Cargando…

The callus formation capacity of strawberry leaf explants is modulated by DNA methylation

Shoot regeneration from leaf tissue requires the de-differentiation of cells from a highly differentiated state into an actively dividing state, but it remains unclear how this physiological transition occurs and is regulated, especially at the epigenetic level. Here, we characterized the DNA methyl...

Descripción completa

Detalles Bibliográficos
Autores principales: Liu, Decai, Mu, Qin, Li, Xianyang, Xu, Sheng, Li, Yi, Gu, Tingting
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8947209/
https://www.ncbi.nlm.nih.gov/pubmed/35043170
http://dx.doi.org/10.1093/hr/uhab073
_version_ 1784674384422633472
author Liu, Decai
Mu, Qin
Li, Xianyang
Xu, Sheng
Li, Yi
Gu, Tingting
author_facet Liu, Decai
Mu, Qin
Li, Xianyang
Xu, Sheng
Li, Yi
Gu, Tingting
author_sort Liu, Decai
collection PubMed
description Shoot regeneration from leaf tissue requires the de-differentiation of cells from a highly differentiated state into an actively dividing state, but it remains unclear how this physiological transition occurs and is regulated, especially at the epigenetic level. Here, we characterized the DNA methylome represented by 5-methylcytosine (5mC) in leaf and callus tissue derived from leaf explants of woodland strawberry, Fragaria vesca. We detected an overall increase in DNA methylation and distinct 5mC enrichment patterns in the CG, CHG, and CHH sequence contexts in genes and transposable elements. Our analyses revealed an intricate relationship between DNA methylation and gene expression level in leaves or leaf-derived callus. However, when considering the genes involved in callus formation and shoot regeneration, e.g. FvePLT3/7, FveWIND3, FveWIND4, FveLOG4 and FveIAA14, their dynamic transcription levels were associated with differentially methylated regions located in the promoters or gene bodies, indicating a regulatory role of DNA methylation in the transcriptional regulation of pluripotency acquisition in strawberry. Furthermore, application of the DNA methyltransferase inhibitor 5′-azacytidine (5′-Aza) hampered both callus formation and shoot regeneration from the leaf explants. We further showed that 5′-Aza downregulated the expression of genes involved in cell wall integrity, such as expansin, pectin lyase, and pectin methylesterase genes, suggesting an essential role of cell wall metabolism during callus formation. This study reveals the contribution of DNA methylation to callus formation capacity and will provide a basis for developing a strategy to improve shoot regeneration for basic and applied research applications.
format Online
Article
Text
id pubmed-8947209
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-89472092022-03-28 The callus formation capacity of strawberry leaf explants is modulated by DNA methylation Liu, Decai Mu, Qin Li, Xianyang Xu, Sheng Li, Yi Gu, Tingting Hortic Res Article Shoot regeneration from leaf tissue requires the de-differentiation of cells from a highly differentiated state into an actively dividing state, but it remains unclear how this physiological transition occurs and is regulated, especially at the epigenetic level. Here, we characterized the DNA methylome represented by 5-methylcytosine (5mC) in leaf and callus tissue derived from leaf explants of woodland strawberry, Fragaria vesca. We detected an overall increase in DNA methylation and distinct 5mC enrichment patterns in the CG, CHG, and CHH sequence contexts in genes and transposable elements. Our analyses revealed an intricate relationship between DNA methylation and gene expression level in leaves or leaf-derived callus. However, when considering the genes involved in callus formation and shoot regeneration, e.g. FvePLT3/7, FveWIND3, FveWIND4, FveLOG4 and FveIAA14, their dynamic transcription levels were associated with differentially methylated regions located in the promoters or gene bodies, indicating a regulatory role of DNA methylation in the transcriptional regulation of pluripotency acquisition in strawberry. Furthermore, application of the DNA methyltransferase inhibitor 5′-azacytidine (5′-Aza) hampered both callus formation and shoot regeneration from the leaf explants. We further showed that 5′-Aza downregulated the expression of genes involved in cell wall integrity, such as expansin, pectin lyase, and pectin methylesterase genes, suggesting an essential role of cell wall metabolism during callus formation. This study reveals the contribution of DNA methylation to callus formation capacity and will provide a basis for developing a strategy to improve shoot regeneration for basic and applied research applications. Oxford University Press 2022-01-19 /pmc/articles/PMC8947209/ /pubmed/35043170 http://dx.doi.org/10.1093/hr/uhab073 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Nanjing Agricultural University https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Article
Liu, Decai
Mu, Qin
Li, Xianyang
Xu, Sheng
Li, Yi
Gu, Tingting
The callus formation capacity of strawberry leaf explants is modulated by DNA methylation
title The callus formation capacity of strawberry leaf explants is modulated by DNA methylation
title_full The callus formation capacity of strawberry leaf explants is modulated by DNA methylation
title_fullStr The callus formation capacity of strawberry leaf explants is modulated by DNA methylation
title_full_unstemmed The callus formation capacity of strawberry leaf explants is modulated by DNA methylation
title_short The callus formation capacity of strawberry leaf explants is modulated by DNA methylation
title_sort callus formation capacity of strawberry leaf explants is modulated by dna methylation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8947209/
https://www.ncbi.nlm.nih.gov/pubmed/35043170
http://dx.doi.org/10.1093/hr/uhab073
work_keys_str_mv AT liudecai thecallusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT muqin thecallusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT lixianyang thecallusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT xusheng thecallusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT liyi thecallusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT gutingting thecallusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT liudecai callusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT muqin callusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT lixianyang callusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT xusheng callusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT liyi callusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation
AT gutingting callusformationcapacityofstrawberryleafexplantsismodulatedbydnamethylation