The Evolution of Sex-Independent Transmission Ratio Distortion Involving Multiple Allelic Interactions at a Single Locus in Rice

Abstract

Transmission ratio distortion (TRD) is frequently observed in inter-and intraspecific hybrids of plants, leading to a violation of Mendelian inheritance. Sex-independent TRD (si TRD) was detected in a hybrid between Asian cultivated rice and its wild ancestor. Here we examined how si TRD caused by an allelic interaction at a specific locus arose in Asian rice species. The si TRD is controlled by the S 6 locus via a mechanism in which the S 6 allele acts as a gamete eliminator, and both the male and female gametes possessing the opposite allele (S 6 a ) are aborted only in heterozygotes (S 6 /S 6 a ). Fine mapping revealed that the S 6 locus is located near the centromere of chromosome 6. Testcross experiments using near-isogenic lines (NILs) carrying either the S 6 or S 6 a alleles revealed that Asian rice strains frequently harbor an additional allele (S 6 n ) the presence of which, in heterozygotic states (S 6 /S 6 n and S 6 a /S 6 n ), does not result in si TRD. A prominent reduction in the nucleotide diversity of S 6 or S 6 a carriers relative to that of S 6 n carriers was detected in the chromosomal region. These results suggest that the two incompatible alleles (S 6 and S 6 a ) arose independently from S 6 n and established genetically discontinuous relationships between limited constituents of the Asian rice population.

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

“…In contrast, no defect was observed in the pollen grains of the heterozygotes, although male gametes possessing the S 6 a allele were rarely transmitted to the next generation (Sano, 1992;Koide et al, 2008a). We have also revealed that Asian rice strains frequently harbor an additional allele (S 6 n ), which however, does not induce any preferential abortion in heterozygotes (S 6 /S 6 n and S 6 a /S 6 n ) at the S 6 locus (Koide et al, 2008a), as shown by test-cross experiments and subsequent genetic mapping using NILs that carry the genetic background of T65wx. The presence of the S 6 n allele, which modifies the effect of the S 6 allele in heterozygotic state at the S 6 locus, suggested that S 6 locus-mediated siTRD was caused by the allelic differentiation at the S 6 locus occurred during the evolution of Asian rice.…”

“…NIL-S 6 carries the short arm and a portion of the long arm of chromosome 6 from Ruf-S 6 in the genetic background of T65wx (Sano, 1992;Matsubara et al, 2003;Koide et al, 2008a formally named as T65S 6 [W593]). T65wx harbors the S 6 a allele at the S 6 locus (near the centromeric region of chromosome 6), whereas Ruf-S 6 and NIL-S 6 harbor the S 6 allele at the S 6 locus (Koide et al, 2008a). Although T65wx harbors wx gene from Kinoshita-mochi (Oka, 1974; derived from BC 12 ), wx gene does not affect S 6 locus-mediated TRD.…”

“…We previously reported S 6 locus-mediated siTRD in a hybrid of Asian cultivated rice (Oryza sativa) and wild rice (Oryza rufipogon; Sano, 1992;Koide et al, 2008a). Asian cultivated rice and wild rice belong to the same biological species, forming a primary gene pool (O. sativa-O.…”

“…The S 6 allele acted as a 'gamete eliminator,' and was transmitted more frequently than S 6 a through both the male and female gametes in heterozygotes (S 6 /S 6 a ). Female gametes possessing the S 6 a allele were aborted in the heterozygotes, causing a reduced seed-setting rate (Sano, 1992;Koide et al, 2008a). In contrast, no defect was observed in the pollen grains of the heterozygotes, although male gametes possessing the S 6 a allele were rarely transmitted to the next generation (Sano, 1992;Koide et al, 2008a).…”

“…Female gametes possessing the S 6 a allele were aborted in the heterozygotes, causing a reduced seed-setting rate (Sano, 1992;Koide et al, 2008a). In contrast, no defect was observed in the pollen grains of the heterozygotes, although male gametes possessing the S 6 a allele were rarely transmitted to the next generation (Sano, 1992;Koide et al, 2008a). We have also revealed that Asian rice strains frequently harbor an additional allele (S 6 n ), which however, does not induce any preferential abortion in heterozygotes (S 6 /S 6 n and S 6 a /S 6 n ) at the S 6 locus (Koide et al, 2008a), as shown by test-cross experiments and subsequent genetic mapping using NILs that carry the genetic background of T65wx.…”