Colleen E Fortier, Antonia E Musso, Maya L Evenden, L Irina Zaharia, Janice E K Cooke
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{"title":"Evidence that Ophiostomatoid Fungal Symbionts of Mountain Pine Beetle Do Not Play a Role in Overcoming Lodgepole Pine Defenses During Mass Attack.","authors":"Colleen E Fortier, Antonia E Musso, Maya L Evenden, L Irina Zaharia, Janice E K Cooke","doi":"10.1094/MPMI-06-23-0077-R","DOIUrl":null,"url":null,"abstract":"<p><p>Mountain pine beetle (MPB; <i>Dendroctonus ponderosae</i> Hopkins) is a devastating forest insect pest that has killed millions of hectares of pines in western North America over the past two decades. Like other bark beetles, MPB vectors ophiostomatoid fungal species, some of which are pathogenic to host pine species. The phytopathogenicity of these fungal symbionts has sparked considerable debate regarding their role in facilitating MPB attack success. We tested the hypothesis that MPB ophiostomatoid fungal associates like <i>Grosmannia clavigera</i> (Robinson-Jeffrey and Davidson) Zipfel, de Beer and Wingfield contribute to overwhelming host defenses during MPB mass attack. We compared responses of mature lodgepole pine (<i>Pinus contorta</i> Dougl. ex Loud. var. <i>latifolia</i> Engelm.) trees growing in natural stands that were mass attacked by MPB with those inoculated with <i>G. clavigera</i> by examining host defense hormones, secondary metabolites, and gene expression profiles. The jasmonate and ethylene signatures of necrotrophic pathogen-triggered response were identified in <i>G. clavigera</i>-inoculated trees, but only the jasmonate signature of a herbivore-triggered response was measured in MPB-attacked trees. Several <i>G. clavigera</i>-induced changes in pine phenolic metabolite profiles and phenolic biosynthesis gene expression patterns were absent in MPB-attacked pines. These findings indicate that ophiostomatoid fungi like <i>G. clavigera</i> are not a major factor in overwhelming host defenses during MPB mass attack. Instead, fungal pathogenicity likely is more important in aiding MPB colonization and development within the host tree. Phenolics appear to play a larger role in the host response to <i>G. clavigera</i> than to MPB, although phenolics may also influence MPB feeding and behavior. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.</p>","PeriodicalId":19009,"journal":{"name":"Molecular Plant-microbe Interactions","volume":" ","pages":"445-458"},"PeriodicalIF":3.2000,"publicationDate":"2024-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular Plant-microbe Interactions","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1094/MPMI-06-23-0077-R","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/5/22 0:00:00","PubModel":"Epub","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
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Abstract
Mountain pine beetle (MPB; Dendroctonus ponderosae Hopkins) is a devastating forest insect pest that has killed millions of hectares of pines in western North America over the past two decades. Like other bark beetles, MPB vectors ophiostomatoid fungal species, some of which are pathogenic to host pine species. The phytopathogenicity of these fungal symbionts has sparked considerable debate regarding their role in facilitating MPB attack success. We tested the hypothesis that MPB ophiostomatoid fungal associates like Grosmannia clavigera (Robinson-Jeffrey and Davidson) Zipfel, de Beer and Wingfield contribute to overwhelming host defenses during MPB mass attack. We compared responses of mature lodgepole pine (Pinus contorta Dougl. ex Loud. var. latifolia Engelm.) trees growing in natural stands that were mass attacked by MPB with those inoculated with G. clavigera by examining host defense hormones, secondary metabolites, and gene expression profiles. The jasmonate and ethylene signatures of necrotrophic pathogen-triggered response were identified in G. clavigera -inoculated trees, but only the jasmonate signature of a herbivore-triggered response was measured in MPB-attacked trees. Several G. clavigera -induced changes in pine phenolic metabolite profiles and phenolic biosynthesis gene expression patterns were absent in MPB-attacked pines. These findings indicate that ophiostomatoid fungi like G. clavigera are not a major factor in overwhelming host defenses during MPB mass attack. Instead, fungal pathogenicity likely is more important in aiding MPB colonization and development within the host tree. Phenolics appear to play a larger role in the host response to G. clavigera than to MPB, although phenolics may also influence MPB feeding and behavior. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.
有证据表明,山松甲虫的Ophiostomatoid真菌共生体在大规模侵袭过程中无法克服落叶松的防御能力。
山松甲虫(MPB;Dendroctonus ponderosae Hopkins)是一种毁灭性的森林害虫,在过去二十年里已造成北美西部数百万公顷松树死亡。与其他树皮甲虫一样,MPB 也传播对寄主松树物种具有致病性的表皮真菌。这些真菌共生体的植物致病性引发了关于它们在促进 MPB 攻击成功中所起作用的大量争论。我们测试了一种假设,即在 MPB 大规模攻击期间,MPB 的表生真菌伴生物(如 Grosmannia clavigera [Robinson-Jeffrey and Davidson] Zipfel、de Beer 和 Wingfield)有助于压倒宿主防御。我们通过研究宿主防御激素、次生代谢物和基因表达谱,比较了生长在受 MPB 大规模侵袭的自然林中的成熟落羽松(Pinus contorta Dougl.在接种了 G. clavigera 的树木中发现了坏死性病原体触发反应的茉莉酸盐和乙烯特征,但在受到 MPB 攻击的树木中只测出了食草动物触发反应的茉莉酸盐特征。在受到 MPB 攻击的松树中,G. clavigera 引起的松树酚类代谢物谱和酚类生物合成基因表达模式的几种变化都不存在。这些研究结果表明,在 MPB 大规模侵袭期间,像 G. clavigera 这样的表生真菌并不是压倒宿主防御系统的主要因素。相反,真菌的致病性可能对帮助 MPB 在寄主树上的定殖和发展更为重要。在宿主对 G. clavigera 的反应中,酚类物质的作用似乎大于 MPB,尽管酚类物质也可能影响 MPB 的取食和行为。
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