Photodamage repair pathways contribute to the accurate maintenance of the DNA methylome landscape upon UV exposure

English version

Autoři: Stéfanie Graindorge ^aff001; Valérie Cognat ^aff001; Philippe Johann to Berens ^aff001; Jérôme Mutterer ^aff001; Jean Molinier ^aff001
Působiště autorů: Institut de biologie moléculaire des plantes, UPR2357-CNRS, Strasbourg, France ^aff001
Vyšlo v časopise: Photodamage repair pathways contribute to the accurate maintenance of the DNA methylome landscape upon UV exposure. PLoS Genet 15(11): e32767. doi:10.1371/journal.pgen.1008476
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1008476

Souhrn

Plants are exposed to the damaging effect of sunlight that induces DNA photolesions. In order to maintain genome integrity, specific DNA repair pathways are mobilized. Upon removal of UV-induced DNA lesions, the accurate re-establishment of epigenome landscape is expected to be a prominent step of these DNA repair pathways. However, it remains poorly documented whether DNA methylation is accurately maintained at photodamaged sites and how photodamage repair pathways contribute to the maintenance of genome/methylome integrities.

Using genome wide approaches, we report that UV-C irradiation leads to CHH DNA methylation changes. We identified that the specific DNA repair pathways involved in the repair of UV-induced DNA lesions, Direct Repair (DR), Global Genome Repair (GGR) and small RNA-mediated GGR prevent the excessive alterations of DNA methylation landscape. Moreover, we identified that UV-C irradiation induced chromocenter reorganization and that photodamage repair factors control this dynamics. The methylome changes rely on misregulation of maintenance, de novo and active DNA demethylation pathways highlighting that molecular processes related to genome and methylome integrities are closely interconnected. Importantly, we identified that photolesions are sources of DNA methylation changes in repressive chromatin. This study unveils that DNA repair factors, together with small RNA, act to accurately maintain both genome and methylome integrities at photodamaged silent genomic regions, strengthening the idea that plants have evolved sophisticated interplays between DNA methylation dynamics and DNA repair.

Klíčová slova:

DNA methylation – Plant genomics – Methylation – Small interfering RNAs – DNA damage – DNA repair – Arabidopsis thaliana – Ultraviolet C

Zdroje

1. Wang G, Vasquez KM. Effects of Replication and Transcription on DNA Structure-Related Genetic Instability. Genes. 2017; 1: pii: E17.

2. Eberhard S, Finazzi G, Wollman FA. The dynamics of photosynthesis. Annual Review of Genetics. 2008; 42: 463–515. doi: 10.1146/annurev.genet.42.110807.091452 18983262

3. Molinier J. Genome and Epigenome Surveillance Processes Underlying UV Exposure in Plants. Genes. 2017; 11: pii: E316.

4. Britt AB. Repair of DNA damage induced by ultraviolet radiation. Plant Physiol. 1995; 108: 891–896. doi: 10.1104/pp.108.3.891 7630970

5. Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T. Bursts of retrotransposition reproduced in Arabidopsis. Nature. 2009; 7262: 423–426.

6. Tittel-Elmer M, Bucher E, Broger L, Mathieu O, Paszkowski J, Vaillant I. Stress-induced activation of heterochromatic transcription. PLoS Genet. 2010; 6: e1001175. doi: 10.1371/journal.pgen.1001175 21060865

7. Bennetzen JL. Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev. 2005; 6: 621–627.

8. Kim MY, Zilberman D. DNA methylation as a system of plant genomic immunity. Trends Plant Sci. 2014; 5: 320–326.

9. Spampinato CP. Protecting DNA from errors and damage: an overview of DNA repair mechanisms in plants compared to mammals. Cell Mol Life Sci. 2017; 9: 1693–1709.

10. Schuch AP, Garcia CC, Makita K, Menck CF. DNA damage as a biological sensor for environmental sunlight. Photochem. Photobiol. Sci. 2013; 8: 1259–1272.

11. Mullenders LHF. Solar UV damage to cellular DNA: from mechanisms to biological effects. Photochem Photobiol Sci. 2018; 12: 1842–1852.

12. Tomura T, van Lancker JL. DNA repair of U.V.-damage in heterochromatin and euchromatin of rat liver. Int J Radiat Biol Relat Stud Phys Chem Med. 1980; 2: 231–235.

13. Sancar A. Photolyase and cryptochrome blue-light photoreceptors. Adv. Protein Chem. 2004; 73–100. doi: 10.1016/S0065-3233(04)69003-6 15588840

14. Schärer OD. Nucleotide Excision Repair in Eukaryotes. Cold Spring Harb. Perspect. Biol. 2013; 5: a012609. doi: 10.1101/cshperspect.a012609 24086042

15. Chu G and Chang E. Xeroderma pigmentosum group E cells lack a nuclear factor that binds to damaged DNA. Science. 1988; 4878: 564–567.

16. Schalk C, Cognat V, Graindorge S, Vincent T, Voinnet O, Molinier J. Small RNA-mediated repair of UV-induced DNA lesions by the DNA DAMAGE BINDING protein 2 and ARGONAUTE 1. PNAS. 2017; 14: E2965–E2974.

17. Rigal M, Mathieu O. A "mille-feuille" of silencing: epigenetic control of transposable elements. Biochim Biophys Acta. 2011; 1809: 452–458. doi: 10.1016/j.bbagrm.2011.04.001 21514406

18. Law JA and Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 2010; 11: 204–220. doi: 10.1038/nrg2719 20142834

19. Matzke MA and Mosher RA. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 2014; 15: 394–408. doi: 10.1038/nrg3683 24805120

20. Zhang H, Lang Z, Zhu JK. Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol. 2018; 8: 489–506.

21. Zhu JK. Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet. 2009; 43: 143–66. doi: 10.1146/annurev-genet-102108-134205 19659441

22. Virdi KS, Laurie JD, Xu YZ, Yu J, Shao MR, Sanchez R, Kundariya H, Wang D, Riethoven JJ, Wamboldt Y, Arrieta-Montiel MP, Shedge V, Mackenzie SA. Arabidopsis MSH1 mutation alters the epigenome and produces heritable changes in plant growth. Nat Commun. 2015; 6: 6386. doi: 10.1038/ncomms7386 25722057

23. Schalk C, Drevensek S, Kramdi A, Kassam M, Ahmed I, Cognat V, Graindorge S, Bergdoll M, Baumberger N, Heintz D, Bowler C, Genschik P, Barneche F, Colot V, Molinier J. DNA DAMAGE BINDING PROTEIN 2 (DDB2) Shapes the DNA Methylation Landscape. Plant Cell. 2016; 9: 2043–2059.

24. Córdoba-Cañero D, Cognat V, Ariza RR, Roldán Arjona T, Molinier J. Dual control of ROS1-mediated active DNA demethylation by the DNA DAMAGE BINDING protein 2 (DDB2). Plant J. 2017; 6: 1170–1181.

25. Le May N, Fradin D, Iltis I, Bougnères P, Egly JM. XPG and XPF endonucleases trigger chromatin looping and DNA demethylation for accurate expression of activated genes. Mol Cell. 2012; 4: 622–632.

26. Schalk C, Molinier J. Global Genome Repair factors control DNA methylation patterns in Arabidopsis. Plant Signaling & Behavior. 2016; 12: e1253648.

27. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR. Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl. Acad. Sci. USA 2012; 109: E2183–E2191. doi: 10.1073/pnas.1209329109 22733782

28. Yu A, Lepère G, Jay F, Wang J, Bapaume L, Wang Y, Abraham AL, Penterman J, Fischer RL, Voinnet O, Navarro L 2013. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc Natl Acad Sci U S A. 2013; 6: 2389–2394.

29. Yong-Villalobos L, González-Morales SI, Wrobel K, Gutiérrez-Alanis D, Cervantes-Peréz SA, Hayano-Kanashiro C, Oropeza-Aburto A, Cruz-Ramírez A, Martínez O, Herrera-Estrella L. Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc. Natl. Acad. Sci. USA. 2015; 112: E7293–E7302. doi: 10.1073/pnas.1522301112 26668375

30. Liu TK, Li Y, Duan WK, Huang FY, Hou XL. Cold acclimation alters DNA methylation patterns and confers tolerance to heat and increases growth rate in Brassica rapa. J. Exp. Bot. 2017; 68: 1213–1224. doi: 10.1093/jxb/erw496 28158841

31. Secco D, Wang C, Shou H, Schultz MD, Chiarenza S, Nussaume L, Ecker JR, Whelan J, Lister R. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife, 2015; 4: e09343.

32. Eichten SR, Springer NM. Minimal evidence for consistent changes in maize DNA methylation patterns following environmental stress. Front. Plant Sci. 2015; 6: 308. doi: 10.3389/fpls.2015.00308 25999972

33. Schuermann D, Molinier J, Fritsch O, Hohn B. The dual nature of homologous recombination in plants. Trends in Genetics. 2005; 21: 172–181. doi: 10.1016/j.tig.2005.01.002 15734576

34. Molinier J, Ramos C, Fritsch O, Hohn B. CENTRIN 2 modulates Homologous Recombination and Nucleotide Excision Repair in Arabidopsis. Plant Cell. 2004; 16: 1633–1643. doi: 10.1105/tpc.021378 15155891

35. Molinier J, Oakeley EJ, Niederhauser O, Kovalchuk I, Hohn B. Dynamic response of plant genome to ultraviolet and other genotoxic stresses. Mutation Research. 2005; 571: 235–247. doi: 10.1016/j.mrfmmm.2004.09.016 15748650

36. Sequeira-Mendes J, Aragüez I, Peiró R, Mendez-Giraldez R, Zhang X, Jacobsen SE, Bastolla U, Gutierrez C. The Functional Topography of the Arabidopsis Genome Is Organized in a Reduced Number of Linear Motifs of Chromatin States. Plant Cell. 2014; 6: 2351–2366.

37. Cao X, Jacobsen SE. Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc. Natl. Acad. Sci. U S A. 2002; 4: 16491–16498.

38. Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell. 2013; 1–2: 352–364.

39. Castells E, Molinier J, Genschik P, Drevensek S, Barneche F, Bowler C. det1-1 induced UV-C hyposensitivity through UVR3 and PHR1 photolyase overexpression. Plant J. 2010; 63: 392–404. doi: 10.1111/j.1365-313X.2010.04249.x 20487384

40. Molinier J, Lechner E, Dumbliauskas E, Genschik P. Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. Plos Genet. 2008; 6: e1000093.

41. Ries G, Buchholz G, Frohnmeyer H, Hohn B. UV-damage-mediated induction of homologous recombination in Arabidopsis is dependent on photosynthetically active radiation. Proc Natl Acad Sci U S A. 2000; 24: 13425–13429.

42. Morel JB, Godon C, Mourrain P, Béclin C, Boutet S, Feuerbach F, Proux F, Vaucheret H. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell. 2002; 3: 629–639.

43. Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature. 2011; 7341: 115–119.

44. Walbot V. UV-B damage amplified by transposons in maize. Nature. 1999; 6718: 398–399.

45. Xu W, Wang T, Xu S, Li F, Deng C, Wu L, Wu Y, Bian P. UV-C-Induced alleviation of transcriptional gene silencing through plant-plant communication: Key roles of jasmonic acid and salicylic acid pathways. Mutat Res. 2016; 790: 56–67. doi: 10.1016/j.mrfmmm.2016.04.003 27131397

46. Van Dooren TJM, Bortolini Silveira A, Gilbault E, Jiménez-Gómez JM, Martin A, Bach L, Tisné S, Quadrana L, Loudet O, Colot V. Mild drought induces phenotypic and DNA methylation plasticity but no transgenerational effects in Arabidopsis. bioRxiv 370320; https://doi.org/10.1101/370320.

47. Fransz P, De Jong JH, Lysak M, Castiglione MR, Schubert I. Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc Natl Acad Sci U S A. 2002; 22: 14584–14589.

48. Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Mittelsten Scheid O. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell. 2010; 9: 3118–3129.

49. Cuerda-Gil D and Slotkin RK. Non-canonical RNA-directed DNA methylation. Nat. Plants. 2016; 11: 16163.

50. Pontier D, Picart C, Roudier F, Garcia D, Lahmy S, Azevedo J, Alart E, Laudié M, Karlowski WM, Cooke R, Colot V, Voinnet O, Lagrange T. NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol Cell. 2012; 1: 121–132.

51. McCue AD, Panda K, Nuthikattu S, Choudury SG, Thomas EN, Slotkin RK. ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. EMBO J. 2015; 1: 20–35.

52. Ahmed I, Sarazin A, Bowler C, Colot V, Quesneville H. Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res. 2011; 16: 6919–6931.

53. Ye R, Chen Z, Lian B, Rowley MJ, Xia N, Chai J, Li Y, He XJ, Wierzbicki AT, Qi Y. A Dicer-Independent Route for Biogenesis of siRNAs that Direct DNA Methylation in Arabidopsis. Mol Cell. 2016; 2: 222–235.

54. Ulm R, Jenkins GI. Q&A: How do plants sense and respond to UV-B radiation? BMC Biol. 2015; 13: 45. doi: 10.1186/s12915-015-0156-y 26123292

55. Bourguet P, de Bossoreille S, López-González L, Pouch-Pélissier MN, Gómez-Zambrano Á, Devert A, Pélissier T, Pogorelcnik R, Vaillant I, Mathieu O. A role for MED14 and UVH6 in heterochromatin transcription upon destabilization of silencing. Life Sci Alliance. 2018; 6: e201800197.

56. Groisman R, Polanowska J, Kuraoka I, Sawada J, Saijo M, Drapkin R, Kisselev AF, Tanaka K, Nakatani Y. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell. 2003; 3: 357–367.

57. Marí-Ordóñez A Marchais A, Etcheverry M, Martin A, Colot V, Voinnet O. Reconstructing de novo silencing of an active plant retrotransposon. Nat. Genet. 2013; 45: 1029–1039. doi: 10.1038/ng.2703 23852169

58. Nuthikattu S, McCue AD, Panda K, Fultz D, DeFraia C, Thomas EN, Slotkin RK. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21–22 nucleotide small interfering RNAs. Plant Physiol. 2013; 1: 116–131.

59. Rochette PJ, Lacoste S, Therrien JP, Bastien N, Brash DE, Drouin R. Influence of cytosine methylation on ultraviolet-induced cyclobutane pyrimidine dimer formation in genomic DNA. Mutat Res. 2009; 665: 7–13. doi: 10.1016/j.mrfmmm.2009.02.008 19427505

60. Hu J, Lieb JD, Sancar A, Adar S. Cisplatin DNA damage and repair maps of the human genome at single-nucleotide resolution. Proc Natl Acad Sci U S A. 2016; 41: 11507–11512.

61. Bourbousse C, Mestiri I, Zabulon G, Bourge M, Formiggini F, Koini MA, Brown SC, Fransz P, Bowler C, Barneche F. Light signaling controls nuclear architecture reorganization during seedling establishment. Proc Natl Acad Sci U S A. 2015; 21: E2836–E2844.

62. Castells E, Molinier J, Benvenuto G, Bourbousse C, Zabulon G, Zalc A, Cazzaniga S, Genschik P, Barneche F, Bowler C. The conserved factor DE-ETIOLATED 1 cooperates with CUL4-DDB1DDB2 to maintain genome integrity upon UV stress. EMBO J. 2011; 6: 1162–1172.

63. Fei J, Kaczmarek N, Luch A, Glas A, Carell T, Naegeli H. Regulation of nucleotide excision repair by UV-DDB: prioritization of damage recognition to internucleosomal DNA. PLoS Biol. 2011; 10: e1001183.

64. Feng W, Michaels SD. Accessing the Inaccessible: The Organization, Transcription, Replication, and Repair of Heterochromatin in Plants. Annu Rev Genet. 2015; 49: 439–459. doi: 10.1146/annurev-genet-112414-055048 26631514

65. Simon L, Voisin M, Tatout C, Probst AV. Structure and Function of Centromeric and Pericentromeric Heterochromatin in Arabidopsis thaliana Front Plant Sci. 2015; 6: 1049. doi: 10.3389/fpls.2015.01049 26648952

66. Puchta H, Swoboda P, Gal S, Blot M, Hohn B. Somatic intrachromosomal homologous recombination events in populations of plant siblings. Plant Mol Biol. 1995; 2: 281–292.

67. Questa J, Walbot V, Casati P. UV-B radiation induces Mu element somatic transposition in maize. Mol Plant. 2013; 6: 2004–2007. doi: 10.1093/mp/sst112 23877058

68. Ito H, Yoshida T, Tsukahara S, Kawabe A. Evolution of the ONSEN retrotransposon family activated upon heat stress in Brassicaceae. Gene. 2013; 2: 256–261.

69. Masuda S, Nozawa K, Matsunaga W, Masuta Y, Kawabe A, Kato A, Ito H. Characterization of a heat-activated retrotransposon in natural accessions of Arabidopsis thaliana. Genes Genet Syst. 2017; 6: 293–299.

70. Daccord N, Celton JM, Linsmith G, Becker C, Choisne N, Schijlen E, van de Geest H, Bianco L, Micheletti D, Velasco R, Di Pierro EA, Gouzy J, Rees DJG, Guérif P, Muranty H, Durel CE, Laurens F, Lespinasse Y, Gaillard S, Aubourg S, Quesneville H, Weigel D, van de Weg E, Troggio M, Bucher E. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet. 2017; 7: 1099–1106.