Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense

Transcriptional gene silencing (TGS) can serve as an innate immunity against invading DNA viruses throughout Eukaryotes. Geminivirus code for TrAP protein to suppress the TGS pathway. Here, we identified an Arabidopsis H3K9me2 histone methyltransferase, Su(var)3-9 homolog 4/Kryptonite (SUVH4/KYP), a...

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Main Authors: Claudia Castillo-González, Xiuying Liu, Changjun Huang, Changjiang Zhao, Zeyang Ma, Tao Hu, Feng Sun, Yijun Zhou, Xueping Zhou, Xiu-Jie Wang, Xiuren Zhang
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/06671
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author Claudia Castillo-González
Xiuying Liu
Changjun Huang
Changjiang Zhao
Zeyang Ma
Tao Hu
Feng Sun
Yijun Zhou
Xueping Zhou
Xiu-Jie Wang
Xiuren Zhang
author_facet Claudia Castillo-González
Xiuying Liu
Changjun Huang
Changjiang Zhao
Zeyang Ma
Tao Hu
Feng Sun
Yijun Zhou
Xueping Zhou
Xiu-Jie Wang
Xiuren Zhang
author_sort Claudia Castillo-González
collection DOAJ
description Transcriptional gene silencing (TGS) can serve as an innate immunity against invading DNA viruses throughout Eukaryotes. Geminivirus code for TrAP protein to suppress the TGS pathway. Here, we identified an Arabidopsis H3K9me2 histone methyltransferase, Su(var)3-9 homolog 4/Kryptonite (SUVH4/KYP), as a bona fide cellular target of TrAP. TrAP interacts with the catalytic domain of KYP and inhibits its activity in vitro. TrAP elicits developmental anomalies phenocopying several TGS mutants, reduces the repressive H3K9me2 mark and CHH DNA methylation, and reactivates numerous endogenous KYP-repressed loci in vivo. Moreover, KYP binds to the viral chromatin and controls its methylation to combat virus infection. Notably, kyp mutants support systemic infection of TrAP-deficient Geminivirus. We conclude that TrAP attenuates the TGS of the viral chromatin by inhibiting KYP activity to evade host surveillance. These findings provide new insight on the molecular arms race between host antiviral defense and virus counter defense at an epigenetic level.
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spelling doaj.art-132126e619c14663ba16845e6316c0352022-12-22T04:32:17ZengeLife Sciences Publications LtdeLife2050-084X2015-09-01410.7554/eLife.06671Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defenseClaudia Castillo-González0Xiuying Liu1Changjun Huang2Changjiang Zhao3Zeyang Ma4Tao Hu5Feng Sun6Yijun Zhou7Xueping Zhou8Xiu-Jie Wang9Xiuren Zhang10Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States; Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, United StatesDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, United States; Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, United States; State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, United States; Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, United States; State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou, China; Yunnan Academy of Tobacco Agricultural Sciences, Yunnan, ChinaDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, United States; Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, United States; College of Agronomy, Heilongjiang Bayi Agricultural University, Daqing, ChinaDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, United States; Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, United StatesDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, United States; Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, United States; State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University, Hangzhou, ChinaDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, United States; Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, United States; Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaInstitute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaBiotechnology Institute, College of Agriculture & Biotechnology, Zhejiang University, Zhejiang, ChinaState Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, ChinaDepartment of Biochemistry and Biophysics, Texas A&M University, College Station, United States; Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, United StatesTranscriptional gene silencing (TGS) can serve as an innate immunity against invading DNA viruses throughout Eukaryotes. Geminivirus code for TrAP protein to suppress the TGS pathway. Here, we identified an Arabidopsis H3K9me2 histone methyltransferase, Su(var)3-9 homolog 4/Kryptonite (SUVH4/KYP), as a bona fide cellular target of TrAP. TrAP interacts with the catalytic domain of KYP and inhibits its activity in vitro. TrAP elicits developmental anomalies phenocopying several TGS mutants, reduces the repressive H3K9me2 mark and CHH DNA methylation, and reactivates numerous endogenous KYP-repressed loci in vivo. Moreover, KYP binds to the viral chromatin and controls its methylation to combat virus infection. Notably, kyp mutants support systemic infection of TrAP-deficient Geminivirus. We conclude that TrAP attenuates the TGS of the viral chromatin by inhibiting KYP activity to evade host surveillance. These findings provide new insight on the molecular arms race between host antiviral defense and virus counter defense at an epigenetic level.https://elifesciences.org/articles/06671epigenetic silencingviral suppressiongeminivirushistone methyltransferaseTrAP/AL2/AC2host–virus interaction
spellingShingle Claudia Castillo-González
Xiuying Liu
Changjun Huang
Changjiang Zhao
Zeyang Ma
Tao Hu
Feng Sun
Yijun Zhou
Xueping Zhou
Xiu-Jie Wang
Xiuren Zhang
Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense
eLife
epigenetic silencing
viral suppression
geminivirus
histone methyltransferase
TrAP/AL2/AC2
host–virus interaction
title Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense
title_full Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense
title_fullStr Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense
title_full_unstemmed Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense
title_short Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense
title_sort geminivirus encoded trap suppressor inhibits the histone methyltransferase suvh4 kyp to counter host defense
topic epigenetic silencing
viral suppression
geminivirus
histone methyltransferase
TrAP/AL2/AC2
host–virus interaction
url https://elifesciences.org/articles/06671
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