Duplication and Loss of Function of Genes Encoding RNA Polymerase III Subunit C4 Causes Hybrid Incompatibility in Rice

Abstract

Reproductive barriers are commonly observed in both animals and plants, in which they maintain species integrity and contribute to speciation. This report shows that a combination of loss-of-function alleles at two duplicated loci, <i>DUPLICATED GAMETOPHYTIC STERILITY 1</i> (<i>DGS1</i>) on chromosome 4 and <i>DGS2</i> on chromosome 7, causes pollen sterility in hybrid progeny derived from an interspecific cross between cultivated rice, <i>Oryza sativa</i>, and an Asian annual wild rice, <i>O. nivara</i> Male gametes carrying the <i>DGS1</i> allele from <i>O. nivara</i> (<i>DGS1-nivara^s</i> ) and the <i>DGS2</i> allele from <i>O. sativa</i> (<i>DGS2-T65^s</i> ) were sterile, but female gametes carrying the same genotype were fertile. We isolated the causal gene, which encodes a protein homologous to DNA-dependent RNA polymerase (RNAP) III subunit C4 (RPC4). RPC4 facilitates the transcription of 5S rRNAs and tRNAs. The loss-of-function alleles at <i>DGS1-nivara^s</i> and <i>DGS2-T65^s</i> were caused by weak or nonexpression of <i>RPC4</i> and an absence of <i>RPC4</i>, respectively. Phylogenetic analysis demonstrated that gene duplication of <i>RPC4</i> at <i>DGS1</i> and <i>DGS2</i> was a recent event that occurred after divergence of the ancestral population of <i>Oryza</i> from other Poaceae or during diversification of AA-genome species.