid inviability is assumed to be caused by epistasis (Dobzhansky, 1936;Muller, 1942), has been widely accepted.…”

Section: Introductionsupporting

confidence: 65%

Linkage group correction using epistatic distorted markers in F2 and backcross populations

Zhang

2014

Heredity

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Epistasis has been frequently observed in all types of mapping populations. However, relatively little is known about the effect of epistatic distorted markers on linkage group construction. In this study, a new approach was proposed to correct the recombination fraction between epistatic distorted markers in backcross and F 2 populations under the framework of fitness and liability models. The information for three or four markers flanking with an epistatic segregation distortion locus was used to estimate the recombination fraction by the maximum likelihood method, implemented via an expectation-maximisation algorithm. A set of Monte Carlo simulation experiments along with a real data analysis in rice was performed to validate the new method. The results showed that the estimates from the new method are unbiased. In addition, five statistical properties for the new method in a backcross were summarised and confirmed by theoretical, simulated and real data analyses.

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Section: Introductionsupporting

confidence: 65%

Linkage group correction using epistatic distorted markers in F2 and backcross populations

Zhang

2014

Heredity

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“…S19-S23 and Table S36). We further examined the other two ORFs (ORF3 and ORF4) at this locus that work with ORF5 to form a killer-protector system (46). In the high-quality assemblies of S5 orthologous genomic regions for all five newly sequenced genomes, our results showed that ORF3 was fragmented and ORF4 was not detected in both GLA and BAR genomes.…”

Section: Resultsmentioning

confidence: 84%

Rapid diversification of five Oryza AA genomes associated with rice adaptation

Zhang

Zhu

Xia

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

138

149

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Comparative genomic analyses among closely related species can greatly enhance our understanding of plant gene and genome evolution. We report de novo-assembled AA-genome sequences for Oryza nivara, Oryza glaberrima, Oryza barthii, Oryza glumaepatula, and Oryza meridionalis. Our analyses reveal massive levels of genomic structural variation, including segmental duplication and rapid gene family turnover, with particularly high instability in defense-related genes. We show, on a genomic scale, how lineage-specific expansion or contraction of gene families has led to their morphological and reproductive diversification, thus enlightening the evolutionary process of speciation and adaptation. Despite strong purifying selective pressures on most Oryza genes, we documented a large number of positively selected genes, especially those genes involved in flower development, reproduction, and resistance-related processes. These diversifying genes are expected to have played key roles in adaptations to their ecological niches in Asia, South America, Africa and Australia. Extensive variation in noncoding RNA gene numbers, function enrichment, and rates of sequence divergence might also help account for the different genetic adaptations of these rice species. Collectively, these resources provide new opportunities for evolutionary genomics, numerous insights into recent speciation, a valuable database of functional variation for crop improvement, and tools for efficient conservation of wild rice germplasm.comparative genomics | full-genome sequencing | genomic variation | positive selection | Oryza D rawing the landscape of genomic divergence among multiple lineages is fundamental to understanding plant gene and genome evolution (1, 2). The comprehensive comparison of closely related genomes in different chronologically ordered stages under a well-resolved phylogenetic framework could dramatically improve the inference precision and sensitivity of gene evolution studies and should allow more robust results for investigating broad-scale patterns of genomic architecture in the course of the speciation process compared with analyses of single genomes (3, 4). For instance, studies of yeast, Drosophila, and human genomes have demonstrated how comparisons of closely related genome sequences can reveal mechanisms of gene and genome evolution in fungi and animals (5-7). In plants, however, we know little about broad-scale patterns of evolutionary dynamics, differentiation, and consequences. Studies are needed of very closely related plant species that span the speciation continuum and have well-characterized biogeographic histories.The genus Oryza, consisting of 24 species, provides a uniquely powerful system for studying comparative genomics and evolutionary biology, and can contribute to the improvement of rice, which is of pivotal significance in worldwide food production and security (8-10). Many genes involved in rice improvement are derived from wild AA-genome species, and broadening the gene pool of cultivated rice through i...

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“…In rice in particular, a number of gamete killers have been described in crosses between cultivated rice (O. sativa) and its wild relatives (Sano 1990;Hu et al 2006;Garavito et al 2010), or between O. sativa subspecies (Oka 1974;Zhang et al 2006). The genes underlying two of the latter have been identified (Chen et al 2008;Long et al 2008;Yang et al 2012). Gamete killers are also found in wild species, as in the interspecific cross between Mimulus guttatus and M. nasutus (Fishman and Saunders 2008), and, at the intraspecific level, in some populations of the dioecious Silene latifolia (Taylor and Ingvarsson 2003).…”

Section: Discussionmentioning

confidence: 99%

“…In both of these BDM interactions, a particular combination of alleles present at the two loci is deleterious at the haploid stage, leading to the production of deficient pollen grains in the hybrid plant. In addition, at least two examples of one-locus hybrid sterility have been reported in rice (Long et al 2008;Yang et al 2012). In these cases, hybrid sterility results from the abortion of the gametophytes (pollen grains in one case, embryo sacs in the other) that carry one of the parental alleles, when in the presence of the other allele in the hybrid.…”

mentioning

confidence: 99%

Genomic Conflicts that Cause Pollen Mortality and Raise Reproductive Barriers inArabidopsis thaliana

et al. 2016

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Species differentiation and the underlying genetics of reproductive isolation are central topics in evolutionary biology. Hybrid sterility is one kind of reproductive barrier that can lead to differentiation between species. Here, we analyze the complex genetic basis of the intraspecific hybrid male sterility that occurs in the offspring of two distant natural strains of Arabidopsis thaliana, Shahdara and Mr-0, with Shahdara as the female parent. Using both classical and quantitative genetic approaches as well as cytological observation of pollen viability, we demonstrate that this particular hybrid sterility results from two causes of pollen mortality. First, the Shahdara cytoplasm induces gametophytic cytoplasmic male sterility (CMS) controlled by several nuclear loci. Second, several segregation distorters leading to allele-specific pollen abortion (pollen killers) operate in hybrids with either cytoplasm. The complete sterility of the hybrid with the Shahdara cytoplasm results from the genetic linkage of the two causes of pollen mortality, i.e., CMS nuclear determinants and pollen killers. Furthermore, natural variation at these loci in A. thaliana is associated with different malesterility phenotypes in intraspecific hybrids. Our results suggest that the genomic conflicts that underlie segregation distorters and CMS can concurrently lead to reproductive barriers between distant strains within a species. This study provides a new framework for identifying molecular mechanisms and the evolutionary history of loci that contribute to reproductive isolation, and possibly to speciation. It also suggests that two types of genomic conflicts, CMS and segregation distorters, may coevolve in natural populations.

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A Killer-Protector System Regulates Both Hybrid Sterility and Segregation Distortion in Rice

Cited by 252 publications

References 38 publications

Linkage group correction using epistatic distorted markers in F2 and backcross populations

Linkage group correction using epistatic distorted markers in F2 and backcross populations

Rapid diversification of five Oryza AA genomes associated with rice adaptation

Genomic Conflicts that Cause Pollen Mortality and Raise Reproductive Barriers inArabidopsis thaliana

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