Catalases Induction in High Virulence Pinewood Nematode Bursaphelenchus xylophilus under Hydrogen Peroxide-Induced Stress

Vicente, Cláudia S. L.; Ikuyo, Yoriko; Shinya, Ryoji; Mota, Manuel; Hasegawa, Koichi

doi:10.1371/journal.pone.0123839

Cited by 31 publications

(48 citation statements)

References 35 publications

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“…In the present study, antioxidant proteins were also identified in the secretome of B. xylophilus . These proteins have been proved as pivotal tools in protecting B. xylophilus from ROS and toxic compounds accumulated inside the pine trees3738.…”

Section: Discussionmentioning

confidence: 99%

Bursaphelenchus xylophilus and B. mucronatus secretomes: a comparative proteomic analysis

Cardoso

Anjo

Fonseca

et al. 2016

Sci Rep

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The pinewood nematode, Bursaphelenchus xylophilus, recognized as a worldwide major forest pest, is a migratory endoparasitic nematode with capacity to feed on pine tissues and also on fungi colonizing the trees. Bursaphelenchus mucronatus, the closest related species, differs from B. xylophilus on its pathogenicity, making this nematode a good candidate for comparative analyses. Secretome profiles of B. xylophilus and B. mucronatus were obtained and proteomic differences were evaluated by quantitative SWATH-MS. From the 681 proteins initially identified, 422 were quantified and compared between B. xylophilus and B. mucronatus secretomes and from these, 243 proteins were found differentially regulated: 158 and 85 proteins were increased in B. xylophilus and B. mucronatus secretomes, respectively. While increased proteins in B. xylophilus secretome revealed a strong enrichment in proteins with peptidase activity, the increased proteins in B. mucronatus secretome were mainly related to oxidative stress responses. The changes in peptidases were evaluated at the transcription level by RT-qPCR, revealing a correlation between the mRNA levels of four cysteine peptidases with secretion levels. The analysis presented expands our knowledge about molecular basis of B. xylophilus and B. mucronatus hosts interaction and supports the hypothesis of a key role of secreted peptidases in B. xylophilus pathogenicity.

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Section: Discussionmentioning

confidence: 99%

Bursaphelenchus xylophilus and B. mucronatus secretomes: a comparative proteomic analysis

Cardoso

Anjo

Fonseca

et al. 2016

Sci Rep

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“…Interestingly, Siddique et al (2014) showed a positive role for H 2 O 2 in Arabidopsis susceptibility to cyst nematodes, indicating that nematodes can also induce ROS to promote infection. Correlations between nematode virulence and resistance to oxidative stress have been observed in the pinewood nematode, Bursaphelenchus xylophilus (Vicente et al , 2015). Together, these findings support the idea that the establishment of a cytoprotective mechanism against environmental oxidative stresses is a crucial prerequisite for successful PPN infection at both early and later time points after contact with the plant cell.…”

Section: Section I: Plant Basal Defence the Apoplast And The Redox Bmentioning

confidence: 99%

“…Similarly, nematode J2s that have not yet entered the root (pre-parasitic plant nematodes) also provide pronounced resistance to oxidative stress, correlating with their degree of virulence (Dubreuil et al , 2011; Vicente et al , 2015; Li et al , 2016). In fact, previous findings have reported the insulin/IGF-1 signalling (IIS) pathway as a mediator between development and stress responses following the model ‘ should I stay or should I go ’ (Schindler and Sherwood, 2014).…”

Section: Section Ii: Potential Key Regulators Of Oxidative Stress Resmentioning

confidence: 99%

“…These studies have found mitochondrial and cytoplasmic SODs and CTLs in M. incognita and B. xylophilus (Bellafiore et al , 2008; Shinya et al , 2013). Moreover, the virulence of B. xylophilus is correlated with the degree of catalase expression and, by extension, its resistance to oxidative stress (Vicente et al , 2015). The PPN secretome also comprises two other relevant ROS-scavengers, GPX and PRX enzymes that are implicated in the regulation of a defensive oxidative burst from the plant.…”

Section: Section Ii: Potential Key Regulators Of Oxidative Stress Resmentioning

confidence: 99%

“…For instance, pre-parasitic plant nematodes show certain identical morphological and metabolic features, such as a strong cuticle and fat storage (Cassada and Russell, 1975; Robinson et al , 1987; Davies and Curtis, 2011). Another relevant similarity is the high resistance of PPNs to oxidative stress (Larsen, 1993; Dubreuil et al , 2011; Vicente et al , 2015). With regard to the evolutionary history of nematodes, Blaxter and Koutsovoulos (2014) proposed that the transition from a free-living habit to parasitism defined three origins of plant parasitism in the phylum Nematoda.…”

Section: Introductionmentioning

confidence: 99%

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Plant-parasitic nematodes: towards understanding molecular players in stress responses

Gillet

Bournaud

Júnior

et al. 2017

Ann Bot

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Background Plant–parasitic nematode interactions occur within a vast molecular plant immunity network. Following initial contact with the host plant roots, plant-parasitic nematodes (PPNs) activate basal immune responses. Defence priming involves the release in the apoplast of toxic molecules derived from reactive species or secondary metabolism. In turn, PPNs must overcome the poisonous and stressful environment at the plant–nematode interface. The ability of PPNs to escape this first line of plant immunity is crucial and will determine its virulence. Scope Nematodes trigger crucial regulatory cytoprotective mechanisms, including antioxidant and detoxification pathways. Knowledge of the upstream regulatory components that contribute to both of these pathways in PPNs remains elusive. In this review, we discuss how PPNs probably orchestrate cytoprotection to resist plant immune responses, postulating that it may be derived from ancient molecular mechanisms. The review focuses on two transcription factors, DAF-16 and SKN-1, which are conserved in the animal kingdom and are central regulators of cell homeostasis and immune function. Both regulate the unfolding protein response and the antioxidant and detoxification pathways. DAF-16 and SKN-1 target a broad spectrum of Caenorhabditis elegans genes coding for numerous protein families present in the secretome of PPNs. Moreover, some regulatory elements of DAF-16 and SKN-1 from C. elegans have already been identified as important genes for PPN infection. Conclusion DAF-16 and SKN-1 genes may play a pivotal role in PPNs during parasitism. In the context of their hub status and mode of regulation, we suggest alternative strategies for control of PPNs through RNAi approaches.

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Autophagy contributes to resistance to the oxidative stress induced by pine reactive oxygen species metabolism, promoting infection by Bursaphelenchus xylophilus

Liu

Lin

Feng

et al. 2020

Pest Management Science

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BACKGROUNDAutophagy plays an important role in eukaryotes. We investigated its role in the pine wood nematode (PWN), Bursaphelenchus xylophilus, the causative agent of pine wilt disease (PWD), to find promising control strategies against PWD.RESULTSWe analysed the expression levels of PtRBOH1 and PtRBOH2, which regulate reactive oxygen species (ROS) metabolism, in Pinus thunbergii and the expression of three autophagy genes, BxATG5, BxATG9 and BxATG16, in PWN by quantitative reverse transcription‐polymerase chain reaction (qRT‐PCR), and measured the content of H2O2, the main product of ROS metabolism, in pine stem. There was a correlation between the expression of autophagy genes in PWN and pine ROS metabolism during early infection. We also found that oxidative stress induces autophagy in PWN according to qRT‐PCR, transmission electron microscopy and Western blot analyses. Inhibition of autophagy by 3‐methyladenine or silencing of the autophagy genes BxATG9 and BxATG16 in PWN showed that autophagy is essential for feeding, fecundity, egg hatching and survival of PWN under oxidative stress, confirming the importance of autophagy in the antioxidant defences of PWN. Similarly, we demonstrated that autophagy contributes to the virulence of PWN. Moreover, PWN likely ameliorates oxidative damage by enhancing the activities of the peroxidase and catalase antioxidant pathways when autophagy is inhibited.CONCLUSIONAutophagy contributes to resistance to the oxidative stress induced by pine ROS metabolism, thus promoting infection by PWN. Our findings clarify the defence mechanisms of PWN and the pathogenesis of PWD, and provide promising hints for control of PWD by blocking autophagy. © 2020 Society of Chemical Industry

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Catalases Induction in High Virulence Pinewood Nematode Bursaphelenchus xylophilus under Hydrogen Peroxide-Induced Stress

Cited by 31 publications

References 35 publications

Bursaphelenchus xylophilus and B. mucronatus secretomes: a comparative proteomic analysis

Bursaphelenchus xylophilus and B. mucronatus secretomes: a comparative proteomic analysis

Plant-parasitic nematodes: towards understanding molecular players in stress responses

Autophagy contributes to resistance to the oxidative stress induced by pine reactive oxygen species metabolism, promoting infection by Bursaphelenchus xylophilus

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