Dataset Information

Two Verticillium dahliae MAPKKKs, VdSsk2 and VdSte11, Have Distinct Roles in Pathogenicity, Microsclerotial Formation, and Stress Adaptation.

ABSTRACT: Verticillium dahliae causes destructive vascular wilt diseases on more than 200 plant species, including economically important crops and ornamental trees worldwide. The melanized microsclerotia enable the fungus to survive for years in soil and are crucial for its disease cycle. Previously, we found that the VdPbs2-VdHog1 (V. dahliae Pbs2-V. dahliae Hog1) module plays key roles in microsclerotial formation, stress responses, and virulence in V. dahliae In this study, two mitogen-activated protein kinase kinase kinases (MAPKKKs) homologous to Ssk2p and Ste11p, which activate the Pbs2p-Hog1p module by phosphorylation in budding yeast, were identified in the genome of V. dahliae Both ?VdSsk2 (V. dahliae Ssk2) and ?VdSte11 strains showed severe defects in microsclerotial formation and melanin biosynthesis, but the relative importance of these two genes in microsclerotial development was different. Deletion of VdSsk2, but not VdSte11, affected responses to osmotic stress, fungicidal response, and cell wall stressors. The ?VdSsk2 strain exhibited a significant reduction in virulence, while the ?VdSte11 strain was nonpathogenic due to failure to penetrate and form hyphopodia. Phosphorylation assays demonstrated that VdSsk2, but not VdSte11, can phosphorylate VdHog1 in V. dahliae Moreover, VdCrz1, encoding a calcineurin-responsive zinc finger transcription factor and a key regulator of calcium signaling in fungi, was misregulated in the ?VdSsk2, ?VdPbs2, and ?VdHog1 mutants.IMPORTANCE These data provide insights into the distinctive functions of VdSsk2 and VdSte11 in pathogenicity, stress adaptation, and microsclerotial formation in V. dahliae.

SUBMITTER: Yu J

PROVIDER: S-EPMC6620378 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Two Verticillium dahliae MAPKKKs, VdSsk2 and VdSte11, Have Distinct Roles in Pathogenicity, Microsclerotial Formation, and Stress Adaptation.

Yu Jun J Li Tianyu T Tian Longyan L Tang Chen C Klosterman Steven J SJ Tian Chengming C Wang Yonglin Y

mSphere 20190710 4

Verticillium dahliae causes destructive vascular wilt diseases on more than 200 plant species, including economically important crops and ornamental trees worldwide. The melanized microsclerotia enable the fungus to survive for years in soil and are crucial for its disease cycle. Previously, we found that the VdPbs2-VdHog1 (V. dahliae Pbs2-V. dahliae Hog1) module plays key roles in microsclerotial formation, stress responses, and virulence in V. dahliae In this study, ...[more]

PMID: 31292234

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Project description:IntroductionVerticillium wilt (VW) caused by Verticillium dahliae is a soil-borne vascular fungal disease that severely affects cotton yield and fiber quality. Sugar metabolism plays an important role in the growth and pathogenicity of V. dahliae. However, limited information is known about the sugar transporter genes and their roles in the growth and pathogenicity of V. dahliae.MethodIn this study, genome-wide identification of sugar transporter genes in V. dahliae was conducted and the expression profiles of these genes in response to root exudates from cotton varieties susceptible or resistant to V. dahliae were investigated based on RNA-seq data. Tobacco Rattle Virus-based host-induced gene silencing (TRV-based HIGS) and artificial small interfering RNAs (asiRNAs) were applied to investigate the function of candidate genes involved in the growth and pathogenic process of V. dahliae.ResultsA total of 65 putative sugar transporter genes were identified and clustered into 8 Clades. Of the 65 sugar transporter genes, 9 were found to be induced only by root exudates from the susceptible variety, including VdST3 and VdST12 that were selected for further functional study. Silencing of VdST3 or VdST12 in host plants by TRV-based HIGS reduced fungal biomass and enhanced cotton resistance against V. dahliae. Additionally, silencing of VdST12 and VdST3 by feeding asiRNAs targeting VdST12 (asiR815 or asiR1436) and VdST3 (asiR201 or asiR1238) inhibited fungal growth, exhibiting significant reduction in hyphae and colony diameter, with a more significant effect observed for the asiRNAs targeting VdST12. The inhibitory effect of asiRNAs on the growth of V. dahliae was enhanced with the increasing concentration of asiRNAs. Silencing of VdST12 by feeding asiR815+asiR1436 significantly decreased the pathogenicity of V. dahliae.DiscussionThe results suggest that VdST3 and VdST12 are sugar transporter genes required for growth and pathogenicity of V. dahliae and that asiRNA is a valuable tool for functional characterization of V. dahliae genes.

Project description:The initial interaction of a pathogenic fungus with its host is complex and involves numerous metabolic pathways and regulatory proteins. Considerable attention has been devoted to proteins that play a crucial role in these interactions, with an emphasis on so-called effector molecules that are secreted by the invading microbe to establish the symbiosis. However, the contribution of other types of molecules, such as glycans, is less well appreciated. Here, we present a random genetic screen that enabled us to identify 58 novel candidate genes that are involved in the pathogenic potential of the fungal pathogen Verticillium dahliae, which causes vascular wilt diseases in over 200 dicotyledonous plant species, including economically important crops. One of the candidate genes that was identified concerns a putative biosynthetic gene involved in nucleotide sugar precursor formation, as it encodes a putative nucleotide-rhamnose synthase/epimerase-reductase (NRS/ER). This enzyme has homology to bacterial enzymes involved in the biosynthesis of the nucleotide sugar deoxy-thymidine diphosphate (dTDP)-rhamnose, a precursor of L-rhamnose, which has been shown to be required for virulence in several human pathogenic bacteria. Rhamnose is known to be a minor cell wall glycan in fungi and has therefore not been suspected as a crucial molecule in fungal-host interactions. Nevertheless, our study shows that deletion of the VdNRS/ER gene from the V. dahliae genome results in complete loss of pathogenicity on tomato and Nicotiana benthamiana plants, whereas vegetative growth and sporulation are not affected. We demonstrate that VdNRS/ER is a functional enzyme in the biosynthesis of uridine diphosphate (UDP)-rhamnose, and further analysis has revealed that VdNRS/ER deletion strains are impaired in the colonization of tomato roots. Collectively, our results demonstrate that rhamnose, although only a minor cell wall component, is essential for the pathogenicity of V. dahliae.

Dataset Information

Two Verticillium dahliae MAPKKKs, VdSsk2 and VdSte11, Have Distinct Roles in Pathogenicity, Microsclerotial Formation, and Stress Adaptation.

Publications

Two Verticillium dahliae MAPKKKs, VdSsk2 and VdSte11, Have Distinct Roles in Pathogenicity, Microsclerotial Formation, and Stress Adaptation.

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