The CCR4-NOT complex component NOT1 regulates RNA-directed DNA methylation and transcriptional silencing by facilitating Pol IV-dependent siRNA production.
CCR4
DNA methylation
NOT1
RNA
pol IV
transcriptional silencing
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
03
03
2020
revised:
29
04
2020
accepted:
07
05
2020
pubmed:
16
5
2020
medline:
20
3
2021
entrez:
16
5
2020
Statut:
ppublish
Résumé
Small interfering RNAs (siRNAs) are responsible for establishing and maintaining DNA methylation through the RNA-directed DNA methylation (RdDM) pathway in plants. Although siRNA biogenesis is well known, it is relatively unclear about how the process is regulated. By a forward genetic screen in Arabidopsis thaliana, we identified a mutant defective in NOT1 and demonstrated that NOT1 is required for transcriptional silencing at RdDM target genomic loci. We demonstrated that NOT1 is required for Pol IV-dependent siRNA accumulation and DNA methylation at a subset of RdDM target genomic loci. Furthermore, we revealed that NOT1 is a constituent of a multi-subunit CCR4-NOT deadenylase complex by immunoprecipitation combined with mass spectrometry and demonstrated that the CCR4-NOT components can function as a whole to mediate chromatin silencing. Therefore, our work establishes that the CCR4-NOT complex regulates the biogenesis of Pol IV-dependent siRNAs, and hence facilitates DNA methylation and transcriptional silencing in Arabidopsis.
Substances chimiques
AT1G02080 protein, Arabidopsis
0
Arabidopsis Proteins
0
RNA, Small Interfering
0
Repressor Proteins
0
Transcription Factors
0
RNA polymerase IV, Arabidopsis
EC 2.7.7.-
DNA-Directed RNA Polymerases
EC 2.7.7.6
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1503-1515Informations de copyright
© 2020 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Arae, T., Morita, K., Imahori, R., Suzuki, Y., Yasuda, S., Sato, T., Yamaguchi, J. and Chiba, Y. (2019) Identification of Arabidopsis CCR4-NOT complexes with pumilio RNA-binding proteins, APUM5 and APUM2. Plant Cell Physiol. 60, 2015-2025.
Ausin, I., Greenberg, M.V., Li, C.F. and Jacobsen, S.E. (2012) The splicing factor SR45 affects the RNA-directed DNA methylation pathway in Arabidopsis. Epigenetics. 7, 29-33.
Bayne, E.H., Portoso, M., Kagansky, A., Kos-Braun, I.C., Urano, T., Ekwall, K., Alves, F., Rappsilber, J. and Allshire, R.C. (2008) Splicing factors facilitate RNAi-directed silencing in fission yeast. Science. 322, 602-606.
Blevins, T., Podicheti, R., Mishra, V., Marasco, M., Tang, H. and Pikaard, C.S. (2015) Identification of Pol IV and RDR2-dependent precursors of 24 nt siRNAs guiding de novo DNA methylation in Arabidopsis. eLife. 4, e09591.
Blevins, T., Pontvianne, F., Cocklin, R. et al. (2014) A two-step process for epigenetic inheritance in Arabidopsis. Mol. Cell. 54, 30-42.
Bohmdorfer, G., Rowley, M.J., Kucinski, J., Zhu, Y., Amies, I. and Wierzbicki, A.T. (2014) RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA. Plant J. 79, 181-191.
Borges, F. and Martienssen, R.A. (2013) Establishing epigenetic variation during genome reprogramming. RNA Biol. 10, 490-494.
Braun, J.E., Huntzinger, E., Fauser, M. and Izaurralde, E. (2011) GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets. Mol. Cell. 44, 120-133.
Chen, C.Y. and Shyu, A.B. (2011) Mechanisms of deadenylation-dependent decay. Wiley Interdiscipl. Rev. RNA. 2, 167-183.
Collart, M.A. and Panasenko, O.O. (2012) The Ccr4-not complex. Gene, 492, 42-53.
Collart, M.A., Panasenko, O.O. and Nikolaev, S.I. (2013) The Not3/5 subunit of the Ccr4-Not complex: a central regulator of gene expression that integrates signals between the cytoplasm and the nucleus in eukaryotic cells. Cell. Signal. 25, 743-751.
Dou, K., Huang, C.F., Ma, Z.Y., Zhang, C.J., Zhou, J.X., Huang, H.W., Cai, T., Tang, K., Zhu, J.K. and He, X.J. (2013) The PRP6-like splicing factor STA1 is involved in RNA-directed DNA methylation by facilitating the production of Pol V-dependent scaffold RNAs. Nucl. Acids Res. 41, 8489-8502.
Du, J., Johnson, L.M., Jacobsen, S.E. and Patel, D.J. (2015) DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol. 16, 519-532.
Garneau, N.L., Wilusz, J. and Wilusz, C.J. (2007) The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8, 113-126.
Gong, Z., Morales-Ruiz, T., Ariza, R.R., Roldan-Arjona, T., David, L. and Zhu, J.K. (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell, 111, 803-814.
Haag, J.R. and Pikaard, C.S. (2011) Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol. 12, 483-492.
Haag, J.R., Ream, T.S., Marasco, M., Nicora, C.D., Norbeck, A.D., Pasa-Tolic, L. and Pikaard, C.S. (2012) In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell. 48, 811-818.
Han, Y.F., Dou, K., Ma, Z.Y., Zhang, S.W., Huang, H.W., Li, L., Cai, T., Chen, S., Zhu, J.K. and He, X.J. (2014) SUVR2 is involved in transcriptional gene silencing by associating with SNF2-related chromatin-remodeling proteins in Arabidopsis. Cell Res. 24, 1445-1465.
Han, Y.F., Zhao, Q.Y., Dang, L.L. et al. (2016) The SUMO E3 ligase-like proteins PIAL1 and PIAL2 interact with MOM1 and form a novel complex required for transcriptional silencing. Plant Cell, 28, 1215-1229.
He, X.J., Chen, T. and Zhu, J.K. (2011) Regulation and function of DNA methylation in plants and animals. Cell Res. 21, 442-465.
He, X.J., Hsu, Y.F., Pontes, O., Zhu, J., Lu, J., Bressan, R.A., Pikaard, C., Wang, C.S. and Zhu, J.K. (2009a) NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation. Genes Dev. 23, 318-330.
He, X.J., Hsu, Y.F., Zhu, S., Wierzbicki, A.T., Pontes, O., Pikaard, C.S., Liu, H.L., Wang, C.S., Jin, H. and Zhu, J.K. (2009b) An effector of RNA-directed DNA methylation in arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell, 137, 498-508.
He, X.J., Ma, Z.Y. and Liu, Z.W. (2014) Non-coding RNA transcription and RNA-directed DNA methylation in Arabidopsis. Mol. Plant. 7, 1406-1414.
Henderson, I.R. and Jacobsen, S.E. (2008) Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading. Genes Dev. 22, 1597-1606.
Herr, A.J., Jensen, M.B., Dalmay, T. and Baulcombe, D.C. (2005) RNA polymerase IV directs silencing of endogenous DNA. Science, 308, 118-120.
Inada, T. and Makino, S. (2014) Novel roles of the multi-functional CCR4-NOT complex in post-transcriptional regulation. Front. Genet. 5, 135.
Johnson, L.M., Du, J., Hale, C.J. et al. (2014) SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature, 507, 124-128.
Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
Law, J.A., Du, J., Hale, C.J., Feng, S., Krajewski, K., Palanca, A.M., Strahl, B.D., Patel, D.J. and Jacobsen, S.E. (2013) Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature, 498, 385-389.
Law, J.A. and Jacobsen, S.E. (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204-220.
Lee, T.F., Gurazada, S.G., Zhai, J., Li, S., Simon, S.A., Matzke, M.A., Chen, X. and Meyers, B.C. (2012) RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats. Epigenetics, 7, 781-795.
Li, S., Vandivier, L.E., Tu, B., Gao, L., Won, S.Y., Li, S., Zheng, B., Gregory, B.D. and Chen, X. (2015) Detection of Pol IV/RDR2-dependent transcripts at the genomic scale in Arabidopsis reveals features and regulation of siRNA biogenesis. Genome Res. 25, 235-245.
Liu, J., Bai, G., Zhang, C., Chen, W., Zhou, J., Zhang, S., Chen, Q., Deng, X., He, X.J. and Zhu, J.K. (2011) An atypical component of RNA-directed DNA methylation machinery has both DNA methylation-dependent and -independent roles in locus-specific transcriptional gene silencing. Cell Res. 21, 1691-1700.
Liu, Z.W., Shao, C.R., Zhang, C.J., Zhou, J.X., Zhang, S.W., Li, L., Chen, S., Huang, H.W., Cai, T. and He, X.J. (2014) The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci. PLoS Genet. 10, e1003948.
Liu, Z.W., Zhou, J.X., Huang, H.W., Li, Y.Q., Shao, C.R., Li, L., Cai, T., Chen, S. and He, X.J. (2016) Two Components of the RNA-Directed DNA methylation pathway associate with MORC6 and silence loci targeted by MORC6 in Arabidopsis. PLoS Genet. 12, e1006026.
Mathys, H., Basquin, J., Ozgur, S., Czarnocki-Cieciura, M., Bonneau, F., Aartse, A., Dziembowski, A., Nowotny, M., Conti, E. and Filipowicz, W. (2014) Structural and biochemical insights to the role of the CCR4-NOT complex and DDX6 ATPase in microRNA repression. Mol. Cell. 54, 751-765.
Matzke, M.A. and Mosher, R.A. (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15, 394-408.
Miller, J.E. and Reese, J.C. (2012) Ccr4-Not complex: the control freak of eukaryotic cells. Crit. Rev. Biochem. Mol. Biol. 47, 315-333.
Mosher, R.A., Schwach, F., Studholme, D. and Baulcombe, D.C. (2008) PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc. Natl Acad. Sci. USA. 105, 3145-3150.
Motomura, K., Arae, T., Araki-Uramoto, H. et al. (2020) AtNOT1 Is a novel regulator of gene expression during pollen development. Plant Cell Physiol. 61, 712-721.
Naftelberg, S., Schor, I.E., Ast, G. and Kornblihtt, A.R. (2015) Regulation of alternative splicing through coupling with transcription and chromatin structure. Annu. Rev. Biochem. 84, 165-198.
Nasertorabi, F., Batisse, C., Diepholz, M., Suck, D. and Bottcher, B. (2011) Insights into the structure of the CCR4-NOT complex by electron microscopy. FEBS Lett. 585, 2182-2186.
Neugebauer, K.M. (2002) On the importance of being co-transcriptional. J. Cell Sci. 115, 3865-3871.
Pontes, O., Li, C.F., Costa Nunes, P., Haag, J., Ream, T., Vitins, A., Jacobsen, S.E. and Pikaard, C.S. (2006) The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell, 126, 79-92.
Reddy, A.S., Marquez, Y., Kalyna, M. and Barta, A. (2013) Complexity of the alternative splicing landscape in plants. Plant Cell. 25, 3657-3683.
Shirai, Y.T., Suzuki, T., Morita, M., Takahashi, A. and Yamamoto, T. (2014) Multifunctional roles of the mammalian CCR4-NOT complex in physiological phenomena. Front. Genet. 5, 286.
Stroud, H., Greenberg, M.V., Feng, S., Bernatavichute, Y.V. and Jacobsen, S.E. (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell, 152, 352-364.
Suzuki, Y., Arae, T., Green, P.J., Yamaguchi, J. and Chiba, Y. (2015) AtCCR4a and AtCCR4b are involved in determining the Poly(A) length of granule-bound starch synthase 1 transcript and modulating sucrose and starch metabolism in Arabidopsis thaliana. Plant Cell Physiol. 56, 863-874.
Tabach, Y., Billi, A.C., Hayes, G.D. et al. (2013) Identification of small RNA pathway genes using patterns of phylogenetic conservation and divergence. Nature, 493, 694-698.
Temme, C., Simonelig, M. and Wahle, E. (2014) Deadenylation of mRNA by the CCR4-NOT complex in Drosophila: molecular and developmental aspects. Front. Genet. 5, 143.
van Hoof, A. and Parker, R. (2002) Messenger RNA degradation: beginning at the end. Curr. Biol. 12, R285-R287.
Wahle, E. and Winkler, G.S. (2013) RNA decay machines: deadenylation by the Ccr4-not and Pan2-Pan3 complexes. Biochem. Biophys. Acta. 1829, 561-570.
Walley, J.W., Kelley, D.R., Nestorova, G., Hirschberg, D.L. and Dehesh, K. (2010) Arabidopsis deadenylases AtCAF1a and AtCAF1b play overlapping and distinct roles in mediating environmental stress responses. Plant Physiol. 152, 866-875.
Wang, L., Song, X., Gu, L., Li, X., Cao, S., Chu, C., Cui, X., Chen, X. and Cao, X. (2013) NOT2 Proteins promote polymerase II-dependent transcription and interact with multiple microRNA biogenesis factors in Arabidopsis. Plant Cell. 25, 715-727.
Wang, W., Ye, R., Xin, Y., Fang, X., Li, C., Shi, H., Zhou, X. and Qi, Y. (2011) An importin beta protein negatively regulates MicroRNA activity in Arabidopsis. Plant Cell. 23, 3565-3576.
Wierzbicki, A.T., Cocklin, R., Mayampurath, A., Lister, R., Rowley, M.J., Gregory, B.D., Ecker, J.R., Tang, H. and Pikaard, C.S. (2012) Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev. 26, 1825-1836.
Wierzbicki, A.T., Haag, J.R. and Pikaard, C.S. (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell, 135, 635-648.
Xie, Z., Johansen, L.K., Gustafson, A.M., Kasschau, K.D., Lellis, A.D., Zilberman, D., Jacobsen, S.E. and Carrington, J.C. (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104.
Yamanaka, S., Mehta, S., Reyes-Turcu, F.E., Zhuang, F., Fuchs, R.T., Rong, Y., Robb, G.B. and Grewal, S.I. (2013) RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature, 493, 557-560.
Yang, D.L., Zhang, G., Tang, K., Li, J., Yang, L., Huang, H., Zhang, H. and Zhu, J.K. (2015) Dicer-independent RNA-directed DNA methylation in Arabidopsis. Cell Res. 26, 66-82.
Yang, D.L., Zhang, G., Wang, L. et al. (2018) Four putative SWI2/SNF2 chromatin remodelers have dual roles in regulating DNA methylation in Arabidopsis. Cell Discov. 4, 55.
Ye, R., Chen, Z., Lian, B., Rowley, M.J., Xia, N., Chai, J., Li, Y., He, X.J., Wierzbicki, A.T. and Qi, Y. (2016) A dicer-independent route for biogenesis of siRNAs that direct DNA methylation in Arabidopsis. Mol. Cell. 61, 222-235.
Ye, R., Wang, W., Iki, T., Liu, C., Wu, Y., Ishikawa, M., Zhou, X. and Qi, Y. (2012) Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol. Cell. 46, 859-870.
Zemach, A., Kim, M.Y., Hsieh, P.H., Coleman-Derr, D., Eshed-Williams, L., Thao, K., Harmer, S.L. and Zilberman, D. (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell, 153, 193-205.
Zhai, J., Bischof, S., Wang, H. et al. (2015) A one precursor one siRNA model for Pol IV-dependent siRNA biogenesis. Cell, 163, 445-455.
Zhang, C.J., Ning, Y.Q., Zhang, S.W., Chen, Q., Shao, C.R., Guo, Y.W., Zhou, J.X., Li, L., Chen, S. and He, X.J. (2012) IDN2 and its paralogs form a complex required for RNA-directed DNA methylation. PLoS Genet. 8, e1002693.
Zhang, C.J., Zhou, J.X., Liu, J. et al. (2013a) The splicing machinery promotes RNA-directed DNA methylation and transcriptional silencing in Arabidopsis. EMBO J. 32, 1128-1140.
Zhang, H., Lang, Z. and Zhu, J.K. (2018) Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19, 489-506.
Zhang, H., Ma, Z.Y., Zeng, L. et al. (2013b) DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. Proc. Natl Acad. Sci. USA. 110, 8290-8295.
Zhang, H., Tang, K., Qian, W. et al. (2014) An Rrp6-like protein positively regulates noncoding RNA levels and DNA methylation in Arabidopsis. Mol. Cell. 54, 418-430.
Zhang, X., Henderson, I.R., Lu, C., Green, P.J. and Jacobsen, S.E. (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc. Natl Acad. Sci. USA. 104, 4536-4541.
Zheng, B., Wang, Z., Li, S., Yu, B., Liu, J.Y. and Chen, X. (2009) Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 23, 2850-2860.
Zhong, X., Du, J., Hale, C.J., Gallego-Bartolome, J., Feng, S., Vashisht, A.A., Chory, J., Wohlschlegel, J.A., Patel, D.J. and Jacobsen, S.E. (2014) Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell, 157, 1050-1060.
Zhou, H.R., Zhang, F.F., Ma, Z.Y., Huang, H.W., Jiang, L., Cai, T., Zhu, J.K., Zhang, C. and He, X.J. (2013) Folate polyglutamylation is involved in chromatin silencing by maintaining global DNA methylation and histone H3K9 dimethylation in Arabidopsis. Plant Cell. 25, 2545-2559.
Zhou, M., Palanca, A.M.S. and Law, J.A. (2018) Locus-specific control of the de novo DNA methylation pathway in Arabidopsis by the CLASSY family. Nat. Genet. 50, 865-873.