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H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome

Zhen Wang, Claudia M. Castillo-González, Changjiang Zhao, Chun-Yip Tong, Changhao Li, Songxiao Zhong, Zhiyang Liu, Kaili Xie, Jiaying Zhu, Zhongshou Wu, Xu Peng, Yannick Jacob, Scott D. Michaels, Steven E. Jacobsen and Xiuren Zhang ()
Additional contact information
Zhen Wang: Texas A&M University
Claudia M. Castillo-González: Texas A&M University
Changjiang Zhao: Texas A&M University
Chun-Yip Tong: Texas A&M University
Changhao Li: Texas A&M University
Songxiao Zhong: Texas A&M University
Zhiyang Liu: Texas A&M University
Kaili Xie: Texas A&M University
Jiaying Zhu: Texas A&M University
Zhongshou Wu: University of California, Los Angeles
Xu Peng: Texas A&M University
Yannick Jacob: Yale University
Scott D. Michaels: Indiana University
Steven E. Jacobsen: University of California, Los Angeles
Xiuren Zhang: Texas A&M University

Nature Communications, 2023, vol. 14, issue 1, 1-20

Abstract: Abstract The H3 methyltransferases ATXR5 and ATXR6 deposit H3.1K27me1 to heterochromatin to prevent genomic instability and transposon re-activation. Here, we report that atxr5 atxr6 mutants display robust resistance to Geminivirus. The viral resistance is correlated with activation of DNA repair pathways, but not with transposon re-activation or heterochromatin amplification. We identify RAD51 and RPA1A as partners of virus-encoded Rep protein. The two DNA repair proteins show increased binding to heterochromatic regions and defense-related genes in atxr5 atxr6 vs wild-type plants. Consequently, the proteins have reduced binding to viral DNA in the mutant, thus hampering viral amplification. Additionally, RAD51 recruitment to the host genome arise via BRCA1, HOP2, and CYCB1;1, and this recruitment is essential for viral resistance in atxr5 atxr6. Thus, Geminiviruses adapt to healthy plants by hijacking DNA repair pathways, whereas the unstable genome, triggered by reduced H3.1K27me1, could retain DNA repairing proteins to suppress viral amplification in atxr5 atxr6.

Date: 2023
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DOI: 10.1038/s41467-023-43311-1

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