Abstract

Gene duplication plays an important role in genetic diversification, adaptive evolution, and speciation. Understanding the mechanisms and effects of postzygotic isolation genes is important for further studies of speciation and crop breeding. The duplicate recessive genes hwe1 and hwe2 cause hybrid breakdown, characterized by poor vegetative growth and reproductive dysgenesis in intersubspecific crosses between Oryza sativa ssp. indica and japonica. Using a map-based cloning strategy, we found that HWE1 and HWE2 encode the Esa1-associated factor 6 (EAF6) protein, a component of histone acetyltransferase complexes. The indica hwe1 and japonica hwe2 alleles lacked functional EAF6, demonstrating that the double recessive homozygote causes hybrid breakdown. Morphological and physiological observations showed that weak plants with double recessive homozygotes had serious morphological defects with a wide range of effects on development and organs, leading to leaves with reduced chlorophyll content, flower and pistil malformation, and anomalies of gametogenesis. These findings suggest that EAF6 plays a pivotal role in the transcriptional regulation of essential genes during the vegetative and reproductive development of rice.

Highlights

  • In eukaryotic cells, histone acetylation regulates the chromatin structure, affecting gene transcription, DNA replication, and DNA damage repair

  • Genetic analysis showed that epistasis between hwe1 and hwe2 caused a hybrid breakdown in other cross combinations (Nipponbare/9311 and Nipponbare/IR8) (Supplementary Figures 1, 2)

  • We demonstrated that hybrid breakdown is caused by HWE1/2 encoding a rice homolog of the NuA4 HAT complex subunit protein Esa1-associated factor 6 (EAF6)

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Summary

Introduction

Histone acetylation regulates the chromatin structure, affecting gene transcription, DNA replication, and DNA damage repair. Nucleosome acetyltransferase of histone 4 (NuA4), a histone acetyltransferase (HAT) complex, is composed of multiple proteins and preferentially acetylates histones H4 and H2A on the nucleosome. Yeast NuA4 consists of 13 subunits, with two independent NuA4 sub-complexes, namely, piccolo-NuA4, composed of Esa, Epl, Yng, and Eaf, and the TINTIN triad of Eaf5/7/3 (Wang X. et al, 2018). Piccolo-NuA4, which is thought to exist alone, contains the catalytic subunit protein essential Sas2-related acetyltransferase-1 (Esa1) (Ohba et al, 1999; Boudreault et al, 2003). Esa alone can acetylate free histones but cannot acetylate nucleosomal histones (Doyon et al, 2004). This protein plays a crucial role in cell cycle progression and DNA double-strand break repair

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