Understanding and breaking down the reproductive barrier between Asian and African cultivated rice: a new start for hybrid rice breeding

Abstract

Oryza sativa and O. glaberrima, commonly known as Asian and African cultivated rice, are two domesticated rice species in Oryza genus. Asian cultivated rice may produce higher yields with better quality, whereas African cultivated rice shows a wide range of tolerance to abiotic and biotic stresses. Interspecific hybrids between O. sativa and O. glaberrima would show strong heterosis and thus increasing production because of their distant genetic diversity and complementary agronomic traits. However, reduced fertility is observed in hybrids from interspecific crosses; this hinders further utilization of rice heterosis in agriculture production. Such severe abnormal development of gametophytes in hybrids is caused by reproductive isolation, a process that prevents individuals of genetically diverged groups from mating, survival or producing fertile offspring. These reproductive barriers would drive speciation and maintain species identity by restriction of gene flow between differentiated populations. Therefore, understanding the genetic and molecular basis of reproductive isolation represents a fundamental concern in evolutionary biology. Near thirty years after the first glimpse of the reproductive barrier between O. sativa and O. glaberrima (Sano, 1990), the genetic factors regulating incompatibility between these two cultivated rice species have now been unveiled. The S1 locus is an important speciation locus as it affects both male and female sterility in hybrids from such interspecific crosses. Genetically, the gametes carrying S1 alleles from Asian rice are selectively eliminated, leading to preferential transmission of the African alleles at S1 locus and consequently male and female sterilities in the heterozygotes. By a first glance of the causal gene(s) responsible for S1 locus two years ago, researchers from South China Agricultural University and their collaborators identified the involvement of an O. glaberrima-divergent gene OgTPR1 in S1-mediated hybrid sterility (Xie et al., 2017), followed by identification of another O. glaberrima-specific peptidase-coding gene SSP at S1 locus by Koide and his colleagues (Koide et al., 2018). A complete understanding of such Asian-African reproductive barrier has now been released by the same team in South China Agricultural University and their collaborators (Xie et al., 2019a). In this study, they identified a classical killer-protector system driving an extremely asymmetric allelic interaction in interspecific rice hybrids. Three tightly linked genes in the African rice allele S1-g, S1A4, S1TPR (OgTPR1 mentioned in the previous study by Xie et al. 2017), and S1A6 (SSP mentioned in the previous study by Koide et al. 2018), constitute a functional killer that triggers a sterility signal in sporophytic meiotic cells, which selectively eliminates both male and female gametes without the African rice gene S1TPR, thus leading to reduced fertility and segregation distortion in the offspring. A novel and interesting feature is that one of the causal genes, S1TPR,