#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization


Autoři: Nicolas Christophorou aff001;  Wenjing She aff002;  Jincheng Long aff002;  Aurélie Hurel aff001;  Sébastien Beaubiat aff001;  Yassir Idir aff001;  Marina Tagliaro-Jahns aff001;  Aurélie Chambon aff001;  Victor Solier aff001;  Daniel Vezon aff001;  Mathilde Grelon aff001;  Xiaoqi Feng aff002;  Nicolas Bouché aff001;  Christine Mézard aff001
Působiště autorů: Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech, Université Paris-Saclay, Versailles, France aff001;  Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom aff002
Vyšlo v časopise: AXR1 affects DNA methylation independently of its role in regulating meiotic crossover localization. PLoS Genet 16(6): e1008894. doi:10.1371/journal.pgen.1008894
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008894

Souhrn

Meiotic crossovers (COs) are important for reshuffling genetic information between homologous chromosomes and they are essential for their correct segregation. COs are unevenly distributed along chromosomes and the underlying mechanisms controlling CO localization are not well understood. We previously showed that meiotic COs are mis-localized in the absence of AXR1, an enzyme involved in the neddylation/rubylation protein modification pathway in Arabidopsis thaliana. Here, we report that in axr1-/-, male meiocytes show a strong defect in chromosome pairing whereas the formation of the telomere bouquet is not affected. COs are also redistributed towards subtelomeric chromosomal ends where they frequently form clusters, in contrast to large central regions depleted in recombination. The CO suppressed regions correlate with DNA hypermethylation of transposable elements (TEs) in the CHH context in axr1-/- meiocytes. Through examining somatic methylomes, we found axr1-/- affects DNA methylation in a plant, causing hypermethylation in all sequence contexts (CG, CHG and CHH) in TEs. Impairment of the main pathways involved in DNA methylation is epistatic over axr1-/- for DNA methylation in somatic cells but does not restore regular chromosome segregation during meiosis. Collectively, our findings reveal that the neddylation pathway not only regulates hormonal perception and CO distribution but is also, directly or indirectly, a major limiting pathway of TE DNA methylation in somatic cells.

Klíčová slova:

Arabidopsis thaliana – DNA methylation – Chromosome pairs – Leaves – Meiosis – Prophase – Telomeres – Cytosine


Zdroje

1. de Massy B. Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu Rev Genet. 2013;47: 563–599. doi: 10.1146/annurev-genet-110711-155423 24050176

2. Sturtevent AH. The behaviour of the chromosomes as studied through linkage. Mol Gen Genet Genet. 1915;13: 234–287.

3. Gray S, Cohen PE. Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation. Annu Rev Genet. 2016;50: 175–210. doi: 10.1146/annurev-genet-120215-035111 27648641

4. Jones GH, Franklin FCH. Meiotic crossing-over: obligation and interference. Cell. 2006;126: 246–8. doi: 10.1016/j.cell.2006.07.010 16873056

5. Talbert PB, Henikoff S. Centromeres convert but don’t cross. PLoS Biol. 2010;8: e1000326. doi: 10.1371/journal.pbio.1000326 20231873

6. Malik HS, Henikoff S. Major evolutionary transitions in centromere complexity. Cell. 2009;138: 1067–1082. doi: 10.1016/j.cell.2009.08.036 19766562

7. Vincenten N, Kuhl L-M, Lam I, Oke A, Kerr AR, Hochwagen A, et al. The kinetochore prevents centromere-proximal crossover recombination during meiosis. Elife. 2015;4: doi: 10.7554/eLife.10850 26653857

8. Nambiar M, Smith GR. Repression of harmful meiotic recombination in centromeric regions. Semin Cell Dev Biol. 2016;54: 188–197. doi: 10.1016/j.semcdb.2016.01.042 26849908

9. Sato S, Tabata S, Hirakawa H, Asamizu E, Shirasawa K, Isobe S, et al. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012;485: 635–641. doi: 10.1038/nature11119 22660326

10. Choulet F, Alberti A, Theil S, Glover N, Barbe V, Daron J, et al. Structural and functional partitioning of bread wheat chromosome 3B. Science (80-). 2014;345: 1249721. doi: 10.1126/science.1249721 25035497

11. Mayer KFX, Waugh R, Langridge P, Close TJ, Wise RP, Graner A, et al. A physical, genetic and functional sequence assembly of the barley genome. Nature. 2012;491: 711–716. doi: 10.1038/nature11543 23075845

12. Mézard C, Tagliaro Jahns M, Grelon M. Where to cross? New insights into the location of meiotic crossovers. Trends Genet. 2015;31: 393–401. doi: 10.1016/j.tig.2015.03.008 25907025

13. Smagulova F, Gregoretti I V, Brick K, Khil P, Camerini-Otero RD, Petukhova G V. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature. 2011/04/05. 2011;472: 375–378. doi: 10.1038/nature09869 21460839

14. Pratto F, Brick K, Khil P, Smagulova F, Petukhova G V, Camerini-Otero RD. DNA recombination. Recombination initiation maps of individual human genomes. Science (80-). 2014;346: 1256442. doi: 10.1126/science.1256442 25395542

15. He Y, Wang M, Dukowic-Schulze S, Zhou A, Tiang C-L, Shilo S, et al. Genomic features shaping the landscape of meiotic double-strand-break hotspots in maize. Proc Natl Acad Sci. 2017;114: 201713225. doi: 10.1073/pnas.1713225114 29087335

16. Choi K, Zhao X, Tock AJ, Lambing C, Underwood CJ, Hardcastle TJ, et al. Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions. Genome Res. 2018;28: 532–546. doi: 10.1101/gr.225599.117 29530928

17. Murakami H, Keeney S. Regulating the formation of DNA double-strand breaks in meiosis. Genes Dev. 2008;22: 286–92. doi: 10.1101/gad.1642308 18245442

18. Higgins JD, Perry RM, Barakate A, Ramsay L, Waugh R, Halpin C, et al. Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley. Plant Cell. 2012;24: 4096–4109. doi: 10.1105/tpc.112.102483 23104831

19. Serrentino M-E, Chaplais E, Sommermeyer V, Borde V. Differential association of the conserved SUMO ligase Zip3 with meiotic double-strand break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genet. 2013;9: e1003416. doi: 10.1371/journal.pgen.1003416 23593021

20. Joshi N, Brown MS, Bishop DK, Börner GV. Gradual Implementation of the Meiotic Recombination Program via Checkpoint Pathways Controlled by Global DSB Levels. Mol Cell. 2015;57: 797–811. doi: 10.1016/j.molcel.2014.12.027 25661491

21. Hulten M. Chiasma distribution at diakinesis in the normal human male. Hereditas. 1974;76: 55–78. doi: 10.1111/j.1601-5223.1974.tb01177.x 4136005

22. Revenkova E, Jessberger R. Shaping meiotic prophase chromosomes: cohesins and synaptonemal complex proteins. Chromosoma. 2006;115: 235–240. doi: 10.1007/s00412-006-0060-x 16518630

23. Qiao H, Offenberg HH, Anderson LK. Altered distribution of MLH1 foci is associated with changes in cohesins and chromosome axis compaction in an asynaptic mutant of tomato. Chromosoma. 2012;121: 291–305. doi: 10.1007/s00412-012-0363-z 22350750

24. Nabeshima K, Villeneuve AM, Hillers KJ. Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics. 2004/12/08. 2004;168: 1275–1292. doi: 10.1534/genetics.104.030700 15579685

25. Roig I, Dowdle JA, Toth A, de Rooij DG, Jasin M, Keeney S. Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLoS Genet. 2010;6: e1001062. doi: 10.1371/journal.pgen.1001062 20711356

26. Koszul R, Kleckner N. Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends in Cell Biology. 2009. pp. 716–724. doi: 10.1016/j.tcb.2009.09.007 19854056

27. Varas J, Graumann K, Osman K, Pradillo M, Evans DE, Santos JL, et al. Absence of SUN1 and SUN2 proteins in Arabidopsis thaliana leads to a delay in meiotic progression and defects in synapsis and recombination. Plant J. 2015;81: 329–346. doi: 10.1111/tpj.12730 25412930

28. Duroc Y, Lemhemdi A, Larchevêque C, Hurel A, Cuacos M, Cromer L, et al. The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis. PLoS Genet. 2014;10: e1004674. doi: 10.1371/journal.pgen.1004674 25330379

29. Zhang H, Lang Z, Zhu JK. Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol. 2018;19: 489–506. doi: 10.1038/s41580-018-0016-z 29784956

30. Matzke MA, Kanno T, Matzke AJM. RNA-Directed DNA Methylation: The Evolution of a Complex Epigenetic Pathway in Flowering Plants. Annu Rev Plant Biol. 2015;66: 243–267. doi: 10.1146/annurev-arplant-043014-114633 25494460

31. Walker J, Gao H, Zhang J, Aldridge B, Vickers M, Higgins JD, et al. Sexual-lineage-specific DNA methylation regulates meiosis in Arabidopsis. Nat Genet. 2018;50: 130–137. doi: 10.1038/s41588-017-0008-5 29255257

32. Underwood CJ, Choi K, Lambing C, Zhao X, Serra H, Borges F, et al. Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation. Genome Res. 2018;28: 519–531. doi: 10.1101/gr.227116.117 29530927

33. Yelina NE, Choi K, Chelysheva L, Macaulay M, de Snoo B, Wijnker E, et al. Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. Barsh GS, editor. PLoS Genet. 2012;8: e1002844. doi: 10.1371/journal.pgen.1002844 22876192

34. Colome-Tatche M, Cortijo S, Wardenaar R, Morgado L, Lahouze B, Sarazin A, et al. Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc Natl Acad Sci. 2012;109: 16240–16245. doi: 10.1073/pnas.1212955109 22988127

35. Melamed-Bessudo C, Levy A a. Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109: E981–8. doi: 10.1073/pnas.1120742109 22460791

36. Mirouze M, Lieberman-Lazarovich M, Aversano R, Bucher E, Nicolet J, Reinders J, et al. Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109: 5880–5. doi: 10.1073/pnas.1120841109 22451936

37. Jahns MT, Vezon D, Chambon A, Pereira L, Falque M, Martin OC, et al. Crossover localisation is regulated by the neddylation posttranslational regulatory pathway. Lichten M, editor. PLoS Biol. 2014;12: e1001930. doi: 10.1371/journal.pbio.1001930 25116939

38. Girard C, Chelysheva L, Choinard S, Froger N, Macaisne N, Lehmemdi A, et al. AAA-ATPase FIDGETIN-LIKE 1 and Helicase FANCM Antagonize Meiotic Crossovers by Distinct Mechanisms. PLoS Genet. 2015;11: e1005369. doi: 10.1371/journal.pgen.1005369 26161528

39. Scherthan H. A bouquet makes ends meet. Nature Reviews Molecular Cell Biology. 2001. pp. 621–627. doi: 10.1038/35085086 11483995

40. Zickler D, Kleckner N. A few of our favorite things: Pairing, the bouquet, crossover interference and evolution of meiosis. Semin Cell Dev Biol. 2016;54: 135–148. doi: 10.1016/j.semcdb.2016.02.024 26927691

41. Hurel A, Phillips D, Vrielynck N, Mézard C, Grelon M, Christophorou N. A cytological approach to studying meiotic recombination and chromosome dynamics in Arabidopsis thaliana male meiocytes in three dimensions. Plant J. 2018;95: 385–396. doi: 10.1111/tpj.13942 29681056

42. Oliver C, Santos JL, Pradillo M. Accurate chromosome segregation at first meiotic division requires AGO4, a protein involved in RNA-dependent DNA methylation in Arabidopsis thaliana. Genetics. 2016;204: 543–553. doi: 10.1534/genetics.116.189217 27466226

43. Smallwood SA, Lee HJ, Angermueller C, Krueger F, Saadeh H, Peat J, et al. Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat Methods. 2014;11: 817–820. doi: 10.1038/nmeth.3035 25042786

44. Hsieh PH, He S, Buttress T, Gao H, Couchman M, Fischer RL, et al. Arabidopsis male sexual lineage exhibits more robust maintenance of CG methylation than somatic tissues. Proc Natl Acad Sci U S A. 2016;113: 15132–15137. doi: 10.1073/pnas.1619074114 27956643

45. Park K, Kim MY, Vickers M, Park JS, Hyun Y, Okamoto T, et al. DNA demethylation is initiated in the central cells of Arabidopsis and rice. Proc Natl Acad Sci U S A. 2016;113: 15138–15143. doi: 10.1073/pnas.1619047114 27956642

46. Sanchez Moran E, Armstrong SJ, Santos JL, Franklin FC, Jones GH, Sanchez-Moran E, et al. Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res. 2001;9: 121–8. doi: 10.1023/a:1009278902994 11321367

47. Viera A, Santos JL, Parra MT, Calvente A, Gómez R, De La Fuente R, et al. Incomplete synapsis and chiasma localization: The chicken or the egg? Cytogenet Genome Res. 2010;128: 139–151. doi: 10.1159/000290637 20389032

48. Higgins JD, Osman K, Jones GH, Franklin FCH. Factors Underlying Restricted Crossover Localization in Barley Meiosis. Annu Rev Genet. 2014;48: 29–47. doi: 10.1146/annurev-genet-120213-092509 25089719

49. Tessé S, Bourbon HM, Debuchy R, Budin K, Dubois E, Liangran Z, et al. Asy2/Mer2: An evolutionarily conserved mediator of meiotic recombination, pairing, and global chromosome compaction. Genes Dev. 2017;31: 1880–1893. doi: 10.1101/gad.304543.117 29021238

50. Hua Z, Vierstra RD. The Cullin-RING Ubiquitin-Protein Ligases. Annu Rev Plant Biol. 2011;62: 299–334. doi: 10.1146/annurev-arplant-042809-112256 21370976

51. Fyodorov D V., Zhou B-R, Skoultchi AI, Bai Y. Emerging roles of linker histones in regulating chromatin structure and function. Nat Rev Mol Cell Biol. 2018;19: 192–206. doi: 10.1038/nrm.2017.94 29018282

52. Rutowicz K, Puzio M, Halibart-Puzio J, Lirski M, Kotliński M, Kroteń MA, et al. A Specialized Histone H1 Variant Is Required for Adaptive Responses to Complex Abiotic Stress and Related DNA Methylation in Arabidopsis. Plant Physiol. 2015;169: 2080–101. doi: 10.1104/pp.15.00493 26351307

53. Zemach A, Kim MY, Hsieh P-H, 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: 193–205. doi: 10.1016/j.cell.2013.02.033 23540698

54. Lyons DB, Zilberman D. DDM1 and Lsh remodelers allow methylation of DNA wrapped in nucleosomes. Elife. 2017;6: doi: 10.7554/elife.30674 29140247

55. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, et al. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics. 2003;163: 1109–22. 12663548

56. Chan SWL, Henderson IR, Zhang X, Shah G, Chien JSC, Jacobsen SE. RNAi, DRD1, and histone methylation actively target developmentally important Non-CG DNA methylation in Arabidopsis. PLoS Genet. 2006;2: 0791–0797. doi: 10.1371/journal.pgen.0020083 16741558

57. Herr AJ, Jensen MB, Dalmay T, Baulcombe DC. RNA Polymerase IV Directs Silencing of Endogenous DNA. Science (80-). 2005;308: 118–120. doi: 10.1126/science.1106910 15692015

58. Giraut L, Falque M, Drouaud J, Pereira L, Martin OC, Mezard C. Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet. 2011/11/11. 2011;7: e1002354. doi: 10.1371/journal.pgen.1002354 22072983

59. Fernandes JB, Seguéla-Arnaud M, Larchevêque C, Lloyd AH, Mercier R. Unleashing meiotic crossovers in hybrid plants. Proc Natl Acad Sci. 2017;115: 2431–2436. doi: 10.1073/pnas.1713078114 29183972

60. Lorieux M. MapDisto: Fast and efficient computation of genetic linkage maps. Mol Breed. 2012;30: 1231–1235. doi: 10.1007/s11032-012-9706-y

61. Vignard J, Siwiec T, Chelysheva L, Vrielynck N, Gonord F, Armstrong SJ, et al. The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet. 2007;3: 1894–1906. doi: 10.1371/journal.pgen.0030176 17937504

62. Richards EJ, Ausubel FM. Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell. 1988;53: 127–136. doi: 10.1016/0092-8674(88)90494-1 3349525

63. Chelysheva L, Vezon D, Belcram K, Gendrot G, Grelon M. The Arabidopsis BLAP75/Rmi1 homologue plays crucial roles in meiotic double-strand break repair. PLoS Genet. 2008/12/20. 2008;4: e1000309. doi: 10.1371/journal.pgen.1000309 19096505

64. Armstrong SJ, Caryl AP, Jones GH, Franklin FCH. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci. 2002;115: 3645–3655. doi: 10.1242/jcs.00048 12186950

65. Chelysheva L. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci. 2005;118: 4621–4632. doi: 10.1242/jcs.02583 16176934

66. Hansen KD, Langmead B, Irizarry RA. BSmooth: from whole genome bisulfite sequencing reads to differentially methylated regions. Genome Biol. 2012;13: R83. doi: 10.1186/gb-2012-13-10-r83 23034175

67. Wu H, Xu T, Feng H, Chen L, Li B, Yao B, et al. Detection of differentially methylated regions from whole-genome bisulfite sequencing data without replicates. Nucleic Acids Res. 2015;43: e141. doi: 10.1093/nar/gkv715 26184873

68. Corem S, Doron-Faigenboim A, Jouffroy O, Maumus F, Arazi T, Bouché N. Redistribution of CHH Methylation and Small Interfering RNAs across the Genome of Tomato ddm1 Mutants. Plant Cell. 2018;30: 1628–1644. doi: 10.1105/tpc.18.00167 29875274

69. Stroud H, Greenberg MVC, Feng S, Bernatavichute Y V., Jacobsen SE. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell. 2013; doi: 10.1016/j.cell.2012.10.054 23313553


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 6
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková, Ph.D.

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#