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Predictable and stable epimutations induced during clonal plant propagation with embryonic transcription factor

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Wibowo, Anjar Tri, Antunez-Sanchez, Javier, Dawson, Alexander, Price, Jonathan Lewis, Meehan, Cathal, Wrightsman, Travis, Collenberg, Maximillian, Bezrukov, Ilja, Becker, Claude, Benhamed, Moussa, Weigel, Detlef and Gutierrez-Marcos, José F. (2022) Predictable and stable epimutations induced during clonal plant propagation with embryonic transcription factor. PLOS Genetics, 18 (11). e1010479. doi:10.1371/journal.pgen.1010479 ISSN 1553-7404.

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Official URL: https://doi.org/10.1371/journal.pgen.1010479

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Abstract

Clonal propagation is frequently used in commercial plant breeding and biotechnology programs because it minimizes genetic variation, yet it is not uncommon to observe clonal plants with stable phenotypic changes, a phenomenon known as somaclonal variation. Several studies have linked epigenetic modifications induced during regeneration with this newly acquired phenotypic variation. However, the factors that determine the extent of somaclonal variation and the molecular changes underpinning this process remain poorly understood. To address this gap in our knowledge, we compared clonally propagated Arabidopsis thaliana plants derived from somatic embryogenesis using two different embryonic transcription factors- RWP-RK DOMAIN-CONTAINING 4 (RKD4) or LEAFY COTYLEDON2 (LEC2) and from two epigenetically distinct founder tissues. We found that both the epi(genetic) status of the explant and the regeneration protocol employed play critical roles in shaping the molecular and phenotypic landscape of clonal plants. Phenotypic variation in regenerated plants can be largely explained by the inheritance of tissue-specific DNA methylation imprints, which are associated with specific transcriptional and metabolic changes in sexual progeny of clonal plants. For instance, regenerants were particularly affected by the inheritance of root-specific epigenetic imprints, which were associated with an increased accumulation of salicylic acid in leaves and accelerated plant senescence. Collectively, our data reveal specific pathways underpinning the phenotypic and molecular variation that arise and accumulate in clonal plant populations.

Item Type: Journal Article
Subjects: Q Science > QH Natural history > QH426 Genetics
Q Science > QK Botany
S Agriculture > SB Plant culture
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
SWORD Depositor: Library Publications Router
Library of Congress Subject Headings (LCSH): Clones (Plants), Plant propagation, Genetic regulation, Genetic transcription
Journal or Publication Title: PLOS Genetics
Publisher: Public Library of Science
ISSN: 1553-7404
Official Date: 16 November 2022
Dates:
DateEvent
16 November 2022Published
15 October 2022Accepted
Volume: 18
Number: 11
Article Number: e1010479
DOI: 10.1371/journal.pgen.1010479
Status: Peer Reviewed
Publication Status: Published
Reuse Statement (publisher, data, author rights): ** From PLOS via Jisc Publications Router ** History: received 27-04-2022; accepted 15-10-2022; collection 11-2022; epub 16-11-2022. ** Licence for this article: http://creativecommons.org/licenses/by/4.0/ ** Acknowledgements: We thank Gary Grant for help with plant husbandry, and Liliana M. Costa for discussions and comments on the manuscript.
Access rights to Published version: Open Access (Creative Commons)
Date of first compliant deposit: 19 December 2022
Date of first compliant Open Access: 19 December 2022
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
ERA-CAPS AUREATE[DFG] Deutsche Forschungsgemeinschafthttp://dx.doi.org/10.13039/501100001659
UNSPECIFIEDMax-Planck-Gesellschafthttp://dx.doi.org/10.13039/501100004189
751204-H2020-MSCA-IF-2016European Research Councilhttp://dx.doi.org/10.13039/501100000781
387/UN3.14/PT/2020Universitas Airlanggahttp://dx.doi.org/10.13039/501100008463
BB/L003023/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/N005279/1 [BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/N00194X/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/P02601X/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
Related URLs:
  • http://creativecommons.org/licenses/by/4...
Contributors:
ContributionNameContributor ID
UNSPECIFIEDSpringer, Nathan M.UNSPECIFIED

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