Epigenetic Regulation of Ecotype-specific Expression of the Heat-activated Transposon

Overview

Journal Front Plant Sci

Date 2022 Aug 4

PMID 35923888

Authors

Kosuke Nozawa

Seiji Masuda

Hidetoshi Saze

Yoko Ikeda

Takamasa Suzuki

Hiroki Takagi

Keisuke Tanaka

Naohiko Ohama

Xiaoying Niu

Atsushi Kato

Hidetaka Ito

Affiliations

Soon will be listed here.

Abstract

Transposable elements are present in a wide variety of organisms; however, our understanding of the diversity of mechanisms involved in their activation is incomplete. In this study, we analyzed the transcriptional activation of the retrotransposon, which is activated by high-temperature stress in . We found that its transcription is significantly higher in the Japanese ecotype Kyoto. Considering that transposons are epigenetically regulated, DNA methylation levels were analyzed, revealing that CHH methylation was reduced in Kyoto compared to the standard ecotype, Col-0. A mutation was also detected in the Kyoto gene, encoding a CHH methyltransferase, suggesting that it may be responsible for increased expression of . CHH methylation is controlled by histone modifications through a self-reinforcing loop between DNA methyltransferase and histone methyltransferase. Analysis of these modifications revealed that the level of H3K9me2, a repressive histone marker for gene expression, was lower in Kyoto than in Col-0. The level of another repressive histone marker, H3K27me1, was decreased in Kyoto; however, it was not impacted in a Col-0 mutant. Therefore, in addition to the mutation, other factors may reduce repressive histone modifications in Kyoto.

Citing Articles

Natural Diversity of Heat-Induced Transcription of Retrotransposons in Arabidopsis thaliana.

Xu W, Thieme M, Roulin A Genome Biol Evol. 2024; 16(11).

PMID: 39523776 PMC: 11580521. DOI: 10.1093/gbe/evae242.

Substrate specificity and protein stability drive the divergence of plant-specific DNA methyltransferases.

Jiang J, Gwee J, Fang J, Leichter S, Sanders D, Ji X Sci Adv. 2024; 10(45):eadr2222.

PMID: 39504374 PMC: 11540031. DOI: 10.1126/sciadv.adr2222.

Barley AGO4 proteins show overlapping functionality with distinct small RNA-binding properties in heterologous complementation.

Miloro F, Kis A, Havelda Z, Dalmadi A Plant Cell Rep. 2024; 43(4):96.

PMID: 38480545 PMC: 10937801. DOI: 10.1007/s00299-024-03177-z.

Plant environmental memory: implications, mechanisms and opportunities for plant scientists and beyond.

Auge G, Hankofer V, Groth M, Antoniou-Kourounioti R, Ratikainen I, Lampei C AoB Plants. 2023; 15(4):plad032.

PMID: 37415723 PMC: 10321398. DOI: 10.1093/aobpla/plad032.

Long-read direct RNA sequencing reveals epigenetic regulation of chimeric gene-transposon transcripts in Arabidopsis thaliana.

Berthelier J, Furci L, Asai S, Sadykova M, Shimazaki T, Shirasu K Nat Commun. 2023; 14(1):3248.

PMID: 37277361 PMC: 10241880. DOI: 10.1038/s41467-023-38954-z.

References

. 1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana. Cell. 2016; 166(2):481-491. PMC: 4949382. DOI: 10.1016/j.cell.2016.05.063. View

Quadrana L, Silveira A, Mayhew G, LeBlanc C, Martienssen R, Jeddeloh J . The Arabidopsis thaliana mobilome and its impact at the species level. Elife. 2016; 5. PMC: 4917339. DOI: 10.7554/eLife.15716. View

Shen X, de Jonge J, Forsberg S, Pettersson M, Sheng Z, Hennig L . Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLoS Genet. 2014; 10(12):e1004842. PMC: 4263395. DOI: 10.1371/journal.pgen.1004842. View

Du J, Zhong X, Bernatavichute Y, Stroud H, Feng S, Caro E . Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell. 2012; 151(1):167-80. PMC: 3471781. DOI: 10.1016/j.cell.2012.07.034. View

Cavrak V, Lettner N, Jamge S, Kosarewicz A, Bayer L, Mittelsten Scheid O . How a retrotransposon exploits the plant's heat stress response for its activation. PLoS Genet. 2014; 10(1):e1004115. PMC: 3907296. DOI: 10.1371/journal.pgen.1004115. View

Nozawa K, Chen J, Jiang J, Leichter S, Yamada M, Suzuki T . DNA methyltransferase CHROMOMETHYLASE3 prevents ONSEN transposon silencing under heat stress. PLoS Genet. 2021; 17(8):e1009710. PMC: 8376061. DOI: 10.1371/journal.pgen.1009710. View

Liu S, de Jonge J, Trejo-Arellano M, Santos-Gonzalez J, Kohler C, Hennig L . Role of H1 and DNA methylation in selective regulation of transposable elements during heat stress. New Phytol. 2020; 229(4):2238-2250. PMC: 7894476. DOI: 10.1111/nph.17018. View

Fultz D, Choudury S, Slotkin R . Silencing of active transposable elements in plants. Curr Opin Plant Biol. 2015; 27:67-76. DOI: 10.1016/j.pbi.2015.05.027. View

Cao X, Jacobsen S . Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol. 2002; 12(13):1138-44. DOI: 10.1016/s0960-9822(02)00925-9. View

10.

Krueger F, Andrews S . Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011; 27(11):1571-2. PMC: 3102221. DOI: 10.1093/bioinformatics/btr167. View

11.

Ito H, Yoshida T, Tsukahara S, Kawabe A . Evolution of the ONSEN retrotransposon family activated upon heat stress in Brassicaceae. Gene. 2013; 518(2):256-61. DOI: 10.1016/j.gene.2013.01.034. View

12.

Bucher E, Reinders J, Mirouze M . Epigenetic control of transposon transcription and mobility in Arabidopsis. Curr Opin Plant Biol. 2012; 15(5):503-10. DOI: 10.1016/j.pbi.2012.08.006. View

13.

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; 472(7341):115-9. DOI: 10.1038/nature09861. View

14.

Lisch D . Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol. 2008; 60:43-66. DOI: 10.1146/annurev.arplant.59.032607.092744. View

15.

Bolger A, Lohse M, Usadel B . Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30(15):2114-20. PMC: 4103590. DOI: 10.1093/bioinformatics/btu170. View

16.

Matzke M, Birchler J . RNAi-mediated pathways in the nucleus. Nat Rev Genet. 2005; 6(1):24-35. DOI: 10.1038/nrg1500. View

17.

Masuda S, Nozawa K, Matsunaga W, Masuta Y, Kawabe A, Kato A . Characterization of a heat-activated retrotransposon in natural accessions of Arabidopsis thaliana. Genes Genet Syst. 2016; 91(6):293-299. DOI: 10.1266/ggs.16-00045. View

18.

Zemach A, Kim M, Hsieh P, Coleman-Derr D, Eshed-Williams L, Thao K . The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell. 2013; 153(1):193-205. PMC: 4035305. DOI: 10.1016/j.cell.2013.02.033. View

19.

Miura F, Enomoto Y, Dairiki R, Ito T . Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Res. 2012; 40(17):e136. PMC: 3458524. DOI: 10.1093/nar/gks454. View

20.

Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L . Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol. 2013; 21(1):64-72. PMC: 4103798. DOI: 10.1038/nsmb.2735. View