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MicroRNA-mediated post-transcriptional regulation of Pinus pinaster response and resistance to pinewood nematode

Pine wilt disease (PWD), caused by the parasitic nematode Bursaphelenchus xylophilus, or pinewood nematode (PWN), is a serious threat to pine forests in Europe. Pinus pinaster is highly susceptible to the disease and it is currently the most affected European pine species. In this work, we investiga...

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Autores principales: Modesto, Inês, Inácio, Vera, Van de Peer, Yves, Miguel, Célia M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8956650/
https://www.ncbi.nlm.nih.gov/pubmed/35338210
http://dx.doi.org/10.1038/s41598-022-09163-3
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author Modesto, Inês
Inácio, Vera
Van de Peer, Yves
Miguel, Célia M.
author_facet Modesto, Inês
Inácio, Vera
Van de Peer, Yves
Miguel, Célia M.
author_sort Modesto, Inês
collection PubMed
description Pine wilt disease (PWD), caused by the parasitic nematode Bursaphelenchus xylophilus, or pinewood nematode (PWN), is a serious threat to pine forests in Europe. Pinus pinaster is highly susceptible to the disease and it is currently the most affected European pine species. In this work, we investigated the role of small RNAs (sRNAs) in regulating P. pinaster–PWN interaction in an early stage of infection. After performing an artificial PWN inoculation assay, we have identified 105 plant microRNAs (miRNAs) responsive to PWN. Based on their predicted targets, part of these miRNAs was associated with roles in jasmonate-response pathway, ROS detoxification, and terpenoid biosynthesis. Furthermore, by comparing resistant and susceptible plants, eight miRNAs with putative functions in plant defence and resistance to PWN have been identified. Finally, we explored the possibility of bidirectional trans-kingdom RNA silencing, identifying several P. pinaster genes putatively targeted by PWN miRNAs, which was supported by degradome analysis. Targets for P. pinaster miRNAs were also predicted in PWN, suggesting a role for trans-kingdom miRNA transfer and gene silencing both in PWN parasitism as in P. pinaster resistance to PWD. Our results provide new insights into previously unexplored roles of sRNA post-transcriptional regulation in P. pinaster response and resistance to PWN.
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spelling pubmed-89566502022-03-28 MicroRNA-mediated post-transcriptional regulation of Pinus pinaster response and resistance to pinewood nematode Modesto, Inês Inácio, Vera Van de Peer, Yves Miguel, Célia M. Sci Rep Article Pine wilt disease (PWD), caused by the parasitic nematode Bursaphelenchus xylophilus, or pinewood nematode (PWN), is a serious threat to pine forests in Europe. Pinus pinaster is highly susceptible to the disease and it is currently the most affected European pine species. In this work, we investigated the role of small RNAs (sRNAs) in regulating P. pinaster–PWN interaction in an early stage of infection. After performing an artificial PWN inoculation assay, we have identified 105 plant microRNAs (miRNAs) responsive to PWN. Based on their predicted targets, part of these miRNAs was associated with roles in jasmonate-response pathway, ROS detoxification, and terpenoid biosynthesis. Furthermore, by comparing resistant and susceptible plants, eight miRNAs with putative functions in plant defence and resistance to PWN have been identified. Finally, we explored the possibility of bidirectional trans-kingdom RNA silencing, identifying several P. pinaster genes putatively targeted by PWN miRNAs, which was supported by degradome analysis. Targets for P. pinaster miRNAs were also predicted in PWN, suggesting a role for trans-kingdom miRNA transfer and gene silencing both in PWN parasitism as in P. pinaster resistance to PWD. Our results provide new insights into previously unexplored roles of sRNA post-transcriptional regulation in P. pinaster response and resistance to PWN. Nature Publishing Group UK 2022-03-25 /pmc/articles/PMC8956650/ /pubmed/35338210 http://dx.doi.org/10.1038/s41598-022-09163-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Modesto, Inês
Inácio, Vera
Van de Peer, Yves
Miguel, Célia M.
MicroRNA-mediated post-transcriptional regulation of Pinus pinaster response and resistance to pinewood nematode
title MicroRNA-mediated post-transcriptional regulation of Pinus pinaster response and resistance to pinewood nematode
title_full MicroRNA-mediated post-transcriptional regulation of Pinus pinaster response and resistance to pinewood nematode
title_fullStr MicroRNA-mediated post-transcriptional regulation of Pinus pinaster response and resistance to pinewood nematode
title_full_unstemmed MicroRNA-mediated post-transcriptional regulation of Pinus pinaster response and resistance to pinewood nematode
title_short MicroRNA-mediated post-transcriptional regulation of Pinus pinaster response and resistance to pinewood nematode
title_sort microrna-mediated post-transcriptional regulation of pinus pinaster response and resistance to pinewood nematode
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8956650/
https://www.ncbi.nlm.nih.gov/pubmed/35338210
http://dx.doi.org/10.1038/s41598-022-09163-3
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