Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes

Mizuta, Yoko; Harushima, Yoshiaki; Kurata, Nori

doi:10.1073/pnas.1003124107

Cited by 165 publications

(209 citation statements)

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“…Because the wild relatives of rice are adapted to different biogeographic ranges (Fig. 1a) and can tolerate many biotic and abiotic stresses [1][2][3][4][5][6] , they constitute an important reservoir for crop improvement. Strategies to harness such traits for crop improvement show clear promise, as exemplified by the introgression of bacterial blight resistance (Xa21) from the wild species Oryza longistaminata 7 .…”

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Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

et al. 2018

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Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

et al. 2018

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“…In plants, it is not yet clear how often natural selection is a primary driver of hybrid incompatibilities. In several cases, hybrid dysfunction is caused by divergence at duplicate genes in a manner consistent with the action of random genetic drift (Bikard et al 2009;Mizuta et al 2010;Yamagata et al 2010). On the other hand, it was recently shown that a hybrid lethality allele has risen to high frequency in a population of M. guttatus due to linked selection for an allele that confers copper tolerance (Wright et al 2013).…”

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confidence: 99%

“…In Arabidopsis and rice, genetic incompatibilities have been mapped to duplicate genes that carry loss-of-function alleles in alternate copies (Bikard et al 2009;Mizuta et al 2010;Yamagata et al 2010), suggesting that divergence among paralogs via mutation and genetic drift might cause postzygotic reproductive isolation (Lynch and Force 2000). There are also hints that natural selection can contribute to the spread of incompatible alleles within populations and species.…”

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Evidence of Natural Selection Acting on a Polymorphic Hybrid Incompatibility Locus in Mimulus

Sweigart

Flagel

2014

Genetics

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As a common cause of reproductive isolation in diverse taxa, hybrid incompatibilities are fundamentally important to speciation. A key question is which evolutionary forces drive the initial substitutions within species that lead to hybrid dysfunction. Previously, we discovered a simple genetic incompatibility that causes nearly complete male sterility and partial female sterility in hybrids between the two closely related yellow monkeyflower species Mimulus guttatus and M. nasutus. In this report, we fine map the two major incompatibility loci-hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2)-to small nuclear genomic regions (each ,70 kb) that include strong candidate genes. With this improved genetic resolution, we also investigate the evolutionary dynamics of hms1 in a natural population of M. guttatus known to be polymorphic at this locus. Using classical genetic crosses and population genomics, we show that a 320-kb region containing the hms1 incompatibility allele has risen to intermediate frequency in this population by strong natural selection. This finding provides direct evidence that natural selection within plant species can lead to hybrid dysfunction between species.KEYWORDS speciation; hybrid incompatibilities; postzygotic reproductive isolation; Mimulus; monkeyflower S PECIATION occurs when diverging populations accumulate genetic differences that cause reproductive isolation. Many forms of prezygotic reproductive isolation likely evolve as byproducts of adaptation to different ecological conditions (e.g., habitat or behavioral differences), but the evolutionary dynamics of intrinsic postzygotic isolation are less clear. This is because the production of dead or sterile hybrids cannot be favored by natural selection. Dobzhansky (1937) and Muller (1942) proposed a solution to this long-standing mystery (Darwin 1859), explaining that a new mutation might function perfectly well with alleles present in its native species, and only cause sterility or inviability when found in a hybrid genetic background. The so-called Dobzhansky-Muller model shows that natural selection need not oppose the evolution of hybrid dysfunction, but it makes no predictions about the nature of the genetic changes or the evolutionary forces that give rise to hybrid incompatibilities.The recent identification of several hybrid incompatibility genes in diverse taxa has begun to reveal some insights into the evolution of hybrid dysfunction (reviewed in Presgraves 2010; Maheshwari and Barbash 2011;Sweigart and Willis 2012). In Arabidopsis and rice, genetic incompatibilities have been mapped to duplicate genes that carry loss-of-function alleles in alternate copies (Bikard et al. 2009;Mizuta et al. 2010;Yamagata et al. 2010), suggesting that divergence among paralogs via mutation and genetic drift might cause postzygotic reproductive isolation (Lynch and Force 2000). There are also hints that natural selection can contribute to the spread of incompatible alleles within populations and species. For example, ...

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“…Classical two-locus BDM interactions between differentially inactivated duplicated genes appear to cause pollen sterility in hybrids between Oryza sativa and O. glumaepatula (Yamagata et al 2010) and between the two O. sativa subspecies japonica and indica (Mizuta et al 2010). 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.…”

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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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Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes

Cited by 165 publications

References 45 publications

Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

Evidence of Natural Selection Acting on a Polymorphic Hybrid Incompatibility Locus in Mimulus

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

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