A two-locus interaction causes interspecific hybrid weakness in rice

Chen, Chen; Chen, Hao; Lin, Youshun; Shen, Jinbo; Shan, Jun-Xiang; Peng, Qi; Shi, Min; Zhu, Meizhen; Huang, Xuehui; Feng, Qi; Han, Bin; Jiang, Liwen; Gao, Jinliang; Lin, Hong‐Xuan

doi:10.1038/ncomms4357

Cited by 94 publications

(133 citation statements)

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“…In addition, a chemically induced allele at a gene encoding a cysteine synthase can combine with a natural DM2 allele to cause necrosis (Tahir et al, 2012). Outside of A. thaliana , hybrid necrosis alleles encode a cysteine protease (Krüger et al, 2002), a kinase (Yamamoto et al, 2010) and a subtilisin-like protease (Chen et al, 2014). Enzyme-encoding genes are clearly enriched, but in most cases we do not know yet how they modulate the activity of NLRs.…”

Section: Discussionmentioning

confidence: 99%

“…Of the six causal loci that have been positively identified, one encodes an NLR and another one a known NLR-interactor. In addition, the mapping interval for one of the remaining loci includes several NLRs (Chen et al, 2014; Jeuken et al, 2009; Krüger et al, 2002; Yamamoto et al, 2010). Similarly, the first hybrid necrosis gene positively identified in Arabidopsis thaliana , DANGEROUS MIX1 ( DM1 ), encodes an NLR.…”

Section: Introductionmentioning

confidence: 99%

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Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis

Chae

Bomblies

Kim

et al. 2014

Cell

256

300

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Summary Intraspecific genetic incompatibilities prevent the assembly of specific alleles into single genotypes and influence genome- and species-wide patterns of sequence variation. A common incompatibility in plants is hybrid necrosis, characterized by autoimmune responses due to epistatic interactions between natural genetic variants. By systematically testing thousands of F1 hybrids of Arabidopsis thaliana strains, we identified a small number of incompatibility hotspots in the genome, often in regions densely populated by NLR immune receptor genes. In several cases, these immune receptor loci interact with each other, suggestive of conflict within the immune system. A particularly dangerous locus is a highly variable cluster of NLR genes, DANGEROUS MIX2 (DM2), which causes multiple, independent incompatibilities with genes that encode a range of biochemical functions, including NLRs. Our findings suggest that deleterious interactions of immune receptors at the front lines of host-pathogen co-evolution limit the combinations of favorable disease resistance alleles accessible to plant genomes.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis

Chae

Bomblies

Kim

et al. 2014

Cell

256

300

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“…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). Natural selection is also presumed to play a role in divergence among disease resistance genes that cause hybrid necrosis in Arabidopsis and rice (Kruger et al 2002;Alcazar et al 2009;Jeuken et al 2009;Yamamoto et al 2010;Chen et al 2014), although direct population genetic evidence is lacking. Likewise, the genes that cause cytoplasmic male sterility between Mimulus species (involving the same IM62 and SF lines used in this study) seem more likely to have evolved by selfish mitochondrial evolution and compensatory nuclear coevolution than by genetic drift (Barr and Fishman 2010).…”

Section: Discussionmentioning

confidence: 99%

“…There are also hints that natural selection can contribute to the spread of incompatible alleles within populations and species. For example, plant hybrid necrosis has been mapped repeatedly to disease resistance genes (Krüger et al 2002; Alcazar et al 2009;Jeuken et al 2009;Yamamoto et al 2010;Chen et al 2014), which are likely targets of adaptive divergence to unique pathogen communities (Bomblies and Weigel 2007). Additionally, many hybrid incompatibility genes show molecular signatures of positive selection (Presgraves et al 2003;Brideau et al 2006;Maheshwari et al 2008;Oliver et al 2009;Phadnis and Orr 2009;Tang and Presgraves 2009), but, interestingly, few of these genes seem to be involved in classical ecological adaptation.…”

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confidence: 99%

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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“…Recently, Chen et al (2014) identified two incompatible dominant loci, Hwi1 and Hwi2, controlling the hybrid weakness in the interspecific hybrids of rice. These two loci are located on chromosome 11 and 1, respectively.…”

Section: Introductionmentioning

confidence: 99%

Genetic dissection of hybrid breakdown in an indica/japonica cross and fine mapping of a quantitative trait locus qSF-12 in rice (Oryza sativa L.)

Guo

et al. 2015

Mol Breeding

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Hybrid breakdown is an important form of post-zygotic reproductive barriers, often arising from hybrid progeny between two varietal groups of Asian cultivated rice (Oryza sativa L.), indica and japonica. However, the genetic mechanism underlying the hybrid breakdown remains unclear. In the present study, a chromosomal segment substitute line (CSSL) population together with a backcross inbred line population, derived from the same cross of Sasanishiki/Habataki, were employed for genetic analysis of rice hybrid breakdown (spikelet fertility as index). Quantitative trait locus mapping results showed that, in both populations, qSF-12 was stably detected across different locations and growing seasons, which was found to interact with qSF-8. Subsequently, a CSSL line SL438 with low spikelet fertility was used to cross with Sasanishiki to generate the secondary F 2 population for the mapping of qSF-12. The results showed that qSF-12 was restricted to a 137-kb long region on BAC clone AL928774, containing 11 predicted ORFs in total. The DNA sequencing revealed that a 3-bp insertion/deletion exists between two parents in the coding region of LOC_Os12g38850. Together with the RNA-seq data, it is suggested that LOC_Os12-g38850is the putative candidate of qSF-12, which encodes a DUF1336 domain containing protein. These results provide an important clue to further dissect the mechanism of hybrid breakdown in rice and the linked markers will be useful in rice cross breeding.

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A two-locus interaction causes interspecific hybrid weakness in rice

Cited by 94 publications

References 44 publications

Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis

Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis

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

Genetic dissection of hybrid breakdown in an indica/japonica cross and fine mapping of a quantitative trait locus qSF-12 in rice (Oryza sativa L.)

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