H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome
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 pa...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-11-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-43311-1 |
| _version_ | 1797558389373403136 |
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| author | 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 Xiuren Zhang |
| author_facet | 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 Xiuren Zhang |
| author_sort | Zhen Wang |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-10T17:29:48Z |
| format | Article |
| id | doaj.art-8592bad5b0d24d13a6cc15d3c8d43320 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:29:48Z |
| publishDate | 2023-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-8592bad5b0d24d13a6cc15d3c8d433202023-11-20T10:03:31ZengNature PortfolioNature Communications2041-17232023-11-0114112010.1038/s41467-023-43311-1H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genomeZhen Wang0Claudia M. Castillo-González1Changjiang Zhao2Chun-Yip Tong3Changhao Li4Songxiao Zhong5Zhiyang Liu6Kaili Xie7Jiaying Zhu8Zhongshou Wu9Xu Peng10Yannick Jacob11Scott D. Michaels12Steven E. Jacobsen13Xiuren Zhang14Department of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Biochemistry and Biophysics, Texas A&M UniversityDepartment of Molecular, Cell, and Developmental Biology, University of California, Los AngelesDepartment of Molecular Physiology, College of Medicine, Texas A&M UniversityDepartment of Molecular, Cellular & Developmental Biology, Yale UniversityDepartment of Biology, Indiana UniversityDepartment of Molecular, Cell, and Developmental Biology, University of California, Los AngelesDepartment of Biochemistry and Biophysics, Texas A&M UniversityAbstract 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.https://doi.org/10.1038/s41467-023-43311-1 |
| spellingShingle | 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 Xiuren Zhang H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome Nature Communications |
| title | H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome |
| title_full | H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome |
| title_fullStr | H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome |
| title_full_unstemmed | H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome |
| title_short | H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome |
| title_sort | h3 1k27me1 loss confers arabidopsis resistance to geminivirus by sequestering dna repair proteins onto host genome |
| url | https://doi.org/10.1038/s41467-023-43311-1 |
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