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Canalization of genome-wide transcriptional activity in Arabidopsis thaliana accessions by MET1-dependent CG methylation

View ORCID ProfileThanvi Srikant, View ORCID ProfileWei Yuan, View ORCID ProfileKenneth Wayne Berendzen, View ORCID ProfileAdrián Contreras Garrido, View ORCID ProfileHajk-Georg Drost, View ORCID ProfileRebecca Schwab, View ORCID ProfileDetlef Weigel
doi: https://doi.org/10.1101/2022.07.14.500095
Thanvi Srikant
1Department of Molecular Biology, Max Planck Institute for Biology Tübingen, Tübingen, Germany
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Wei Yuan
1Department of Molecular Biology, Max Planck Institute for Biology Tübingen, Tübingen, Germany
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Kenneth Wayne Berendzen
2Plant Transformation and Flow Cytometry Facility, ZMBP, University of Tübingen, Tübingen, Germany
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Adrián Contreras Garrido
1Department of Molecular Biology, Max Planck Institute for Biology Tübingen, Tübingen, Germany
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Hajk-Georg Drost
3Computational Biology Group, Max Planck Institute for Biology Tübingen, Tübingen, Germany
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Rebecca Schwab
1Department of Molecular Biology, Max Planck Institute for Biology Tübingen, Tübingen, Germany
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Detlef Weigel
1Department of Molecular Biology, Max Planck Institute for Biology Tübingen, Tübingen, Germany
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  • For correspondence: weigel@weigelworld.org
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ABSTRACT

BACKGROUND Eukaryotes employ epigenetic marks such as DNA methylation at cytosines both for gene regulation and genome defense. In Arabidopsis thaliana, a central role is played by methylation in the CG context, with profound effects on gene expression and transposable element (TE) silencing. Nevertheless, despite its conserved role, genome-wide CG methylation differs substantially between wild A. thaliana accessions.

RESULTS We hypothesized that global reduction of CG methylation would reduce epigenomic, transcriptomic and phenotypic diversity in A. thaliana accessions. To test our hypothesis, we knocked out MET1, which is required for CG methylation, in 18 early-flowering A. thaliana accessions. Homozygous met1 mutants in all accessions suffered from a range of common developmental defects such as dwarfism and delayed flowering, in addition to accession-specific abnormalities in rosette leaf architecture, silique morphology and fertility. Integrated analysis of genome-wide methylation, chromatin accessibility and transcriptomes confirmed that inactivation of MET1 greatly reduces CG methylation and alters chromatin accessibility at thousands of loci. While the effects on TE activation were similarly drastic in all accessions, the quantitative effects on non-TE genes varied greatly. The expression profiles of accessions became considerably more divergent from each other after genome-wide removal of CG methylation, although the expression of genes with diverse expression profiles across wild-type accessions tended to become more similar in mutants.

CONCLUSIONS Our systematic analysis of MET1 requirement for genome function in different A. thaliana accessions revealed a dual role for CG methylation: for many genes, CG methylation appears to canalize expression levels, with methylation masking regulatory divergence. However, for a smaller subset of genes, CG methylation increases expression diversity beyond genetically encoded differences.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted July 14, 2022.
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Canalization of genome-wide transcriptional activity in Arabidopsis thaliana accessions by MET1-dependent CG methylation
Thanvi Srikant, Wei Yuan, Kenneth Wayne Berendzen, Adrián Contreras Garrido, Hajk-Georg Drost, Rebecca Schwab, Detlef Weigel
bioRxiv 2022.07.14.500095; doi: https://doi.org/10.1101/2022.07.14.500095
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Canalization of genome-wide transcriptional activity in Arabidopsis thaliana accessions by MET1-dependent CG methylation
Thanvi Srikant, Wei Yuan, Kenneth Wayne Berendzen, Adrián Contreras Garrido, Hajk-Georg Drost, Rebecca Schwab, Detlef Weigel
bioRxiv 2022.07.14.500095; doi: https://doi.org/10.1101/2022.07.14.500095

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