Histone H3K27 dimethylation landscapes contribute to genome stability and genetic recombination during wheat polyploidization

• Published in: The Plant journal : for cell and molecular biology Vol. 105; no. 3; pp. 678 - 690
• Main Authors: Liu, Yanfeng, Yuan, Jingya, Jia, Guanghong, Ye, Wenxue, Jeffrey Chen, Z., Song, Qingxin
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.02.2021
• Subjects: Biological evolution; Deoxyribonucleic acid; Diploids; DNA; DNA damage; Euchromatin; Evolution; Genomes; H3K27me2; Histone H3; Histones; Lysine; Plant breeding; Ploidy; Polyploidy; Recombination; Stability; Transposons; Triticum aestivum; valley; Wheat; Zea mays; valley; wheat; evolution; polyploidy; H3K27me2
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15063

SUMMARY Bread wheat (Triticum aestivum) is an allohexaploid that was formed via two allopolyploidization events. Growing evidence suggests histone modifications are involved in the response to ‘genomic shock’ and environmental adaptation during polyploid formation and evolution. However, the role of histone modifications, especially histone H3 lysine‐27 dimethylation (H3K27me2), in genome evolution remains elusive. Here we analyzed H3K27me2 and H3K27me3 profiles in hexaploid wheat and its tetraploid and diploid relatives. Although H3K27me3 levels were relatively stable among wheat species with different ploidy levels, H3K27me2 intensities increased concurrent with increased ploidy levels, and H3K27me2 peaks were colocalized with massively amplified DTC transposons (CACTA family) in euchromatin, which may silence euchromatic transposons to maintain genome stability during polyploid wheat evolution. Consistently, the distribution of H3K27me2 is mutually exclusive with another repressive histone mark, H3K9me2, that mainly silences transposons in heterochromatic regions. Remarkably, the regions with low H3K27me2 levels (named H3K27me2 valleys) were associated with the formation of DNA double‐strand breaks in genomes of wheat, maize (Zea mays) and Arabidopsis. Our results provide a comprehensive view of H3K27me2 and H3K27me3 distributions during wheat evolution, which support roles for H3K27me2 in silencing euchromatic transposons to maintain genome stability and in modifying genetic recombination landscapes. These genomic insights may empower breeding improvement of crops. Significance Statement Polyploidy is widespread in plants and is a key driver of continuing evolution and speciation. This work studies the roles of H3K27me2 and H3K27me3 in silencing amplified transposons and modifying genetic recombination landscapes during the formation and evolution of hexaploid wheat.