Genomic structural variation-mediated allelic suppression causes hybrid male sterility in rice

Rongxin Shen,Xianrong Xie,Lan Wang,Xupeng Liu,Qinlong Zhu,Huiwu Tang,Qing Li,Xiucai Zhao,Jiang Wu,Letian Chen,Yao-Guang Liu,Weiwei Jin

doi:10.1038/s41467-017-01400-y

Abstract

Hybrids between divergent populations commonly show hybrid sterility; this reproductive barrier hinders hybrid breeding of the japonica and indica rice (Oryza sativa L.) subspecies. Here we show that structural changes and copy number variation at the Sc locus confer japonica–indica hybrid male sterility. The japonica allele, Sc-j, contains a pollen-essential gene encoding a DUF1618-domain protein; the indica allele, Sc-i, contains two or three tandem-duplicated ~ 28-kb segments, each carrying an Sc-j-homolog with a distinct promoter. In Sc-j/Sc-i hybrids, the high-expression of Sc-i in sporophytic cells causes suppression of Sc-j expression in pollen and selective abortion of Sc-j-pollen, leading to transmission ratio distortion. Knocking out one or two of the three Sc-i copies by CRISPR/Cas9 rescues Sc-j expression and male fertility. Our results reveal the gene dosage-dependent allelic suppression as a mechanism of hybrid incompatibility, and provide an effective approach to overcome the reproductive barrier for hybrid breeding.

Highlights

Hybrids between divergent populations commonly show hybrid sterility; this reproductive barrier hinders hybrid breeding of the japonica and indica rice (Oryza sativa L.) subspecies
The coding regions of Sc-j and these paralogous Sc-i genes include nineteen single-nucleotide polymorphisms (SNPs) and three 3-bp insertion/deletions, which result in several aa substitutions, but the coding sequences of Sc-ib[1] and Sc-ib[2] are identical (Supplementary Figs. 3 and 4)
We found that five cultivars (MH63, 93-11, HHZ, Dular, and 02428) contain two duplicates of the segment, whereas three other cultivars (E5, ZS97B, and GLA4) contain three such duplicates (Fig. 1d and Supplementary Fig. 6), consistent with the sequencing results of E5, MH63, and 93-11. These results indicate that the genomic structural change and the segment copy number variation (CNV) at Sc is a common feature in indica cultivars

Summary

Introduction

Hybrids between divergent populations commonly show hybrid sterility; this reproductive barrier hinders hybrid breeding of the japonica and indica rice (Oryza sativa L.) subspecies. Hybrid sterility (HS, including male and female sterilities) reflects the genetic incompatibility between evolutionarily divergent populations in the same or different species. This major form of postzygotic reproductive isolation restricts gene flow and maintains the separation of species (subspecies) during speciation[1,2,3]. Current hybrid rice varieties were bred mainly from crosses between lines from the same subspecies, mostly indica lines, and hybrid yields have reached a plateau due to the narrow genetic diversity of the parental lines, which results in lower degrees of hybrid vigor (heterosis). The hybrids between japonica and indica cultivars have much stronger heterosis, holding great promise for further increasing yield potential[12]

Methods

Results

Conclusion