Monitoring the interplay between transposable element families and DNA methylation in maize

English version

Autoři: Jaclyn M. Noshay ^aff001; Sarah N. Anderson ^aff001; Peng Zhou ^aff001; Lexiang Ji ^aff002; William Ricci ^aff003; Zefu Lu ^aff004; Michelle C. Stitzer ^aff005; Peter A. Crisp ^aff001; Candice N. Hirsch ^aff006; Xiaoyu Zhang ^aff003; Robert J. Schmitz ^aff004; Nathan M. Springer ^aff001
Působiště autorů: Department of Plant and Microbial Biology, University of Minnesota, St. Paul MN, United States of America ^aff001; Institute of Bioinformatics, University of Georgia, Athens GA, United States of America ^aff002; Department of Plant Biology, University of Georgia, Athens GA, United States of America ^aff003; Department of Genetics, University of Georgia, Athens GA, United States of America ^aff004; Department of Plant Sciences, University of California Davis, Davis CA, United States of America ^aff005; Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul MN, United States of America ^aff006
Vyšlo v časopise: Monitoring the interplay between transposable element families and DNA methylation in maize. PLoS Genet 15(9): e32767. doi:10.1371/journal.pgen.1008291
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1008291

Souhrn

DNA methylation and epigenetic silencing play important roles in the regulation of transposable elements (TEs) in many eukaryotic genomes. A majority of the maize genome is derived from TEs that can be classified into different orders and families based on their mechanism of transposition and sequence similarity, respectively. TEs themselves are highly methylated and it can be tempting to view them as a single uniform group. However, the analysis of DNA methylation profiles in flanking regions provides evidence for distinct groups of chromatin properties at different TE families. These differences among TE families are reproducible in different tissues and different inbred lines. TE families with varying levels of DNA methylation in flanking regions also show distinct patterns of chromatin accessibility and modifications within the TEs. The differences in the patterns of DNA methylation flanking TE families arise from a combination of non-random insertion preferences of TE families, changes in DNA methylation triggered by the insertion of the TE and subsequent selection pressure. A set of nearly 70,000 TE polymorphisms among four assembled maize genomes were used to monitor the level of DNA methylation at haplotypes with and without the TE insertions. In many cases, TE families with high levels of DNA methylation in flanking sequence are enriched for insertions into highly methylated regions. The majority of the >2,500 TE insertions into unmethylated regions result in changes in DNA methylation in haplotypes with the TE, suggesting the widespread potential for TE insertions to condition altered methylation in conserved regions of the genome. This study highlights the interplay between TEs and the methylome of a major crop species.

Klíčová slova:

DNA – Biology and life sciences – Cell biology – Chromosome biology – Chromatin – Chromatin modification – DNA methylation – Genetics – Epigenetics – DNA modification – Gene expression – Genomics – Plant genomics – Mobile genetic elements – Transposable elements – Genome analysis – Genome annotation – Plant genetics – Genetic elements – Heredity – Genetic mapping – Haplotypes – Biochemistry – Nucleic acids – Bioengineering – Biotechnology – Plant biotechnology – Plant science – Organisms – Eukaryota – Plants – Grasses – Maize – Computational biology – Physical sciences – Chemistry – Chemical reactions – Methylation – Engineering and technology – Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Plant and algal models

Zdroje

1. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nature reviewsGenetics. 2007;8: 973–982.

2. Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, et al. Improved maize reference genome with single-molecule technologies. Nature. 2017;546: 524–527. doi: 10.1038/nature22971 28605751

3. Stitzer MC, Anderson SN, Springer NM, Ross-Ibarra J. The Genomic Ecosystem of Transposable Elements in Maize [Internet]. doi: 10.1101/559922

4. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: complexity, diversity, and dynamics. Science. Center for Plant Genomics, Iowa State University, Ames, IA 50011, USA.; 2009;326: 1112–1115. doi: 10.1126/science.1178534 19965430

5. Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A, Deragon JM, et al. Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet. 2009;5: e1000732. doi: 10.1371/journal.pgen.1000732 19936065

6. The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408: 796–815. doi: 10.1038/35048692 11130711

7. Zhang H, Lang Z, Zhu J-K. 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

8. Ito H, Kakutani T. Control of transposable elements in Arabidopsis thaliana. Chromosome Res. 2014;22: 217–223. doi: 10.1007/s10577-014-9417-9 24801341

9. Kim MY, Zilberman D. DNA methylation as a system of plant genomic immunity. Trends Plant Sci. 2014;19: 320–326. doi: 10.1016/j.tplants.2014.01.014 24618094

10. Martienssen RA, Colot V. DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science. 2001;293: 1070–1074. doi: 10.1126/science.293.5532.1070 11498574

11. Yoder JA, Walsh CP, Bestor TH. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 1997;13: 335–340. 9260521

12. West PT, Li Q, Ji L, Eichten SR, Song J, Vaughn MW, et al. Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS One. 2014;9: e105267. doi: 10.1371/journal.pone.0105267 25122127

13. Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Kim KD, Page JT, et al. Widespread natural variation of DNA methylation within angiosperms. Genome Biol. 2016;http://dx.doi.org/10.1101/045880:194.

14. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature. 2008;452: 215–219. doi: 10.1038/nature06745 18278030

15. Noshay JM, Crisp PA, Springer NM. The Maize Methylome. In: Bennetzen J, Flint-Garcia S, Hirsch C, Tuberosa R, editors. The Maize Genome. Cham: Springer International Publishing; 2018. pp. 81–96.

16. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature reviewsGenetics. 2010;11: 204–220.

17. Regulski M, Lu Z, Kendall J, Donoghue MT, Reinders J, Llaca V, et al. The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res. 2013;23: 1651–1662. doi: 10.1101/gr.153510.112 23739895

18. Gent JI, Ellis NA, Guo L, Harkess AE, Yao Y, Zhang X, et al. CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res. 2013;23: 628–637. doi: 10.1101/gr.146985.112 23269663

19. Li Q, Gent JI, Zynda G, Song J, Makarevitch I, Hirsch CD, et al. RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome. Proc Natl Acad Sci U S A. 2015;112: 14728–14733. doi: 10.1073/pnas.1514680112 26553984

20. Sultana T, Zamborlini A, Cristofari G, Lesage P. Integration site selection by retroviruses and transposable elements in eukaryotes. Nat Rev Genet. 2017;18: 292–308. doi: 10.1038/nrg.2017.7 28286338

21. Springer NM, Anderson SN, Andorf CM, Ahern KR, Bai F, Barad O, et al. The maize W22 genome provides a foundation for functional genomics and transposon biology. Nat Genet. 2018; doi: 10.1038/s41588-018-0158-0 30061736

22. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL. The paleontology of intergene retrotransposons of maize. Nat Genet. 1998;20: 43–45. doi: 10.1038/1695 9731528

23. Hollister JD, Gaut BS. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 2009;19: 1419–1428. doi: 10.1101/gr.091678.109 19478138

24. Eichten SR, Ellis NA, Makarevitch I, Yeh CT, Gent JI, Guo L, et al. Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet. 2012;8: e1003127. doi: 10.1371/journal.pgen.1003127 23271981

25. Quadrana L, Bortolini Silveira A, Mayhew GF, LeBlanc C, Martienssen RA, Jeddeloh JA, et al. The Arabidopsis thaliana mobilome and its impact at the species level. Elife. 2016;5. doi: 10.7554/eLife.15716 27258693

26. Choi JY, Purugganan MD. Evolutionary Epigenomics of Retrotransposon-Mediated Methylation Spreading in Rice. Mol Biol Evol. 2018;35: 365–382. doi: 10.1093/molbev/msx284 29126199

27. Richards EJ. Inherited epigenetic variation—revisiting soft inheritance. NatRevGenet. 2006;7: 395–401.

28. Springer NM, Schmitz RJ. Exploiting induced and natural epigenetic variation for crop improvement. Nat Rev Genet. 2017; doi: 10.1038/nrg.2017.45 28669983

29. Anderson SN, Stitzer MC, Brohammer AB, Zhou P, Noshay JM, Hirsch CD, et al. Transposable elements contribute to dynamic genome content in maize [Internet]. doi: 10.1101/547398

30. Oka R, Zicola J, Weber B, Anderson SN, Hodgman C, Gent JI, et al. Genome-wide mapping of transcriptional enhancer candidates using DNA and chromatin features in maize. Genome Biol. 2017;18: 137. doi: 10.1186/s13059-017-1273-4 28732548

31. Zhao H, Zhang W, Chen L, Wang L, Marand AP, Wu Y, et al. Proliferation of Regulatory DNA Elements Derived from Transposable Elements in the Maize Genome. Plant Physiol. 2018;176: 2789–2803. doi: 10.1104/pp.17.01467 29463772

32. Anderson SN, Zynda G, Song J, Han Z, Vaughn M, Li Q, et al. Subtle Perturbations of the Maize Methylome Reveal Genes and Transposons Silenced by Chromomethylase or RNA-Directed DNA Methylation Pathways. G3. 2018; doi: 10.1534/g3.118.200284 29618467

33. Walley JW, Sartor RC, Shen Z, Schmitz RJ, Ecker JR, Briggs SP. Integration of omic networks in a developmental atlas of maize. Science. 2016;353: 814–818. doi: 10.1126/science.aag1125 27540173

34. Yuan Y, SanMiguel PJ, Bennetzen JL. Methylation-spanning linker libraries link gene-rich regions and identify epigenetic boundaries in Zea mays. Genome Res. 2002;12: 1345–1349. doi: 10.1101/gr.185902 12213771

35. Rabinowicz PD, Schutz K, Dedhia N, Yordan C, Parnell LD, Stein L, et al. Differential methylation of genes and retrotransposons facilitates shotgun sequencing of the maize genome. Nat Genet. 1999;23: 305–308. doi: 10.1038/15479 10545948

36. Cuerda-Gil D, Slotkin RK. Non-canonical RNA-directed DNA methylation. Nature plants. 2016;2: 16163. doi: 10.1038/nplants.2016.163 27808230

37. Bond DM, Baulcombe DC. Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2015;112: 917–922. doi: 10.1073/pnas.1413053112 25561534

38. Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nature reviewsGenetics. 2007;8: 272–285.

39. Panda K, Ji L, Neumann DA, Daron J, Schmitz RJ, Slotkin RK. Full-length autonomous transposable elements are preferentially targeted by expression-dependent forms of RNA-directed DNA methylation. Genome Biol. 2016;17: 170–016–1032–y.

40. Bennetzen JL, Wang H. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol. 2014;65: 505–530. doi: 10.1146/annurev-arplant-050213-035811 24579996

41. Vollbrecht E, Duvick J, Schares JP, Ahern KR, Deewatthanawong P, Xu L, et al. Genome-wide distribution of transposed Dissociation elements in maize. Plant Cell. 2010;22: 1667–1685. doi: 10.1105/tpc.109.073452 20581308

42. McCarty DR, Latshaw S, Wu S, Suzuki M, Hunter CT, Avigne WT, et al. Mu-seq: sequence-based mapping and identification of transposon induced mutations. PLoS One. 2013;8: e77172. doi: 10.1371/journal.pone.0077172 24194867

43. Piffanelli P, Droc G, Mieulet D, Lanau N, Bès M, Bourgeois E, et al. Large-scale characterization of Tos17 insertion sites in a rice T-DNA mutant library. Plant Mol Biol. 2007;65: 587–601. doi: 10.1007/s11103-007-9222-3 17874225

44. Tsukahara S, Kawabe A, Kobayashi A, Ito T, Aizu T, Shin-i T, et al. Centromere-targeted de novo integrations of an LTR retrotransposon of Arabidopsis lyrata. Genes Dev. 2012;26: 705–713. doi: 10.1101/gad.183871.111 22431508

45. Graaf A van der, Wardenaar R, Neumann DA, Taudt A, Shaw RG, Jansen RC, et al. Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. Proc Natl Acad Sci U S A. 2015;112: 6676–6681. doi: 10.1073/pnas.1424254112 25964364

46. Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science. 2011;334: 369–373. doi: 10.1126/science.1212959 21921155

47. Becker C, Hagmann J, Muller J, Koenig D, Stegle O, Borgwardt K, et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature. 2011;480: 245–249. doi: 10.1038/nature10555 22057020

48. Hofmeister BT, Lee K, Rohr NA, Hall DW, Schmitz RJ. Stable inheritance of DNA methylation allows creation of epigenotype maps and the study of epiallele inheritance patterns in the absence of genetic variation. Genome Biol. Genome Biology; 2017;18: 1–16. doi: 10.1186/s13059-016-1139-1

49. Stuart T, Eichten SR, Cahn J, Karpievitch YV, Borevitz JO, Lister R. Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation. Elife. 2016;5: doi: 10.7554/eLife.20777 27911260

50. Li Q, Eichten SR, Hermanson PJ, Zaunbrecher VM, Song J, Wendt J, et al. Genetic perturbation of the maize methylome. Plant Cell. 2014;26: 4602–4616. doi: 10.1105/tpc.114.133140 25527708

51. Jackson JP, Lindroth AM, Cao X, Jacobsen SE. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature. 2002;416: 556–560. doi: 10.1038/nature731 11898023

52. Du J, Zhong X, Bernatavichute YV, Stroud H, Feng S, Caro E, et al. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell. 2012;151: 167–180. doi: 10.1016/j.cell.2012.07.034 23021223

53. Lisch D. How important are transposons for plant evolution? Nat Rev Genet. 2013;14: 49–61. doi: 10.1038/nrg3374 23247435

54. Lisch D, Bennetzen JL. Transposable element origins of epigenetic gene regulation. Curr Opin Plant Biol. 2011;14: 156–161. doi: 10.1016/j.pbi.2011.01.003 21444239

55. Eichten SR, Schmitz RJ, Springer NM. Epigenetics: Beyond Chromatin Modifications and Complex Genetic Regulation. Plant Physiol. 2014;165: 933–947. doi: 10.1104/pp.113.234211 24872382

56. Eichten SR, Briskine R, Song J, Li Q, Swanson-Wagner R, Hermanson PJ, et al. Epigenetic and genetic influences on DNA methylation variation in maize populations. Plant Cell. 2013;25: 2783–2797. doi: 10.1105/tpc.113.114793 23922207

57. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet. 1999;23: 314–318. doi: 10.1038/15490 10545949

58. Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, et al. A transposon-induced epigenetic change leads to sex determination in melon. Nature. 2009;461: 1135–1138. doi: 10.1038/nature08498 19847267

59. Wittmeyer K, Cui J, Chatterjee D, Lee T-F, Tan Q, Xue W, et al. The Dominant and Poorly Penetrant Phenotypes of Maize Unstable factor for orange1 Are Caused by DNA Methylation Changes at a Linked Transposon. Plant Cell. 2018;30: 3006–3023. doi: 10.1105/tpc.18.00546 30563848

60. Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Campbell MS, et al. The complex sequence landscape of maize revealed by single molecule technologies. 2016; 1–19.

61. Sun S, Zhou Y, Chen J, Shi J, Zhao H, Zhao H, et al. Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes. Nat Genet. 2018;50: 1289–1295. doi: 10.1038/s41588-018-0182-0 30061735

62. Hirsch C, Hirsch CD, Brohammer AB, Bowman MJ, Soifer I, Barad O, et al. Draft Assembly of Elite Inbred Line PH207 Provides Insights into Genomic and Transcriptome Diversity in Maize. Plant Cell. 2016; tpc.00353.2016.

63. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011;17: 10–12.

64. Xi Y, Li W. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics. 2009;10: 232. doi: 10.1186/1471-2105-10-232 19635165

65. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, CB10 1SA, UK, Broad Institute of MIT and Harvard, Cambridge, MA 02141, USA.; 2009;25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

66. Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, et al. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 2007;5: e129. doi: 10.1371/journal.pbio.0050129 17439305

67. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404

68. Langmead B. Aligning short sequencing reads with Bowtie. Curr Protoc Bioinformatics. 2010;Chapter 11: Unit 11.7.