Common alleles of CMT2 and NRPE1 are major determinants of CHH methylation variation in Arabidopsis thaliana
Autoři:
Eriko Sasaki aff001; Taiji Kawakatsu aff002; Joseph R. Ecker aff002; Magnus Nordborg aff001
Působiště autorů:
Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Vienna Biocenter, Vienna, Austria
aff001; Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, California, United States of America
aff002; Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, California, United States of America
aff003; Institute of Agrobiological Sciences, National Agriculture and Food Research Organization. Tsukuba, Ibaraki, Japan
aff004; Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, California, United States of America
aff005
Vyšlo v časopise:
Common alleles of CMT2 and NRPE1 are major determinants of CHH methylation variation in Arabidopsis thaliana. PLoS Genet 15(12): e32767. doi:10.1371/journal.pgen.1008492
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008492
Souhrn
DNA cytosine methylation is an epigenetic mark associated with silencing of transposable elements (TEs) and heterochromatin formation. In plants, it occurs in three sequence contexts: CG, CHG, and CHH (where H is A, T, or C). The latter does not allow direct inheritance of methylation during DNA replication due to lack of symmetry, and methylation must therefore be re-established every cell generation. Genome-wide association studies (GWAS) have previously shown that CMT2 and NRPE1 are major determinants of genome-wide patterns of TE CHH methylation. Here we instead focus on CHH methylation of individual TEs and TE-families, allowing us to identify the pathways involved in CHH methylation simply from natural variation and confirm the associations by comparing them with mutant phenotypes. Methylation at TEs targeted by the RNA-directed DNA methylation (RdDM) pathway is unaffected by CMT2 variation, but is strongly affected by variation at NRPE1, which is largely responsible for the longitudinal cline in this phenotype. In contrast, CMT2-targeted TEs are affected by both loci, which jointly explain 7.3% of the phenotypic variation (13.2% of total genetic effects). There is no longitudinal pattern for this phenotype, however, because the geographic patterns appear to compensate for each other in a pattern suggestive of stabilizing selection.
Klíčová slova:
Alleles – DNA methylation – Genetic loci – Genome-wide association studies – Methylation – Phenotypes – Plant genomics – Longitude
Zdroje
1. Law JA, 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
2. Kawashima T, Berger F. Epigenetic reprogramming in plant sexual reproduction. Nat Rev Genet. 2014;15: 613–624. doi: 10.1038/nrg3685 25048170
3. 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
4. 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
5. 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: 64–72. doi: 10.1038/nsmb.2735 24336224
6. Wassenegger M, Heimes S, Riedel L, Sänger HL. RNA-directed de novo methylation of genomic sequences in plants. Cell. 1994;76: 567–576. doi: 10.1016/0092-8674(94)90119-8 8313476
7. Matzke MA, Mosher RA. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet. 2014;15: 394–408. doi: 10.1038/nrg3683 24805120
8. Schmitz RJ, Ecker JR. Epigenetic and epigenomic variation in Arabidopsis thaliana. Trends Plant Sci. 2012;17: 149–154. doi: 10.1016/j.tplants.2012.01.001 22342533
9. Weigel D, Colot V. Epialleles in plant evolution. Genome Biol. 2012;13: 249. doi: 10.1186/gb-2012-13-10-249 23058244
10. Shen X, De Jonge J, Forsberg SKG, Pettersson ME, Sheng Z, Hennig L, et al. Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLoS Genet. 2014;10: e1004842. doi: 10.1371/journal.pgen.1004842 25503602
11. Dubin MJ, Zhang P, Meng D, Remigereau M-S, Osborne EJ, Paolo Casale F, et al. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. Elife. 2015;4: e05255. doi: 10.7554/eLife.05255 25939354
12. Kawakatsu T, Huang S-SC, Jupe F, Sasaki E, Schmitz RJ, Urich MA, et al. Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions. Cell. 2016;166: 492–505. doi: 10.1016/j.cell.2016.06.044 27419873
13. Stroud H, Greenberg MVC, Feng S, Bernatavichute YV, Jacobsen SE. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell. 2013;152: 352–364. doi: 10.1016/j.cell.2012.10.054 23313553
14. Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, et al. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5’ terminal nucleotide. Cell. 2008;133: 116–127. doi: 10.1016/j.cell.2008.02.034 18342361
15. Harris CJ, Scheibe M, Wongpalee SP, Liu W, Cornett EM, Vaughan RM, et al. A DNA methylation reader complex that enhances gene transcription. Science. 2018;362: 1182–1186. doi: 10.1126/science.aar7854 30523112
16. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40: D1178–86. doi: 10.1093/nar/gkr944 22110026
17. Ogura T, Busch W. From phenotypes to causal sequences: using genome wide association studies to dissect the sequence basis for variation of plant development. Curr Opin Plant Biol. 2015;23: 98–108. doi: 10.1016/j.pbi.2014.11.008 25449733
18. Gallagher MD, Chen-Plotkin AS. The Post-GWAS Era: From Association to Function. Am J Hum Genet. 2018;102: 717–730. doi: 10.1016/j.ajhg.2018.04.002 29727686
19. Wendte JM, Haag JR, Singh J, McKinlay A, Pontes OM, Pikaard CS. Functional Dissection of the Pol V Largest Subunit CTD in RNA-Directed DNA Methylation. Cell Rep. 2017;19: 2796–2808. doi: 10.1016/j.celrep.2017.05.091 28658626
20. Morel J-B, Godon C, Mourrain P, Béclin C, Boutet S, Feuerbach F, et al. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell. 2002;14: 629–639. doi: 10.1105/tpc.010358 11910010
21. Zhong X, Hale CJ, Law JA, Johnson LM, Feng S, Tu A, et al. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat Struct Mol Biol. 2012;19: 870–875. doi: 10.1038/nsmb.2354 22864289
22. Pignatta D, Erdmann RM, Scheer E, Picard CL, Bell GW, Gehring M. Natural epigenetic polymorphisms lead to intraspecific variation in Arabidopsis gene imprinting. Elife. 2014;3: e03198. doi: 10.7554/eLife.03198 24994762
23. Zapata L, Ding J, Willing E-M, Hartwig B, Bezdan D, Jiao W-B, et al. Chromosome-level assembly of Arabidopsis thaliana Ler reveals the extent of translocation and inversion polymorphisms. Proc Natl Acad Sci U S A. 2016;113: E4052–60. doi: 10.1073/pnas.1607532113
24. Pucker B, Holtgräwe D, Stadermann KB, Frey K, Huettel B, Reinhardt R, et al. A Chromosome-level Sequence Assembly Reveals the Structure of the Arabidopsis thaliana Nd-1 Genome and its Gene Set. bioRxiv. 2018. p. 407627.
25. Atwell S, Huang YS, Vilhjálmsson BJ, Willems G, Horton M, Li Y, et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature. 2010;465: 627–631. doi: 10.1038/nature08800 20336072
26. Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M, Epple P, et al. Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature. 2010;465: 632–636. doi: 10.1038/nature09083 20520716
27. 1001 Genomes Consortium. 1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana. Cell. 2016;166: 481–491. doi: 10.1016/j.cell.2016.05.063 27293186
28. Berardini TZ, Reiser L, Li D, Mezheritsky Y, Muller R, Strait E, et al. The Arabidopsis information resource: making and mining the “gold standard” annotated reference plant genome. Genesis. 2015;53: 474–485. doi: 10.1002/dvg.22877 26201819
29. Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet. 2006;38: 203–208. doi: 10.1038/ng1702 16380716
30. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, Daly MJ, et al. Efficient control of population structure in model organism association mapping. Genetics. 2008;178: 1709–1723. doi: 10.1534/genetics.107.080101 18385116
31. Lippert C, Casale FP, Rakitsch B, Stegle O. LIMIX: genetic analysis of multiple traits. bioRxiv. 2014. Available: https://edoc.mdc-berlin.de/16584/.
32. Evangelou E, Ioannidis JPA. Meta-analysis methods for genome-wide association studies and beyond. Nat Rev Genet. 2013;14: 379–389. doi: 10.1038/nrg3472 23657481
33. Lewontin RC. The interaction of selection and linkage. I. General considerations; heterotic models. Genetics. 1964. Available: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1210557/.
Štítky
Genetika Reprodukční medicínaČlánek vyšel v časopise
PLOS Genetics
2019 Číslo 12
Nejčtenější v tomto čísle
- Aspergillus fumigatus calcium-responsive transcription factors regulate cell wall architecture promoting stress tolerance, virulence and caspofungin resistance
- Architecture of the Escherichia coli nucleoid
- Common gardens in teosintes reveal the establishment of a syndrome of adaptation to altitude
- Restricted and non-essential redundancy of RNAi and piRNA pathways in mouse oocytes