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Understanding the Nature of Hybrid Sterility and Divergence of Asian Cultivated Rice

ABSTRACT: Intraspecific hybrid sterility is a common form of postzygotic reproductive isolation in Asian cultivated rice, which is also the major obstacle to utilize the strong heterosis in the rice breeding program. Here, we review recent progress in classification and hybrid sterility in Asian cultivated rice. A genome-wide analysis of numerous wild relatives of rice and Asian cultivated rice has provided insights into the origin and differentiation of Asian cultivated rice, and divided Asian cultivated rice into five subgroups. More than 40 conserved and specific loci were identified to be responsible for the hybrid sterility between subgroup crosses by genetic mapping, which also contributed to the divergence of Asian cultivated rice. Most of the studies are focused on the sterile barriers between indica and japonica crosses, ignoring hybrid sterility among other subgroups, leading to neither a systematical understanding of the nature of hybrid sterility and subgroup divergence, nor effectively utilizing strong heterosis between the subgroups in Asian cultivated rice. Future studies will aim at identifying and characterizing genes for hybrid sterility and segregation distortion, comparing and understanding the molecular mechanism of hybrid sterility, and drawing a blueprint for intraspecific hybrid sterility loci derived from cross combinations among the five subgroups. These studies would provide scientific and accurate guidelines to overcome the intraspecific hybrid sterility according to the parent subgroup type identification, allowing the utilization of heterosis among subgroups, also helping us unlock the mysterious relationship between hybrid sterility and Asian cultivated rice divergence.

SUBMITTER: Zhang Y

PROVIDER: S-EPMC9272003 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

Project description:A strong postzygotic reproductive barrier separates the recently diverged Asian and African cultivated rice species, Oryza sativa and O. glaberrima. Recently a model of genetic incompatibilities between three adjacent loci: S(1)A, S(1) and S(1)B (called together the S(1) regions) interacting epistatically, was postulated to cause the allelic elimination of female gametes in interspecific hybrids. Two candidate factors for the S(1) locus (including a putative F-box gene) were proposed, but candidates for S(1)A and S(1)B remained undetermined. Here, to better understand the basis of the evolution of regions involved in reproductive isolation, we studied the genic and structural changes accumulated in the S(1) regions between orthologous sequences. First, we established an 813 kb genomic sequence in O. glaberrima, covering completely the S(1)A, S(1) and the majority of the S(1)B regions, and compared it with the orthologous regions of O. sativa. An overall strong structural conservation was observed, with the exception of three isolated regions of disturbed collinearity: (1) a local invasion of transposable elements around a putative F-box gene within S(1), (2) the multiple duplication and subsequent divergence of the same F-box gene within S(1)A, (3) an interspecific chromosomal inversion in S(1)B, which restricts recombination in our O. sativa×O. glaberrima crosses. Beside these few structural variations, a uniform conservative pattern of coding sequence divergence was found all along the S(1) regions. Hence, the S(1) regions have undergone no drastic variation in their recent divergence and evolution between O. sativa and O. glaberrima, suggesting that a small accumulation of genic changes, following a Bateson-Dobzhansky-Muller (BDM) model, might be involved in the establishment of the sterility barrier. In this context, genetic incompatibilities involving the duplicated F-box genes as putative candidates, and a possible strengthening step involving the chromosomal inversion might participate to the reproductive barrier between Asian and African rice species.

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Understanding the Nature of Hybrid Sterility and Divergence of Asian Cultivated Rice

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