Abstract

Postzygotic reproductive isolation maintains species integrity and uniformity and contributes to speciation by restricting the free gene flow between divergent species. In this study we identify causal genes of two Mendelian factors S22A and S22B on rice chromosome 2 inducing F1 pollen sterility in hybrids between Oryza sativa japonica-type cultivar Taichung 65 (T65) and a wild relative of rice species Oryza glumaepatula. The causal gene of S22B in T65 encodes a protein containing DUF1668 and gametophytically expressed in the anthers, designated S22B_j. The O. glumaepatula allele S22B-g, allelic to S22B_j, possesses three non-synonymous substitutions and a 2-bp deletion, leading to a frameshifted translation at the S22B C-terminal region. Transcription level of S22B-j and/or S22B_g did not solely determine the fertility of pollen grains by genotypes at S22B. Western blotting of S22B found that one major band with approximately 46 kDa appeared only at the mature stage and was reduced on semi-sterile heterozygotes at S22B, implying that the 46 kDa band may associated in hybrid sterility. In addition, causal genes of S22A in T65 were found to be S22A_j1 and S22A_j3 encoding DUF1668-containing protein. The allele of a wild rice species Oryza meridionalis Ng at S22B, designated S22B_m, is a loss-of-function allele probably due to large deletion of the gene lacking DUF1668 domain and evolved from the different lineage of O. glumaepatula. Phylogenetic analysis of DUF1668 suggested that many gene duplications occurred before the divergence of current crops in Poaceae, and loss-of-function mutations of DUF1668-containing genes represent the candidate causal genetic events contributing to hybrid incompatibilities. The duplicated DUF1668-domain gene may provide genetic potential to induce hybrid incompatibility by consequent mutations after divergence.

Highlights

  • Hybrid incompatibilities (HIs), with respect to both intra‐ and interspecific hybridizations, are a widespread mechanism of postzygotic reproductive isolation, which restricts free gene flow between divergent species (Coyne and Orr, 2004)

  • We revealed that the genes S22B_j, S22A_j1, and S22A_j3 encoding DUF1668-containing protein are causal genes of F1 pollen sterility controlled by S22A or S22B in hybrids derived from a cross between O. sativa cultivar Taichung 65 (T65) and O. glumaepatula accession IRGC105668

  • Our previous genetic analysis demonstrated that S22A and S22B independently induced pollen semi-sterility on heterozygotes, and that pollen grains carrying the sterility allele S22A-glums and S22B-glums in S22A_SS and S22B_SS plants are, respectively, sterile (Sakata et al, 2014)

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Summary

Introduction

Hybrid incompatibilities (HIs), with respect to both intra‐ and interspecific hybridizations, are a widespread mechanism of postzygotic reproductive isolation, which restricts free gene flow between divergent species (Coyne and Orr, 2004). With respect to genic incompatibility, incompatible combinations of genes, each of which is generally an ancestral and variant allele derived from two reproductively isolated species, combine in the sporophytes or gametophytes of hybrids, resulting in maladaptive phenotypes, leading to inviability, sterility, and/or hybrid breakdown. These incompatible zygotes or gametes with reduced fitness are subsequently eliminated in hybrid populations. It is currently central question of evolutionary genetics of HI that how alleles causing HI can evolve and be maintained in a population without falling into fitness valleys

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