Dysfunction of duplicated pair rice histone acetyltransferases causes segregation distortion and an interspecific reproductive barrier
Ben Liao, You-Huang Xiang, Yan Li, Kai-Yang Yang, Jun‐Xiang Shan, Wang‐Wei Ye, Nai‐Qian Dong, Yi Kan, Yi‐Bing Yang, Huai‐Yu Zhao, Hong‐Xiao Yu, Zi‐Qi Lu, Yan Zhao, Qiang Zhao, Dongling Guo, Shuang‐Qin Guo, Jie‐Jie Lei, Xiao-Rui Mu, Yingjie Cao, Bin Han, Hong‐Xuan Lin
Abstract
Abstract Postzygotic reproductive isolation, which results in the irreversible divergence of species, is commonly accompanied by hybrid sterility, necrosis/weakness, or lethality in the F 1 or other offspring generations. Here we show that the loss of function of HWS1 and HWS2 , a couple of duplicated paralogs, together confer complete interspecific incompatibility between Asian and African rice. Both of these non-Mendelian determinants encode the putative Esa1-associated factor 6 (EAF6) protein, which functions as a characteristic subunit of the histone H4 acetyltransferase complex regulating transcriptional activation via genome-wide histone modification. The proliferating tapetum and inappropriate polar nuclei arrangement cause defective pollen and seeds in F 2 hybrid offspring due to the recombinant HWS1/2-mediated misregulation of vitamin (biotin and thiamine) metabolism and lipid synthesis. Evolutionary analysis of HWS1/2 suggests that this gene pair has undergone incomplete lineage sorting (ILS) and multiple gene duplication events during speciation. Our findings have not only uncovered a pair of speciation genes that control hybrid breakdown but also illustrate a passive mechanism that could be scaled up and used in the guidance and optimization of hybrid breeding applications for distant hybridization.