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A two-locus interaction causes interspecific hybrid weakness in rice.

ABSTRACT: Reproductive barriers perform a vital role during speciation. Hybrid weakness, the poorer development of hybrids compared with their parents, hinders gene exchange between different species at the postzygotic stage. Here we show that two incompatible dominant loci (Hwi1 and Hwi2) involving three genes are likely to determine the high temperature-dependent expression of hybrid weakness in interspecific hybrids of rice. Hwi1 comprises two leucine-rich repeat receptor-like kinase (LRR-RLK) genes, 25L1 and 25L2, which are specific to wild rice (Oryza rufipogon) and induce hybrid weakness. Hwi2, a rare allele that is predominantly distributed in indica rice (Oryza sativa), encodes a secreted putative subtilisin-like protease. Functional analysis indicated that pyramiding of Hwi1 and Hwi2 activates the autoimmune response in the basal nodes of hybrids, interrupting root formation and then impairing shoot growth. These findings bring new insights into our understanding of reproductive isolation and may benefit rice breeding.

SUBMITTER: Chen C

PROVIDER: S-EPMC3948059 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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A two-locus interaction causes interspecific hybrid weakness in rice.

Chen Chen C Chen Hao H Lin You-Shun YS Shen Jin-Bo JB Shan Jun-Xiang JX Qi Peng P Shi Min M Zhu Mei-Zhen MZ Huang Xue-Hui XH Feng Qi Q Han Bin B Jiang Liwen L Gao Ji-Ping JP Lin Hong-Xuan HX

Nature communications 20140101

Reproductive barriers perform a vital role during speciation. Hybrid weakness, the poorer development of hybrids compared with their parents, hinders gene exchange between different species at the postzygotic stage. Here we show that two incompatible dominant loci (Hwi1 and Hwi2) involving three genes are likely to determine the high temperature-dependent expression of hybrid weakness in interspecific hybrids of rice. Hwi1 comprises two leucine-rich repeat receptor-like kinase (LRR-RLK) genes, 2 ...[more]

PMID: 24556665

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Project description:Reproductive barriers perform a vital role during speciation1. Hybrid weakness, the poor development of hybrids compared to their parents, hinders gene exchange between different species at the postzygotic stage2,3. The molecular and evolutionary mechanisms of hybrid weakness are poorly understood2. Here, we report that two incompatible dominant loci (Hwi1 and Hwi2) involving three genes determine the high temperature-dependent expression of hybrid weakness in interspecific hybrids of rice. Hwi1 comprises two indispensable wild rice (Oryza rufipogon)-specific leucine-rich repeat receptor-like kinase (LRR-RLK) genes, 25L1 and 25L2, for inducing hybrid weakness, and the genes possibly undergo balancing selection. Hwi2, a rare allele that is predominantly distributed in indica rice (Oryza sativa), encodes a secreted putative subtilisin-like protease. Functional analysis indicated that pyramiding of Hwi1 and Hwi2 activates the autoimmune response in the basal nodes of hybrids, interrupting root formation and then impairing shoot growth, likely due to immune signal is transmitted from the basal nodes to the above-ground parts. Considering the nature of RLK activity of Hwi1 and the protease activity of Hwi2, we propose that a certain endogenous signaling molecule produced by Hwi2 is perceived by Hwi1 to activate autoimmunity through ligand-receptor signal transduction. These findings bring new insights into our understanding of reproductive isolation and may benefit rice breeding to maximally utilize invaluable genes from wild rice. We conducted microarray analysis to unravel the global changes in gene expression of a pair of NILs (nearly isogenic lines). Plants were cultivated at constant 20°C for 20 days and then shifted to constant 30°C conditions. The basal nodes of NIL(Hwi1) and NIL(hwi1) were harvested immediately before the temperature shift (set as the 0 point) or at 3, 7 or 15 days after the shift. Three biological replicates (each comprising basal nodes from 15–20 individuals) were used for each time point.

Project description:Reproductive isolation is an obstacle for plant breeding when a distant cross is demanded. It can be divided into two main types based on different growth stages: prezygotic isolation and postzygotic isolation. The hybrid weakness, which is a type of postzygotic isolation, can become a problem in crop breeding. In order to overcome reproductive isolation, it is necessary to elucidate its mechanism. In this study, genetic analysis for low temperature-dependent hybrid weakness was conducted in a rice F2 population derived from Taichung 65 (T65, Japonica) and Lijiangxintuanheigu (LTH, Japonica). The weak and severe weak plants in F2 showed shorter culm length, late heading, reduced panicle number, decreased grain numbers per panicle, and impaired root development in the field. Our result also showed that hybrid weakness was affected by temperature. It was observed that 24°C enhanced hybrid weakness, whereas 34°C showed recovery from hybrid weakness. In terms of the morphology of embryos, no difference was observed. Therefore, hybrid weakness affects postembryonic development and is independent of embryogenesis. The genotypes of 126 F2 plants were determined through genotyping-by-sequencing and a linkage map consisting of 862 single nucleotide polymorphism markers was obtained. Two major quantitative trait loci (QTLs) were detected on chromosomes 1 [hybrid weakness j 1 (hwj1)] and 11 [hybrid weakness j 2 (hwj2)]. Further genotyping indicated that the hybrid weakness was due to an incompatible interaction between the T65 allele of hwj1 and the LTH allele of hwj2. A large F2 populations consisting of 5,722 plants were used for fine mapping of hwj1 and hwj2. The two loci, hwj1 and hwj2, were mapped in regions of 65-kb on chromosome 1 and 145-kb on chromosome 11, respectively. For hwj1, the 65-kb region contained 11 predicted genes, while in the hwj2 region, 22 predicted genes were identified, two of which are disease resistance-related genes. The identified genes along these regions serve as preliminary information on the molecular networks associated with hybrid weakness in rice.

Project description:Interspecific and intraspecific hybrid sterility is a typical and common phenomenon of postzygotic reproductive barrier in rice. This is an indicator of speciation involved in the formation of new species or subspecies, and it significantly hampers the utilization of favorable genes from distant parents for rice improvement. The Oryza genus includes eight species with the same AA genome and is a model plant for studying the nature of hybrid sterility and its relationship with speciation. Hybrid sterility in rice is mostly controlled by nuclear genes, with more than 50 sterility loci genetically identified to date, of which 10 hybrid sterility loci or pairs were cloned and characterized at the molecular level. Comparing the mapping results for all sterility loci reported indicated that some of these loci from different species should be allelic to each other. Further research revealed that interactions between the multiple alleles at the hybrid sterility locus caused various genetic effect. One hypothesis for this important phenomenon is that the hybrid sterility loci are orthologous loci, which existed in ancient ancestors of rice. When one or more ancestors drifted to different continents, genetic divergence occurred because of adaptation, selection, and isolation among them such that various alleles from orthologous loci emerged over evolutionary time; hence, interspecific hybrid sterility would be mainly controlled by a few orthologous loci with different alleles. This hypothesis was tested and supported by the molecular characterization of hybrid sterility loci from S1, S5, Sa, qHMS7, and S27. From this, we may further deduce that both allelic and non-allelic interactions among different loci are the major genetic basis for the interspecific hybrid sterility between O. sativa and its AA genome relatives, and the same is true for intraspecific hybrid sterility in O. sativa. Therefore, it is necessary to raise the near-isogenic lines with various alleles/haplotypes and pyramided different alleles/haplotypes from sterile loci in the same genetic background aiming to study allelic and non-allelic interaction among different hybrid sterility loci in the AA genome species. Furthermore, the pyramiding lines ought to be used as bridge parents to overcome hybrid sterility for rice breeding purposes.

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A two-locus interaction causes interspecific hybrid weakness in rice.

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A two-locus interaction causes interspecific hybrid weakness in rice.

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