The plant mobile domain proteins MAIN and MAIL1 interact with the phosphatase PP7L to regulate gene expression and silence transposable elements in Arabidopsis thaliana
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Melody Nicolau aff001; Nathalie Picault aff001; Julie Descombin aff001; Yasaman Jami-Alahmadi aff003; Suhua Feng aff004; Etienne Bucher aff005; Steven E. Jacobsen aff004; Jean-Marc Deragon aff001; James Wohlschlegel aff003; Guillaume Moissiard aff001
Působiště autorů:
LGDP-UMR5096, CNRS, Perpignan, France
aff001; LGDP-UMR5096, Université de Perpignan, France
aff002; Department of Biological Chemistry, University of California at Los Angeles, Los Angeles, California, United States of America
aff003; Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, California, United States of America
aff004; Plant Breeding and Genetic Resources, Agroscope, Nyon, Switzerland
aff005; Howard Hughes Medical Institute, University of California at Los Angeles, Los Angeles, California, United States of America
aff006; Institut Universitaire de France, Paris, France
aff007
Vyšlo v časopise:
The plant mobile domain proteins MAIN and MAIL1 interact with the phosphatase PP7L to regulate gene expression and silence transposable elements in Arabidopsis thaliana. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008324
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008324
Souhrn
Transposable elements (TEs) are DNA repeats that must remain silenced to ensure cell integrity. Several epigenetic pathways including DNA methylation and histone modifications are involved in the silencing of TEs, and in the regulation of gene expression. In Arabidopsis thaliana, the TE-derived plant mobile domain (PMD) proteins have been involved in TE silencing, genome stability, and control of developmental processes. Using a forward genetic screen, we found that the PMD protein MAINTENANCE OF MERISTEMS (MAIN) acts synergistically and redundantly with DNA methylation to silence TEs. We found that MAIN and its close homolog MAIN-LIKE 1 (MAIL1) interact together, as well as with the phosphoprotein phosphatase (PPP) PP7-like (PP7L). Remarkably, main, mail1, pp7l single and mail1 pp7l double mutants display similar developmental phenotypes, and share common subsets of upregulated TEs and misregulated genes. Finally, phylogenetic analyses of PMD and PP7-type PPP domains among the Eudicot lineage suggest neo-association processes between the two protein domains to potentially generate new protein function. We propose that, through this interaction, the PMD and PPP domains may constitute a functional protein module required for the proper expression of a common set of genes, and for silencing of TEs.
Klíčová slova:
Arabidopsis thaliana – DNA methylation – Flowering plants – Gene expression – Genetic loci – Plant genomics – Protein domains – Sequence motif analysis
Zdroje
1. Grewal SI, Jia S. Heterochromatin revisited. Nat Rev Genet. 2007;8(1):35–46. doi: 10.1038/nrg2008 17173056
2. Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8(4):272–85. doi: 10.1038/nrg2072 17363976
3. Deniz O, Frost JM, Branco MR. Regulation of transposable elements by DNA modifications. Nat Rev Genet. 2019;20(7):417–31. doi: 10.1038/s41576-019-0106-6 30867571
4. Dergai O, Hernandez N. How to Recruit the Correct RNA Polymerase? Lessons from snRNA Genes. Trends Genet. 2019;35(6):457–69. doi: 10.1016/j.tig.2019.04.001 31040056
5. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010;11(3):204–20. doi: 10.1038/nrg2719 20142834
6. Matzke MA, Mosher RA. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet. 2014;15(6):394–408. doi: 10.1038/nrg3683 24805120
7. Wendte JM, Pikaard CS. The RNAs of RNA-directed DNA methylation. Biochim Biophys Acta. 2016.
8. Du J, Johnson LM, Jacobsen SE, Patel DJ. DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol. 2015;16(9):519–32. doi: 10.1038/nrm4043 26296162
9. Zhang H, Lang Z, Zhu JK. Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol. 2018;19(8):489–506. doi: 10.1038/s41580-018-0016-z 29784956
10. Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell. 2013;153(1):193–205. doi: 10.1016/j.cell.2013.02.033 23540698
11. Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, et al. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol. 2014;21(1):64–72. doi: 10.1038/nsmb.2735 24336224
12. Moissiard G, Cokus SJ, Cary J, Feng S, Billi AC, Stroud H, et al. MORC family ATPases required for heterochromatin condensation and gene silencing. Science. 2012;336(6087):1448–51. doi: 10.1126/science.1221472 22555433
13. Moissiard G, Bischof S, Husmann D, Pastor WA, Hale CJ, Yen L, et al. Transcriptional gene silencing by Arabidopsis microrchidia homologues involves the formation of heteromers. Proc Natl Acad Sci U S A. 2014;111(20):7474–9. doi: 10.1073/pnas.1406611111 24799676
14. Lorkovic ZJ, Naumann U, Matzke AJ, Matzke M. Involvement of a GHKL ATPase in RNA-directed DNA methylation in Arabidopsis thaliana. Curr Biol. 2012;22(10):933–8. doi: 10.1016/j.cub.2012.03.061 22560611
15. Ikeda Y, Pelissier T, Bourguet P, Becker C, Pouch-Pelissier MN, Pogorelcnik R, et al. Arabidopsis proteins with a transposon-related domain act in gene silencing. Nat Commun. 2017;8:15122. doi: 10.1038/ncomms15122 28466841
16. Wenig U, Meyer S, Stadler R, Fischer S, Werner D, Lauter A, et al. Identification of MAIN, a factor involved in genome stability in the meristems of Arabidopsis thaliana. Plant J. 2013;75(3):469–83. doi: 10.1111/tpj.12215 23607329
17. Uhlken C, Horvath B, Stadler R, Sauer N, Weingartner M. MAIN-LIKE1 is a crucial factor for correct cell division and differentiation in Arabidopsis thaliana. Plant J. 2014;78(1):107–20. doi: 10.1111/tpj.12455 24635680
18. Babu MM, Iyer LM, Balaji S, Aravind L. The natural history of the WRKY-GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Res. 2006;34(22):6505–20. doi: 10.1093/nar/gkl888 17130173
19. Steinbauerova V, Neumann P, Novak P, Macas J. A widespread occurrence of extra open reading frames in plant Ty3/gypsy retrotransposons. Genetica. 2011;139(11–12):1543–55. doi: 10.1007/s10709-012-9654-9 22544262
20. Farkas I, Dombradi V, Miskei M, Szabados L, Koncz C. Arabidopsis PPP family of serine/threonine phosphatases. Trends Plant Sci. 2007;12(4):169–76. doi: 10.1016/j.tplants.2007.03.003 17368080
21. Sun X, Kang X, Ni M. Hypersensitive to red and blue 1 and its modification by protein phosphatase 7 are implicated in the control of Arabidopsis stomatal aperture. PLoS Genet. 2012;8(5):e1002674. doi: 10.1371/journal.pgen.1002674 22589732
22. Liu HT, Li GL, Chang H, Sun DY, Zhou RG, Li B. Calmodulin-binding protein phosphatase PP7 is involved in thermotolerance in Arabidopsis. Plant Cell Environ. 2007;30(2):156–64. doi: 10.1111/j.1365-3040.2006.01613.x 17238907
23. Genoud T, Santa Cruz MT, Kulisic T, Sparla F, Fankhauser C, Metraux JP. The protein phosphatase 7 regulates phytochrome signaling in Arabidopsis. PLoS One. 2008;3(7):e2699. doi: 10.1371/journal.pone.0002699 18628957
24. Uhrig RG, Labandera AM, Moorhead GB. Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines. Trends Plant Sci. 2013;18(9):505–13. doi: 10.1016/j.tplants.2013.05.004 23790269
25. Xu D, Marino G, Klingl A, Enderle B, Monte E, Kurth J, et al. Extrachloroplastic PP7L Functions in Chloroplast Development and Abiotic Stress Tolerance. Plant Physiol. 2019.
26. Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell. 2013;152(1–2):352–64. doi: 10.1016/j.cell.2012.10.054 23313553
27. Fransz P, de Jong H. From nucleosome to chromosome: a dynamic organization of genetic information. Plant J. 2011;66(1):4–17. doi: 10.1111/j.1365-313X.2011.04526.x 21443619
28. Zhao S, Cheng L, Gao Y, Zhang B, Zheng X, Wang L, et al. Plant HP1 protein ADCP1 links multivalent H3K9 methylation readout to heterochromatin formation. Cell Res. 2019;29(1):54–66. doi: 10.1038/s41422-018-0104-9 30425322
29. Tessadori F, Schulkes RK, van Driel R, Fransz P. Light-regulated large-scale reorganization of chromatin during the floral transition in Arabidopsis. Plant J. 2007;50(5):848–57. doi: 10.1111/j.1365-313X.2007.03093.x 17470059
30. Yokthongwattana C, Bucher E, Caikovski M, Vaillant I, Nicolet J, Mittelsten Scheid O, et al. MOM1 and Pol-IV/V interactions regulate the intensity and specificity of transcriptional gene silencing. Embo J.29(2):340–51. doi: 10.1038/emboj.2009.328 19910926
31. Rigal M, Mathieu O. A "mille-feuille" of silencing: epigenetic control of transposable elements. Biochim Biophys Acta. 2011;1809(8):452–8. doi: 10.1016/j.bbagrm.2011.04.001 21514406
32. Galperin MY, Koonin EV. Who's your neighbor? New computational approaches for functional genomics. Nat Biotechnol. 2000;18(6):609–13. doi: 10.1038/76443 10835597
33. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16(6):735–43. doi: 10.1046/j.1365-313x.1998.00343.x 10069079
34. Hristova E, Fal K, Klemme L, Windels D, Bucher E. HISTONE DEACETYLASE6 Controls Gene Expression Patterning and DNA Methylation-Independent Euchromatic Silencing. Plant Physiol. 2015;168(4):1298–308. doi: 10.1104/pp.15.00177 25918117
35. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 24695404
36. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–60. doi: 10.1038/nmeth.3317 25751142
37. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9. doi: 10.1093/bioinformatics/btp352 19505943
38. Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166–9. doi: 10.1093/bioinformatics/btu638 25260700
39. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8 25516281
40. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47. doi: 10.1093/nar/gkv007 25605792
41. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 2005;139(1):5–17. doi: 10.1104/pp.105.063743 16166256
42. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37(Web Server issue):W202–8. doi: 10.1093/nar/gkp335 19458158
43. Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27(11):1571–2. doi: 10.1093/bioinformatics/btr167 21493656
44. Huang X, Zhang S, Li K, Thimmapuram J, Xie S, Wren J. ViewBS: a powerful toolkit for visualization of high-throughput bisulfite sequencing data. Bioinformatics. 2018;34(4):708–9. doi: 10.1093/bioinformatics/btx633 29087450
45. Catoni M, Tsang JM, Greco AP, Zabet NR. DMRcaller: a versatile R/Bioconductor package for detection and visualization of differentially methylated regions in CpG and non-CpG contexts. Nucleic Acids Res. 2018;46(19):e114. doi: 10.1093/nar/gky602 29986099
46. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. doi: 10.1093/nar/gkh340 15034147
47. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52(5):696–704. doi: 10.1080/10635150390235520 14530136
48. Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25(7):1307–20. doi: 10.1093/molbev/msn067 18367465
49. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol. 2006;55(4):539–52. doi: 10.1080/10635150600755453 16785212
50. Bernatavichute YV, Zhang X, Cokus S, Pellegrini M, Jacobsen SE. Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE. 2008;3(9):e3156. doi: 10.1371/journal.pone.0003156 18776934
51. Vergara Z, Gutierrez C. Emerging roles of chromatin in the maintenance of genome organization and function in plants. Genome Biol. 2017;18(1):96. doi: 10.1186/s13059-017-1236-9 28535770
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