Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes

Abstract

Sterility is common in hybrids between divergent populations, such as the indica and japonica subspecies of Asian cultivated rice (Oryza sativa). Although multiple loci for plant hybrid sterility have been identified, it remains unknown how alleles of the loci interact at the molecular level. Here we show that a locus for indicajaponica hybrid male sterility, Sa, comprises two adjacent genes, SaM and SaF, encoding a small ubiquitin-like modifier E3 ligase-like protein and an F-box protein, respectively. Most indica cultivars contain a haplotype SaM ؉ SaF ؉ , whereas all japonica cultivars have SaM ؊ SaF ؊ that diverged by nucleotide variations in wild rice. Male semi-sterility in this heterozygous complex locus is caused by abortion of pollen carrying SaM ؊ . This allele-specific gamete elimination results from a selective interaction of SaF ؉ with SaM ؊ , a truncated protein, but not with SaM ؉ because of the presence of an inhibitory domain, although SaM ؉ is required for this male sterility. Lack of any one of the three alleles in recombinant plants does not produce male sterility. We propose a two-gene/threecomponent interaction model for this hybrid male sterility system. The findings have implications for overcoming male sterility in inter-subspecific hybrid rice breeding.allelic interaction ͉ gamete selection ͉ hybrid sterility ͉ reproductive barrier ͉ two-gene/three-component model

Chromosomal Location of HWA1 and HWA2, Complementary Hybrid Weakness Genes in Rice

“…At the hybrid male sterility locus Sa, heterozygotes of Indica allele Sa i and Japonica allele Sa j exhibited male semisterility. Long et al (2008) In this study, the physical distance between the KGC11M1 and RM27122 markers was found to be 1,637 kb. According to the Rice Genome Annotation Project (Ouyang et al 2007, http://rice.plantbiology.msu.…”

“…Many postzygotic reproductive barrier forms have been reported in rice (Oryza sativa), such as hybrid weakness (e.g., Oka 1957), hybrid pollen sterility (e.g., Long et al 2008), and hybrid sterility causing female gamete abortion (e.g., Chen et al 2008). Among them, hybrid weakness is definable as weak growth occurring in F 1 hybrids derived from crosses between two normal strains.…”

Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

“…Despite this progress, several factors motivate additional genetic studies of postzygotic isolation. Although other species have provided important insights (e.g., Sweigart et al 2006;Bomblies et al 2007;Moyle 2007;Chen et al 2008;Lee et al 2008;Long et al 2008;Kao et al 2010;Martin and Willis 2010), current knowledge of the genetics of postzygotic isolation remains highly biased toward Drosophila. In addition, some of the best-studied species hybridize rarely or not at all in the wild, complicating attempts to connect reproductive barriers examined in the lab with gene flow in nature.…”

Complex genetic nature of sex-independent transmission ratio distortion in Asian rice species: the involvement of unlinked modifiers and sex-specific mechanisms

“…TRD is induced by a variety of mechanisms, such as non-random chromosome segregation during meiosis (Birchler et al, 2003;Fishman and Saunders, 2008), preferential gamete dysfunction in hybrids (Lyttle, 1991;Moyle and Graham, 2006;Long et al, 2008;Chen et al, 2008;Tao et al, 2009a, b;Phadnis and Orr, 2009) and preferential gamete success during fertilization (Price, 1997;. Because TRD can dramatically alter the frequency of alleles in a population by disrupting proper Mendelian segregation, it has been hypothesized that TRD is a driving force in the emergence of a reproductive barrier (Frank, 1991;Hurst and Pomiankowski, 1991).…”

“…Among them, TRD occurring in either the male (mTRD) or female (fTRD) gametes has been frequently reported and some of the genes causing sex-specific TRD have been cloned Long et al, 2008). On the other hand, there are few reports on sex-independent TRD (siTRD), which results from preferential transmission of both male and female gametes carrying one of the two alleles in the heterozygote (Rick, 1966;Koide et al, 2008c).…”