Regulatory Mechanism of a Heat-activated Retrotransposon by DDR Complex in

Overview

Journal Front Plant Sci

Date 2023 Jan 9

PMID 36618621

Authors

Xiaoying Niu

Lu Chen

Atsushi Kato

Hidetaka Ito

Affiliations

Soon will be listed here.

Abstract

The RNA-directed DNA methylation (RdDM) pathway plays an essential role in the transposon silencing mechanism; the DDR complex, consisting of DRD1, DMS3, and RDM1, is an essential component of the RdDM pathway. , identified in , is a retrotransposon activated by heat stress at 37°C; however, studies on the regulation of are limited. In this study, we analyzed the regulation of activity by the DDR complex in . We elucidated that loss of any component of the DDR complex increased transcript levels. Transgenerational transposition of was observed in the DDR-complex mutants treated with heat stress for 48 h. Furthermore, the DDR complex components DRD1, DMS3, and RDM1 played independent roles in suppressing transcription and transposition. Moreover, we found that the duration of heat stress affects activity. Therefore, the results of this study provide new insights into the retrotransposon regulatory mechanisms of the DDR complex in the RdDM pathway.

Citing Articles

PTGS is dispensable for the initiation of epigenetic silencing of an active transposon in Arabidopsis.

Trasser M, Bohl-Viallefond G, Barragan-Borrero V, Diezma-Navas L, Loncsek L, Nordborg M EMBO Rep. 2024; 25(12):5780-5809.

PMID: 39511423 PMC: 11624286. DOI: 10.1038/s44319-024-00304-5.

Regulatory mechanism of heat-active retrotransposons by the SET domain protein SUVH2.

Niu X, Ge Z, Ito H Front Plant Sci. 2024; 15:1355626.

PMID: 38390294 PMC: 10883384. DOI: 10.3389/fpls.2024.1355626.

References

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

Zhong X, Hale C, Law J, Johnson L, Feng S, Tu A . DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat Struct Mol Biol. 2012; 19(9):870-5. PMC: 3443314. DOI: 10.1038/nsmb.2354. View

Wessler S . Transposable elements and the evolution of eukaryotic genomes. Proc Natl Acad Sci U S A. 2006; 103(47):17600-1. PMC: 1693792. DOI: 10.1073/pnas.0607612103. 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

Takehira K, Hayashi Y, Nozawa K, Chen L, Suzuki T, Masuta Y . DRD1, a SWI/SNF-like chromatin remodeling protein, regulates a heat-activated transposon in Arabidopsis thaliana. Genes Genet Syst. 2021; 96(3):151-158. DOI: 10.1266/ggs.21-00005. View

Wongpalee S, Liu S, Gallego-Bartolome J, Leitner A, Aebersold R, Liu W . CryoEM structures of Arabidopsis DDR complexes involved in RNA-directed DNA methylation. Nat Commun. 2019; 10(1):3916. PMC: 6718625. DOI: 10.1038/s41467-019-11759-9. View

Ito H . Environmental stress and transposons in plants. Genes Genet Syst. 2022; 97(4):169-175. DOI: 10.1266/ggs.22-00045. View

Sasaki T, Lorkovic Z, Liang S, Matzke A, Matzke M . The ability to form homodimers is essential for RDM1 to function in RNA-directed DNA methylation. PLoS One. 2014; 9(2):e88190. PMC: 3912163. DOI: 10.1371/journal.pone.0088190. View

Kanno T, Aufsatz W, Jaligot E, Mette M, Matzke M, Matzke A . A SNF2-like protein facilitates dynamic control of DNA methylation. EMBO Rep. 2005; 6(7):649-55. PMC: 1369108. DOI: 10.1038/sj.embor.7400446. View

10.

Hayashi Y, Takehira K, Nozawa K, Suzuki T, Masuta Y, Kato A . ONSEN shows different transposition activities in RdDM pathway mutants. Genes Genet Syst. 2020; 95(4):183-190. DOI: 10.1266/ggs.20-00019. View

11.

Matsunaga W, Ohama N, Tanabe N, Masuta Y, Masuda S, Mitani N . A small RNA mediated regulation of a stress-activated retrotransposon and the tissue specific transposition during the reproductive period in Arabidopsis. Front Plant Sci. 2015; 6:48. PMC: 4321352. DOI: 10.3389/fpls.2015.00048. View

12.

Le Q, Wright S, Yu Z, Bureau T . Transposon diversity in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2000; 97(13):7376-81. PMC: 16553. DOI: 10.1073/pnas.97.13.7376. View

13.

Zhang M, Kimatu J, Xu K, Liu B . DNA cytosine methylation in plant development. J Genet Genomics. 2010; 37(1):1-12. DOI: 10.1016/S1673-8527(09)60020-5. View

14.

Haag J, Pikaard C . Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat Rev Mol Cell Biol. 2011; 12(8):483-92. DOI: 10.1038/nrm3152. View

15.

Matzke M, Mosher R . RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet. 2014; 15(6):394-408. DOI: 10.1038/nrg3683. View

16.

Matzke M, Kanno T, Daxinger L, Huettel B, Matzke A . RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol. 2009; 21(3):367-76. DOI: 10.1016/j.ceb.2009.01.025. View

17.

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

18.

Zilberman D, Gehring M, Tran R, Ballinger T, Henikoff S . Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet. 2006; 39(1):61-9. DOI: 10.1038/ng1929. View

19.

Kanno T, Bucher E, Daxinger L, Huettel B, Bohmdorfer G, Gregor W . A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet. 2008; 40(5):670-5. DOI: 10.1038/ng.119. View

20.

Xue Y, Zhong Z, Harris C, Gallego-Bartolome J, Wang M, Picard C . Arabidopsis MORC proteins function in the efficient establishment of RNA directed DNA methylation. Nat Commun. 2021; 12(1):4292. PMC: 8277788. DOI: 10.1038/s41467-021-24553-3. View