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 (siTRD) was detected in a hybrid between Asian cultivated rice and its wild ancestor. Here we examined how siTRD caused by an allelic interaction at a specific locus arose in Asian rice species. The siTRD is controlled by the S6 locus via a mechanism in which the S6 allele acts as a gamete eliminator, and both the male and female gametes possessing the opposite allele ($\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}\) \end{document}$) are aborted only in heterozygotes ($\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}/S_{6}^{\mathrm{a}}\) \end{document}$). Fine mapping revealed that the S6 locus is located near the centromere of chromosome 6. Testcross experiments using near-isogenic lines (NILs) carrying either the S6 or $\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}\) \end{document}$ alleles revealed that Asian rice strains frequently harbor an additional allele ($\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{n}}\) \end{document}$) the presence of which, in heterozygotic states ($\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}/S_{6}^{\mathrm{n}}\) \end{document}$ and $\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}/S_{6}^{\mathrm{n}}\) \end{document}$), does not result in siTRD. A prominent reduction in the nucleotide diversity of S6 or $\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}\) \end{document}$ carriers relative to that of $\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{n}}\) \end{document}$ carriers was detected in the chromosomal region. These results suggest that the two incompatible alleles (S6 and $\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{a}}\) \end{document}$) arose independently from $\batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(S_{6}^{\mathrm{n}}\) \end{document}$ and established genetically discontinuous relationships between limited constituents of the Asian rice population.