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The DNA methylation landscape of the root‐knot nematode‐induced pseudo‐organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism

Root‐knot nematodes (RKNs) induce giant cells (GCs) within galls which are characterized by large‐scale gene repression at early stages. However, the epigenetic mechanism(s) underlying gene silencing is (are) still poorly characterized. DNA methylation in Arabidopsis galls induced by Meloidogyne jav...

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Autores principales: Silva, Ana Cláudia, Ruiz‐Ferrer, Virginia, Müller, Sebastian Y., Pellegrin, Clement, Abril‐Urías, Patricia, Martínez‐Gómez, Ángela, Gómez‐Rojas, Almudena, Berenguer, Eduardo, Testillano, Pilar S., Andrés, Maria Fe, Fenoll, Carmen, Eves‐van den Akker, Sebastian, Escobar, Carolina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9825882/
https://www.ncbi.nlm.nih.gov/pubmed/35872574
http://dx.doi.org/10.1111/nph.18395
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author Silva, Ana Cláudia
Ruiz‐Ferrer, Virginia
Müller, Sebastian Y.
Pellegrin, Clement
Abril‐Urías, Patricia
Martínez‐Gómez, Ángela
Gómez‐Rojas, Almudena
Berenguer, Eduardo
Testillano, Pilar S.
Andrés, Maria Fe
Fenoll, Carmen
Eves‐van den Akker, Sebastian
Escobar, Carolina
author_facet Silva, Ana Cláudia
Ruiz‐Ferrer, Virginia
Müller, Sebastian Y.
Pellegrin, Clement
Abril‐Urías, Patricia
Martínez‐Gómez, Ángela
Gómez‐Rojas, Almudena
Berenguer, Eduardo
Testillano, Pilar S.
Andrés, Maria Fe
Fenoll, Carmen
Eves‐van den Akker, Sebastian
Escobar, Carolina
author_sort Silva, Ana Cláudia
collection PubMed
description Root‐knot nematodes (RKNs) induce giant cells (GCs) within galls which are characterized by large‐scale gene repression at early stages. However, the epigenetic mechanism(s) underlying gene silencing is (are) still poorly characterized. DNA methylation in Arabidopsis galls induced by Meloidogyne javanica was studied at crucial infection stages (3 d post‐infection (dpi) and 14 dpi) using enzymatic, cytological, and sequencing approaches. DNA methyltransferase mutants (met1, cmt2, cmt3, cmt2/3, drm1/2, ddc) and a DNA demethylase mutant (ros1), were analyzed for RKN resistance/tolerance, and galls were characterized by confocal microscopy and RNA‐seq. Early galls were hypermethylated, and the GCs were found to be the major contributors to this hypermethylation, consistent with the very high degree of gene repression they exhibit. By contrast, medium/late galls showed no global increase in DNA methylation compared to uninfected roots, but exhibited large‐scale redistribution of differentially methylated regions (DMRs). In line with these findings, it was also shown that DNA methylation and demethylation mutants showed impaired nematode reproduction and gall/GC‐development. Moreover, siRNAs that were exclusively present in early galls accumulated at hypermethylated DMRs, overlapping mostly with retrotransposons in the CHG/CG contexts that might be involved in their repression, contributing to their stability/genome integrity. Promoter/gene methylation correlated with differentially expressed genes encoding proteins with basic cell functions. Both mechanisms are consistent with reprogramming host tissues for gall/GC formation. In conclusion, RNA‐directed DNA methylation (RdDM; DRM2/1) pathways, maintenance methyltransferases (MET1/CMT3) and demethylation (ROS1) appear to be prominent mechanisms driving a dynamic regulation of the epigenetic landscape during RKN infection.
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spelling pubmed-98258822023-01-09 The DNA methylation landscape of the root‐knot nematode‐induced pseudo‐organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism Silva, Ana Cláudia Ruiz‐Ferrer, Virginia Müller, Sebastian Y. Pellegrin, Clement Abril‐Urías, Patricia Martínez‐Gómez, Ángela Gómez‐Rojas, Almudena Berenguer, Eduardo Testillano, Pilar S. Andrés, Maria Fe Fenoll, Carmen Eves‐van den Akker, Sebastian Escobar, Carolina New Phytol Research Root‐knot nematodes (RKNs) induce giant cells (GCs) within galls which are characterized by large‐scale gene repression at early stages. However, the epigenetic mechanism(s) underlying gene silencing is (are) still poorly characterized. DNA methylation in Arabidopsis galls induced by Meloidogyne javanica was studied at crucial infection stages (3 d post‐infection (dpi) and 14 dpi) using enzymatic, cytological, and sequencing approaches. DNA methyltransferase mutants (met1, cmt2, cmt3, cmt2/3, drm1/2, ddc) and a DNA demethylase mutant (ros1), were analyzed for RKN resistance/tolerance, and galls were characterized by confocal microscopy and RNA‐seq. Early galls were hypermethylated, and the GCs were found to be the major contributors to this hypermethylation, consistent with the very high degree of gene repression they exhibit. By contrast, medium/late galls showed no global increase in DNA methylation compared to uninfected roots, but exhibited large‐scale redistribution of differentially methylated regions (DMRs). In line with these findings, it was also shown that DNA methylation and demethylation mutants showed impaired nematode reproduction and gall/GC‐development. Moreover, siRNAs that were exclusively present in early galls accumulated at hypermethylated DMRs, overlapping mostly with retrotransposons in the CHG/CG contexts that might be involved in their repression, contributing to their stability/genome integrity. Promoter/gene methylation correlated with differentially expressed genes encoding proteins with basic cell functions. Both mechanisms are consistent with reprogramming host tissues for gall/GC formation. In conclusion, RNA‐directed DNA methylation (RdDM; DRM2/1) pathways, maintenance methyltransferases (MET1/CMT3) and demethylation (ROS1) appear to be prominent mechanisms driving a dynamic regulation of the epigenetic landscape during RKN infection. John Wiley and Sons Inc. 2022-09-02 2022-12 /pmc/articles/PMC9825882/ /pubmed/35872574 http://dx.doi.org/10.1111/nph.18395 Text en © 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Silva, Ana Cláudia
Ruiz‐Ferrer, Virginia
Müller, Sebastian Y.
Pellegrin, Clement
Abril‐Urías, Patricia
Martínez‐Gómez, Ángela
Gómez‐Rojas, Almudena
Berenguer, Eduardo
Testillano, Pilar S.
Andrés, Maria Fe
Fenoll, Carmen
Eves‐van den Akker, Sebastian
Escobar, Carolina
The DNA methylation landscape of the root‐knot nematode‐induced pseudo‐organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism
title The DNA methylation landscape of the root‐knot nematode‐induced pseudo‐organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism
title_full The DNA methylation landscape of the root‐knot nematode‐induced pseudo‐organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism
title_fullStr The DNA methylation landscape of the root‐knot nematode‐induced pseudo‐organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism
title_full_unstemmed The DNA methylation landscape of the root‐knot nematode‐induced pseudo‐organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism
title_short The DNA methylation landscape of the root‐knot nematode‐induced pseudo‐organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism
title_sort dna methylation landscape of the root‐knot nematode‐induced pseudo‐organ, the gall, in arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9825882/
https://www.ncbi.nlm.nih.gov/pubmed/35872574
http://dx.doi.org/10.1111/nph.18395
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