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A JUMONJI Protein with E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis.
Plant Physiol. 2016 05; 171(1):344-58.PP

Abstract

Transposable elements (TEs) make up a large proportion of eukaryotic genomes. As their mobilization creates genetic variation that threatens genome integrity, TEs are epigenetically silenced through several pathways, and this may spread to neighboring sequences. JUMONJI (JMJ) proteins can function as antisilencing factors and prevent silencing of genes next to TEs Whether TE silencing is counterbalanced by the activity of antisilencing factors is still unclear. Here, we characterize JMJ24 as a regulator of TE silencing. We show that loss of JMJ24 results in increased silencing of the DNA transposon AtMu1c, while overexpression of JMJ24 reduces silencing. JMJ24 has a JumonjiC (JmjC) domain and two RING domains. JMJ24 autoubiquitinates in vitro, demonstrating E3 ligase activity of the RING domain(s). JMJ24-JmjC binds the N-terminal tail of histone H3, and full-length JMJ24 binds histone H3 in vivo. JMJ24 activity is anticorrelated with histone H3 Lys 9 dimethylation (H3K9me2) levels at AtMu1c Double mutant analyses with epigenetic silencing mutants suggest that JMJ24 antagonizes histone H3K9me2 and requires H3K9 methyltransferases for its activity on AtMu1c Genome-wide transcriptome analysis indicates that JMJ24 affects silencing at additional TEs Our results suggest that the JmjC domain of JMJ24 has lost demethylase activity but has been retained as a binding domain for histone H3. This is in line with phylogenetic analyses indicating that JMJ24 (with the mutated JmjC domain) is widely conserved in angiosperms. Taken together, this study assigns a role in TE silencing to a conserved JmjC-domain protein with E3 ligase activity, but no demethylase activity.

Authors+Show Affiliations

Institute for Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (T.K., K.B., T.F., C.K., I.B.); andMax-Planck-Institute for Molecular Plant Physiology, 14476 Potsdam, Germany (M.G., A.G.).Institute for Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (T.K., K.B., T.F., C.K., I.B.); andMax-Planck-Institute for Molecular Plant Physiology, 14476 Potsdam, Germany (M.G., A.G.).Institute for Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (T.K., K.B., T.F., C.K., I.B.); andMax-Planck-Institute for Molecular Plant Physiology, 14476 Potsdam, Germany (M.G., A.G.).Institute for Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (T.K., K.B., T.F., C.K., I.B.); andMax-Planck-Institute for Molecular Plant Physiology, 14476 Potsdam, Germany (M.G., A.G.).Institute for Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (T.K., K.B., T.F., C.K., I.B.); andMax-Planck-Institute for Molecular Plant Physiology, 14476 Potsdam, Germany (M.G., A.G.).Institute for Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (T.K., K.B., T.F., C.K., I.B.); andMax-Planck-Institute for Molecular Plant Physiology, 14476 Potsdam, Germany (M.G., A.G.).Institute for Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany (T.K., K.B., T.F., C.K., I.B.); andMax-Planck-Institute for Molecular Plant Physiology, 14476 Potsdam, Germany (M.G., A.G.) isabel.baeurle@uni-potsdam.de.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

26979329

Citation

Kabelitz, Tina, et al. "A JUMONJI Protein With E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis." Plant Physiology, vol. 171, no. 1, 2016, pp. 344-58.
Kabelitz T, Brzezinka K, Friedrich T, et al. A JUMONJI Protein with E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis. Plant Physiol. 2016;171(1):344-58.
Kabelitz, T., Brzezinka, K., Friedrich, T., Górka, M., Graf, A., Kappel, C., & Bäurle, I. (2016). A JUMONJI Protein with E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis. Plant Physiology, 171(1), 344-58. https://doi.org/10.1104/pp.15.01688
Kabelitz T, et al. A JUMONJI Protein With E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis. Plant Physiol. 2016;171(1):344-58. PubMed PMID: 26979329.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - A JUMONJI Protein with E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis. AU - Kabelitz,Tina, AU - Brzezinka,Krzysztof, AU - Friedrich,Thomas, AU - Górka,Michał, AU - Graf,Alexander, AU - Kappel,Christian, AU - Bäurle,Isabel, Y1 - 2016/03/15/ PY - 2015/11/02/received PY - 2016/03/14/accepted PY - 2016/3/17/entrez PY - 2016/3/17/pubmed PY - 2018/2/24/medline SP - 344 EP - 58 JF - Plant physiology JO - Plant Physiol. VL - 171 IS - 1 N2 - Transposable elements (TEs) make up a large proportion of eukaryotic genomes. As their mobilization creates genetic variation that threatens genome integrity, TEs are epigenetically silenced through several pathways, and this may spread to neighboring sequences. JUMONJI (JMJ) proteins can function as antisilencing factors and prevent silencing of genes next to TEs Whether TE silencing is counterbalanced by the activity of antisilencing factors is still unclear. Here, we characterize JMJ24 as a regulator of TE silencing. We show that loss of JMJ24 results in increased silencing of the DNA transposon AtMu1c, while overexpression of JMJ24 reduces silencing. JMJ24 has a JumonjiC (JmjC) domain and two RING domains. JMJ24 autoubiquitinates in vitro, demonstrating E3 ligase activity of the RING domain(s). JMJ24-JmjC binds the N-terminal tail of histone H3, and full-length JMJ24 binds histone H3 in vivo. JMJ24 activity is anticorrelated with histone H3 Lys 9 dimethylation (H3K9me2) levels at AtMu1c Double mutant analyses with epigenetic silencing mutants suggest that JMJ24 antagonizes histone H3K9me2 and requires H3K9 methyltransferases for its activity on AtMu1c Genome-wide transcriptome analysis indicates that JMJ24 affects silencing at additional TEs Our results suggest that the JmjC domain of JMJ24 has lost demethylase activity but has been retained as a binding domain for histone H3. This is in line with phylogenetic analyses indicating that JMJ24 (with the mutated JmjC domain) is widely conserved in angiosperms. Taken together, this study assigns a role in TE silencing to a conserved JmjC-domain protein with E3 ligase activity, but no demethylase activity. SN - 1532-2548 UR - https://www.unboundmedicine.com/medline/citation/26979329/A_JUMONJI_Protein_with_E3_Ligase_and_Histone_H3_Binding_Activities_Affects_Transposon_Silencing_in_Arabidopsis_ L2 - http://www.plantphysiol.org/cgi/pmidlookup?view=long&pmid=26979329 DB - PRIME DP - Unbound Medicine ER -