Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense
Claudia Castillo-González,
Xiuying Liu,
Changjun Huang,
Changjiang Zhao,
Zeyang Ma,
Tao Hu,
Feng Sun,
Yijun Zhou,
Xueping Zhou,
Xiu-Jie Wang,
Xiuren Zhang
Affiliations
Claudia Castillo-González
Department 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
Xiuying Liu
Department 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, China
Changjun Huang
Department 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, China
Changjiang Zhao
Department 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, China
Zeyang Ma
Department 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
Tao Hu
Department 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
Feng Sun
Department 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, China
Yijun Zhou
Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, China
Xueping Zhou
Biotechnology Institute, College of Agriculture & Biotechnology, Zhejiang University, Zhejiang, China
Xiu-Jie Wang
State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China
Xiuren Zhang
Department 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
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.