Proteomic analysis of Masson pine with high resistance to pine wood nematodes.

Pine wilt disease is a dangerous pine disease globally. We used Masson pine (Pinus massoniana) clones, selected through traditional breeding and testing for 20 years, to study the molecular mechanism of their high resistance to pine wood nematodes (PWN,Bursaphelenchus xylophilus). Nine strains of se...

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Main Authors: Jingbin Gao, Ting Pan, Xuelian Chen, Qiang Wei, Liuyi Xu
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0273010
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author Jingbin Gao
Ting Pan
Xuelian Chen
Qiang Wei
Liuyi Xu
author_facet Jingbin Gao
Ting Pan
Xuelian Chen
Qiang Wei
Liuyi Xu
author_sort Jingbin Gao
collection DOAJ
description Pine wilt disease is a dangerous pine disease globally. We used Masson pine (Pinus massoniana) clones, selected through traditional breeding and testing for 20 years, to study the molecular mechanism of their high resistance to pine wood nematodes (PWN,Bursaphelenchus xylophilus). Nine strains of seedlings of genetically stable Masson pine screened from different families with high resistance to PWN were used. The same number of sensitive clones were used as susceptible controls. Total proteins were extracted for tandem mass tag (TMT) quantitative proteomic analysis. The key proteins were verified by parallel reaction monitoring (PRM). A threshold of upregulation greater than 1.3-fold or downregulation greater than 0.3-fold was considered significant in highly resistant strains versus sensitive strains. A total of 3491 proteins were identified from the seedling tissues, among which 2783 proteins contained quantitative information. A total of 42 proteins were upregulated and 96 proteins were downregulated in the resistant strains. Functional enrichment analysis found significant differences in the proteins with pectin esterase activity or peroxidase activity. The proteins participating in salicylic acid metabolism, antioxidant stress reaction, polysaccharide degradation, glucose acid ester sheath lipid biosynthesis, and the sugar glycosaminoglycan degradation pathway were also changed significantly. The PRM results showed that pectin acetyl esterase, carbonic anhydrase, peroxidase, and chitinase were significantly downregulated, while aspartic protease was significantly upregulated, which was consistent with the proteomic data. These results suggest that Masson pine can degrade nematode-related proteins by increasing protease to inhibit their infestation, and can enhance the resistance of Masson pine to PWN by downregulating carbon metabolism to limit the carbon available to PWN or for involvement in cell wall components or tissue softening. Most of the downregulated proteins are supposed to act as an alternative mechanism for latter enhancement after pathogen attacks. The highly resistant Masson pine, very likely, harbors multiple pathways, both passive and active, to defend against PWN infestation.
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spelling doaj.art-8cc65e74dbed4b7a9ca4e9a8d80684b72022-12-22T03:12:52ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-01178e027301010.1371/journal.pone.0273010Proteomic analysis of Masson pine with high resistance to pine wood nematodes.Jingbin GaoTing PanXuelian ChenQiang WeiLiuyi XuPine wilt disease is a dangerous pine disease globally. We used Masson pine (Pinus massoniana) clones, selected through traditional breeding and testing for 20 years, to study the molecular mechanism of their high resistance to pine wood nematodes (PWN,Bursaphelenchus xylophilus). Nine strains of seedlings of genetically stable Masson pine screened from different families with high resistance to PWN were used. The same number of sensitive clones were used as susceptible controls. Total proteins were extracted for tandem mass tag (TMT) quantitative proteomic analysis. The key proteins were verified by parallel reaction monitoring (PRM). A threshold of upregulation greater than 1.3-fold or downregulation greater than 0.3-fold was considered significant in highly resistant strains versus sensitive strains. A total of 3491 proteins were identified from the seedling tissues, among which 2783 proteins contained quantitative information. A total of 42 proteins were upregulated and 96 proteins were downregulated in the resistant strains. Functional enrichment analysis found significant differences in the proteins with pectin esterase activity or peroxidase activity. The proteins participating in salicylic acid metabolism, antioxidant stress reaction, polysaccharide degradation, glucose acid ester sheath lipid biosynthesis, and the sugar glycosaminoglycan degradation pathway were also changed significantly. The PRM results showed that pectin acetyl esterase, carbonic anhydrase, peroxidase, and chitinase were significantly downregulated, while aspartic protease was significantly upregulated, which was consistent with the proteomic data. These results suggest that Masson pine can degrade nematode-related proteins by increasing protease to inhibit their infestation, and can enhance the resistance of Masson pine to PWN by downregulating carbon metabolism to limit the carbon available to PWN or for involvement in cell wall components or tissue softening. Most of the downregulated proteins are supposed to act as an alternative mechanism for latter enhancement after pathogen attacks. The highly resistant Masson pine, very likely, harbors multiple pathways, both passive and active, to defend against PWN infestation.https://doi.org/10.1371/journal.pone.0273010
spellingShingle Jingbin Gao
Ting Pan
Xuelian Chen
Qiang Wei
Liuyi Xu
Proteomic analysis of Masson pine with high resistance to pine wood nematodes.
PLoS ONE
title Proteomic analysis of Masson pine with high resistance to pine wood nematodes.
title_full Proteomic analysis of Masson pine with high resistance to pine wood nematodes.
title_fullStr Proteomic analysis of Masson pine with high resistance to pine wood nematodes.
title_full_unstemmed Proteomic analysis of Masson pine with high resistance to pine wood nematodes.
title_short Proteomic analysis of Masson pine with high resistance to pine wood nematodes.
title_sort proteomic analysis of masson pine with high resistance to pine wood nematodes
url https://doi.org/10.1371/journal.pone.0273010
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