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
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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John Wiley & Sons
2022-07-24
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| Subjects: | Arabidopsis, DNA Methylation/Epigenetics signatures, Galls, Giant cells, Meloidogyne javanica, Tomato, Transposons, siRNAs, |
| Online Access: | http://hdl.handle.net/10261/277371 http://dx.doi.org/10.13039/501100000735 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100010805 http://dx.doi.org/10.13039/501100011698 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100007480 |
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Arabidopsis DNA Methylation/Epigenetics signatures Galls Giant cells Meloidogyne javanica Tomato Transposons siRNAs Arabidopsis DNA Methylation/Epigenetics signatures Galls Giant cells Meloidogyne javanica Tomato Transposons siRNAs |
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Arabidopsis DNA Methylation/Epigenetics signatures Galls Giant cells Meloidogyne javanica Tomato Transposons siRNAs Arabidopsis DNA Methylation/Epigenetics signatures Galls Giant cells Meloidogyne javanica Tomato Transposons siRNAs 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, María Fé 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 |
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© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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Ministerio de Ciencia e Innovación (España) |
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Ministerio de Ciencia e Innovación (España) 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, María Fé Fenoll, Carmen Eves-van den Akker, Sebastian Escobar, Carolina |
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artículo |
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Arabidopsis DNA Methylation/Epigenetics signatures Galls Giant cells Meloidogyne javanica Tomato Transposons siRNAs |
| 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, María Fé Fenoll, Carmen Eves-van den Akker, Sebastian Escobar, Carolina |
| author_sort |
Silva, Ana Cláudia |
| 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_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_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_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 |
| publisher |
John Wiley & Sons |
| publishDate |
2022-07-24 |
| url |
http://hdl.handle.net/10261/277371 http://dx.doi.org/10.13039/501100000735 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100010805 http://dx.doi.org/10.13039/501100011698 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100007480 |
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dig-ica-es-10261-2773712024-05-09T07:33:32Z 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, María Fé Fenoll, Carmen Eves-van den Akker, Sebastian Escobar, Carolina Ministerio de Ciencia e Innovación (España) Junta de Comunidades de Castilla-La Mancha Universidad de Castilla La Mancha European Commission University of Cambridge Fundación Tatiana Pérez de Guzmán el Bueno Silva, Ana Cláudia [0000-0002-6113-9722] Ruiz-Ferrer, Virginia [0000- 0002-7840-297X] Pellegrin, Clement [0000-0002-6591- 655X] Abril-Urías, Patricia [0000-0003-0677-5600] Martínez-Gómez, Ángela [0000-0002-8920-4725] Gómez-Rojas, Almudena [0000-0002-7397-4768] Berenguer, Eduardo [0000-0002-0902-1057] Testillano, P. S. [0000-0003-4509-7646] Fenoll, Carmen [0000- 0003-4653-6268] Eves-van den Akker, Sebastian [https://orcid.org/0000-0002-8833-9679] Escobar, Carolina [0000- 0001-9365-0851] Arabidopsis DNA Methylation/Epigenetics signatures Galls Giant cells Meloidogyne javanica Tomato Transposons siRNAs © 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Root-knot-nematodes (RKNs) induce giant cells (GCs) within galls, characterized by large-scale gene-repression at early-stages. However, epigenetic mechanism/s underlying gene silencing are still poorly characterized. DNA-methylation in Arabidopsis thaliana galls induced by Meloidogyne javanica at crucial infection-stages (3/14 days post-infection; dpi) was studied using enzymatic, cytological, and sequencing approaches. Mutants in cytosine-DNA-Methyltransferases (met1, cmt2, cmt3, cmt2/3, drm1/2, ddc) and DNA-demethylase (ros1), were analyzed for RKN-resistance/tolerance, and galls were characterized by confocal-microscopy and RNA-seq. Early-galls were hypermethylated, where the GCs within are the major contributors, correlating with their massive gene-repression. In contrast, medium/late-galls showed no global increase in DNA-methylation compared to uninfected-roots, but large-scale redistribution of differentially methylated regions (DMRs). Accordingly, DNA-methylation, but also demethylation mutants showed impaired nematode reproduction and gall/GC-development. Moreover, siRNAs exclusively present in early-galls accumulated at hypermethylated DMRs overlapping mostly with retrotransposons at 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) seem prominent mechanisms driving a dynamic regulation of the epigenetic landscape during RKN infection. This work was supported by the Spanish Government (RED2018-02407-T) and PID2019-105924RB-I00 funded by MCIN/AEI/ 10.13039/501100011033 and SBPLY/17/180501/000287; SBPLY/21/180501/000033 by the Castilla- La Mancha Government, to CE. The laboratory received support from UCLM intramural funds. ACS. and AM-G were supported by a fellowship from the University of Castilla-La Mancha, co-funded by the European Social Fund and ACS. by an EMBO Short-Term Fellowship during her short-term stay at the University of Cambridge. AM-G was supported by a fellowship from Fundación Tatiana Pérez de Guzmán el Bueno. Work on plant-parasitic nematodes at the University of Cambridge is supported by DEFRA license 125034/359149/3 and funded by BBSRC grants BB/R011311/1, BB/N021908/1, and BB/S006397/1. Peer reviewed 2022-08-25T11:06:02Z 2022-08-25T11:06:02Z 2022-07-24 artículo http://purl.org/coar/resource_type/c_6501 New Phytologist 236(5): 1888-1907 (2022) 0028-646X http://hdl.handle.net/10261/277371 10.1111/nph.18395 1469-8137 http://dx.doi.org/10.13039/501100000735 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100010805 http://dx.doi.org/10.13039/501100011698 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100007480 en #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-105924RB-I00/ES/ESTUDIANDO LOS SITIOS DE ALIMENTACION (AGALLAS%2FCELULAS GIGANTES) DE NEMATODOS FITOPARASITOS CON UNA PERSPECTIVA CELULAR PARA EL DESARROLLO DE HERRAMIENTAS DIRIGIDAS DE CONTROL/ Publisher's version Data openly available in a public repository that does not issue DOIs. The data that support the findings of this study are openly available in GEO at https://www.ncbi.nlm.nih.gov/geo/, under reference nos. GSE155171, GSE155853 and GSE156025. The underlying dataset has been published as supplementary material of the article in the publisher platform at https://doi.org/10.1111/nph.18395 http://doi.org/10.1111/nph.18395 Sí open application/pdf John Wiley & Sons |