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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,
  • Hong-Xuan Lin

摘要

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.