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, Ying-Jie Cao, Bin Han () and Hong-Xuan Lin ()
Additional contact information
Ben Liao: Chinese Academy of Sciences
You-Huang Xiang: Chinese Academy of Sciences
Yan Li: Chinese Academy of Sciences
Kai-Yang Yang: Chinese Academy of Sciences
Jun-Xiang Shan: Chinese Academy of Sciences
Wang-Wei Ye: Chinese Academy of Sciences
Nai-Qian Dong: Chinese Academy of Sciences
Yi Kan: Chinese Academy of Sciences
Yi-Bing Yang: Chinese Academy of Sciences
Huai-Yu Zhao: Chinese Academy of Sciences
Hong-Xiao Yu: Chinese Academy of Sciences
Zi-Qi Lu: Chinese Academy of Sciences
Yan Zhao: Chinese Academy of Sciences
Qiang Zhao: Chinese Academy of Sciences
Dongling Guo: Chinese Academy of Sciences
Shuang-Qin Guo: Chinese Academy of Sciences
Jie-Jie Lei: Chinese Academy of Sciences
Xiao-Rui Mu: Chinese Academy of Sciences
Ying-Jie Cao: Chinese Academy of Sciences
Bin Han: Chinese Academy of Sciences
Hong-Xuan Lin: Chinese Academy of Sciences

Nature Communications, 2024, vol. 15, issue 1, 1-18

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 F1 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 F2 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.

Date: 2024
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DOI: 10.1038/s41467-024-45377-x

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