Two complementary genes in a presence-absence variation contribute to indica-japonica reproductive isolation in rice

Daiqi Wang; Hongru Wang; Xiaomei Xu; Man Wang; Yahuan Wang; Hong Chen; Fei Ping; Huanhuan Zhong; Zhengkun Mu; Wantong Xie; Xiangyu Li; Jingbin Feng; Milan Zhang; Zhilan Fan; Tifeng Yang; Junliang Zhao; Bin Liu; Ying Ruan; Guiquan Zhang; Chunlin Liu; Ziqiang Liu

doi:10.1038/s41467-023-40189-x

Two complementary genes in a presence-absence variation contribute to indica-japonica reproductive isolation in rice

Nat Commun. 2023 Jul 28;14(1):4531. doi: 10.1038/s41467-023-40189-x.

Authors

Daiqi Wang^{1

2

3

4}, Hongru Wang⁵, Xiaomei Xu¹, Man Wang^{1

2}, Yahuan Wang¹, Hong Chen¹, Fei Ping^{1

2}, Huanhuan Zhong¹, Zhengkun Mu^{1

2}, Wantong Xie^{1

2}, Xiangyu Li^{1

2}, Jingbin Feng^{1

2}, Milan Zhang^{1

2}, Zhilan Fan⁶, Tifeng Yang⁷, Junliang Zhao⁷, Bin Liu⁷, Ying Ruan^{3

8}, Guiquan Zhang^{1

2}, Chunlin Liu^{3

4}, Ziqiang Liu^{9

10}

Affiliations

¹ Guangdong Provincial Key Laboratory of Plant Molecular Breeding, College of Agriculture, South China Agricultural University, Guangzhou, Guangdong, 510642, China.
² State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, Guangdong, 510642, China.
³ Key Laboratory of Hunan Provincial on Crop Epigenetic Regulation and Development, Hunan Agricultural University, Changsha, Hunan, 410128, China.
⁴ College of Agronomy, Hunan Agricultural University, Changsha, Hunan, 410128, China.
⁵ Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomic Insitute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, Guangdong, 518120, China.
⁶ National Field Genebank for Wild Rice (Guangzhou), Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, Guangdong, 510640, China.
⁷ Guangdong Provincial Key Laboratory of New Technology in Rice Breeding, Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, Guangdong, 510640, China.
⁸ College of Bioscience and Biotechnology, Hunan Agricultural University, Changsha, Hunan, 410128, China.
⁹ Guangdong Provincial Key Laboratory of Plant Molecular Breeding, College of Agriculture, South China Agricultural University, Guangzhou, Guangdong, 510642, China. zqliu@scau.edu.cn.
¹⁰ State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, Guangdong, 510642, China. zqliu@scau.edu.cn.

Abstract

Understanding the evolutionary forces in speciation is a central goal in evolutionary biology. Asian cultivated rice has two subspecies, indica and japonica, but the underlying mechanism of the partial reproductive isolation between them remains obscure. Here we show a presence-absence variation (PAV) at the Se locus functions as an indica-japonica reproductive barrier by causing hybrid sterility (HS) in indica-japonica crosses. The locus comprises two adjacent genes: ORF3 encodes a sporophytic pollen killer, whereas ORF4 protects pollen in a gametophytic manner. In F₁ of indica-japonica crosses, pollen with the japonica haplotype, which lacks the sequence containing the protective ORF4, is aborted due to the pollen-killing effect of ORF3 from indica. Evolutionary analysis suggests ORF3 is a gene associated with the Asian cultivated rice species complex, and the PAV has contributed to the reproductive isolation between the two subspecies of Asian cultivated rice. Our analyses provide perspectives on rice inter-subspecies post-zygotic isolation, and will promote efforts to overcome reproductive barriers in indica-japonica hybrid rice breeding.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Alleles
Oryza* / genetics
Plant Breeding
Pollen / genetics
Reproductive Isolation