Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood Nematode

Pine wilt disease (PWD), caused by the plant–parasitic nematode Bursaphelenchus xylophilus, has become a severe environmental problem in the Iberian Peninsula with devastating effects in Pinus pinaster forests. Despite the high levels of this species' susceptibility, previous studies reported h...

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Main Authors: Inês Modesto, Lieven Sterck, Vicent Arbona, Aurelio Gómez-Cadenas, Isabel Carrasquinho, Yves Van de Peer, Célia M. Miguel
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.690857/full
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author Inês Modesto
Inês Modesto
Inês Modesto
Lieven Sterck
Lieven Sterck
Vicent Arbona
Aurelio Gómez-Cadenas
Isabel Carrasquinho
Isabel Carrasquinho
Yves Van de Peer
Yves Van de Peer
Yves Van de Peer
Célia M. Miguel
Célia M. Miguel
author_facet Inês Modesto
Inês Modesto
Inês Modesto
Lieven Sterck
Lieven Sterck
Vicent Arbona
Aurelio Gómez-Cadenas
Isabel Carrasquinho
Isabel Carrasquinho
Yves Van de Peer
Yves Van de Peer
Yves Van de Peer
Célia M. Miguel
Célia M. Miguel
author_sort Inês Modesto
collection DOAJ
description Pine wilt disease (PWD), caused by the plant–parasitic nematode Bursaphelenchus xylophilus, has become a severe environmental problem in the Iberian Peninsula with devastating effects in Pinus pinaster forests. Despite the high levels of this species' susceptibility, previous studies reported heritable resistance in P. pinaster trees. Understanding the basis of this resistance can be of extreme relevance for future programs aiming at reducing the disease impact on P. pinaster forests. In this study, we highlighted the mechanisms possibly involved in P. pinaster resistance to PWD, by comparing the transcriptional changes between resistant and susceptible plants after infection. Our analysis revealed a higher number of differentially expressed genes (DEGs) in resistant plants (1,916) when compared with susceptible plants (1,226). Resistance to PWN is mediated by the induction of the jasmonic acid (JA) defense pathway, secondary metabolism pathways, lignin synthesis, oxidative stress response genes, and resistance genes. Quantification of the acetyl bromide-soluble lignin confirmed a significant increase of cell wall lignification of stem tissues around the inoculation zone in resistant plants. In addition to less lignified cell walls, susceptibility to the pine wood nematode seems associated with the activation of the salicylic acid (SA) defense pathway at 72 hpi, as revealed by the higher SA levels in the tissues of susceptible plants. Cell wall reinforcement and hormone signaling mechanisms seem therefore essential for a resistance response.
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spelling doaj.art-6ed4e4b33d7d4078bc871476086e2f182022-12-21T22:28:14ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-06-011210.3389/fpls.2021.690857690857Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood NematodeInês Modesto0Inês Modesto1Inês Modesto2Lieven Sterck3Lieven Sterck4Vicent Arbona5Aurelio Gómez-Cadenas6Isabel Carrasquinho7Isabel Carrasquinho8Yves Van de Peer9Yves Van de Peer10Yves Van de Peer11Célia M. Miguel12Célia M. Miguel13Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, PortugalInstituto de Biologia e Tecnologia Experimental, Oeiras, PortugalDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB-UGent Center for Plant Systems Biology, Ghent, BelgiumDepartament de Ciències Agràries i del Medi Natural, Universitat Jaume I, Castelló de la Plana, SpainDepartament de Ciències Agràries i del Medi Natural, Universitat Jaume I, Castelló de la Plana, SpainInstituto Nacional Investigaciao Agraria e Veterinaria, Oeiras, PortugalLinking Landscape, Environment, Agriculture and Food, Instituto Superior de Agronomia, Universidade de Lisboa, Lisbon, PortugalDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB-UGent Center for Plant Systems Biology, Ghent, BelgiumDepartment of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South AfricaInstituto de Biologia e Tecnologia Experimental, Oeiras, PortugalBiosystems and Integrative Sciences Institute, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalPine wilt disease (PWD), caused by the plant–parasitic nematode Bursaphelenchus xylophilus, has become a severe environmental problem in the Iberian Peninsula with devastating effects in Pinus pinaster forests. Despite the high levels of this species' susceptibility, previous studies reported heritable resistance in P. pinaster trees. Understanding the basis of this resistance can be of extreme relevance for future programs aiming at reducing the disease impact on P. pinaster forests. In this study, we highlighted the mechanisms possibly involved in P. pinaster resistance to PWD, by comparing the transcriptional changes between resistant and susceptible plants after infection. Our analysis revealed a higher number of differentially expressed genes (DEGs) in resistant plants (1,916) when compared with susceptible plants (1,226). Resistance to PWN is mediated by the induction of the jasmonic acid (JA) defense pathway, secondary metabolism pathways, lignin synthesis, oxidative stress response genes, and resistance genes. Quantification of the acetyl bromide-soluble lignin confirmed a significant increase of cell wall lignification of stem tissues around the inoculation zone in resistant plants. In addition to less lignified cell walls, susceptibility to the pine wood nematode seems associated with the activation of the salicylic acid (SA) defense pathway at 72 hpi, as revealed by the higher SA levels in the tissues of susceptible plants. Cell wall reinforcement and hormone signaling mechanisms seem therefore essential for a resistance response.https://www.frontiersin.org/articles/10.3389/fpls.2021.690857/fullcell wall lignificationjasmonatemaritime pinepine wilt diseaseresistance genessecondary metabolism
spellingShingle Inês Modesto
Inês Modesto
Inês Modesto
Lieven Sterck
Lieven Sterck
Vicent Arbona
Aurelio Gómez-Cadenas
Isabel Carrasquinho
Isabel Carrasquinho
Yves Van de Peer
Yves Van de Peer
Yves Van de Peer
Célia M. Miguel
Célia M. Miguel
Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood Nematode
Frontiers in Plant Science
cell wall lignification
jasmonate
maritime pine
pine wilt disease
resistance genes
secondary metabolism
title Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood Nematode
title_full Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood Nematode
title_fullStr Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood Nematode
title_full_unstemmed Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood Nematode
title_short Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood Nematode
title_sort insights into the mechanisms implicated in pinus pinaster resistance to pinewood nematode
topic cell wall lignification
jasmonate
maritime pine
pine wilt disease
resistance genes
secondary metabolism
url https://www.frontiersin.org/articles/10.3389/fpls.2021.690857/full
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