A <i>Verticillium dahliae</i> Extracellular Cutinase Modulates Plant Immune Responses

Gui, Yue-Jing; Zhang, Wenqi; Zhang, Dandan; Zhou, Lei; Short, Dylan P. G.; Wang, Jie; Ma, Xuefeng; Li, Ting‐Gang; Kong, Zwe‐Ling; Wang, Baoli; Wang, Dan; Li, Nan‐Yang; Subbarao, Krishna V.; Chen, Jie‐Yin; Dai, Xiaofeng

doi:10.1094/mpmi-06-17-0136-r

Cited by 50 publications

(77 citation statements)

References 95 publications

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“…In our previous study, we found that V. dahliae can deliver the effector VdCBM1, a protein that also contains four cysteine residues and is a secreted SCP that suppresses PTI (Gui et al , ). VdCBM1 can also suppress the immunity triggered by damage‐associated molecular patterns (DAMPs), including the products from VdCUT11 (Gui et al , ). In this study, we rediscovered that the immunity triggered by VdSCPs in a BAK1/SOBIR1‐dependent manner is also suppressed by VdCBM1 (Figures and ).…”

Section: Discussionmentioning

confidence: 99%

“…In Phytophthora sojae , glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP (Ma et al ., ), and so are VdEG1 and VdEG3 from V. dahliae (Gui et al , ), suggesting that VdSCP27 and VdSCP126 function in virulence, although they also may be recognized by the host plants to induce immunity. Some fungal effectors are often considered dispensable for virulence due to functional or quantitative redundancy (Sharpee and Dean, ), as many PAMPs have been found in V. dahliae (de Jonge et al , ; Zhou et al , ; Santhanam et al , ; Gui et al , ; ) and deletion of VdSCP113 singly perhaps is unable to alter the pathogen virulence. Another hypothesis is that the effectors initially function in virulence and subsequently are recognized by the host to induce immunity as a result of a long coevolutionary arms race, thereby also forcing a dual role during host–pathogen interactions.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies have shown that secreted proteins probably play a critical role in the pathogenesis of V. dahliae (Fradin and Thomma, ; Chu et al , ; Chen et al , ; ; Zhang et al , ), and the function or the activity of several secreted proteins have been elucidated (de Sain and Rep, ; Klimes et al , ; Wang et al , ; Zhang et al , ). Similar to the mechanisms discovered in other phytopathogens, V. dahliae secretes proteins to manipulate host immunity during infection (de Jonge et al , ; Zhou et al , ; Santhanam et al , ; Liu et al , ; Gui et al , , ; Kombrink et al , ; Zhang et al , ; Qin et al , ). Many of these effectors are relatively small and enriched in cysteine residues, including Ave1, VdCBM1, and VdSCP7 (VDAG_07157) (de Jonge et al , ; Gui et al , ; Zhang et al , ).…”

Section: Introductionmentioning

confidence: 89%

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Functional analyses of small secreted cysteine‐rich proteins identified candidate effectors in Verticillium dahliae

Wang

Tian

Zhang

et al. 2020

Molecular Plant Pathology

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Secreted small cysteine-rich proteins (SCPs) play a critical role in modulating host immunity in plant-pathogen interactions. Bioinformatic analyses showed that the fungal pathogen Verticillium dahliae encodes more than 100 VdSCPs, but their roles in host-pathogen interactions have not been fully characterized. Transient expression of 123 VdSCP-encoding genes in Nicotiana benthamiana identified three candidate genes involved in host-pathogen interactions. The expression of these three proteins, VdSCP27, VdSCP113, and VdSCP126, in N. benthamiana resulted in cell death accompanied by a reactive oxygen species burst, callose deposition, and induction of defence genes. The three VdSCPs mainly localized to the periphery of the cell. BAK1 and SOBIR1 (associated with receptor-like protein) were required for the immunity triggered by these three VdSCPs in N. benthamiana. Site-directed mutagenesis showed that cysteine residues that form disulphide bonds are essential for the functioning of VdSCP126, but not VdSCP27 and VdSCP113. VdSCP27, VdSCP113, and VdSCP126 individually are not essential for V. dahliae infection of N. benthamiana and Gossypium hirsutum, although there was a significant reduction of virulence on N. benthamiana and G. hirsutum when inoculated with the VdSCP27/VdSCP126 double deletion strain.These results illustrate that the SCPs play a critical role in the V. dahliae-plant interaction via an intrinsic virulence function and suppress immunity following infection.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 89%

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Functional analyses of small secreted cysteine‐rich proteins identified candidate effectors in Verticillium dahliae

Wang

Tian

Zhang

et al. 2020

Molecular Plant Pathology

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“…In this study, diversity hot spots were identified in the cutinase amino acid sequence when 200 fungal species were compared and this could be explained by divergent evolution allowing different functions of cutinase enzyme in plant pathogenic fungi. Gui et al () conducted functional analysis of 13 cutinase genes (VdCUTs) and found significant sequence divergence in cutinase family members in the genome of Verticillium dahliae Vd991.…”

Section: Discussionmentioning

confidence: 99%

Diversity, structure, and synteny of the cutinase gene ofColletotrichumspecies

Villafana

Rampersad

2020

Ecology and Evolution

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Colletotrichum species complexes are among the top 10 economically important fungal plant pathogens worldwide because they can infect climacteric and nonclimacteric fruit at the pre and/or postharvest stages. C. truncatum is the major pathogen responsible for anthracnose of green and red bell pepper fruit worldwide. C. brevisporum was recently reported to be a minor pathogen of red bell pepper fruit in Trinidad, but has recently been reported as pathogenic to other host species in other countries. The ability of these phytopathogens to produce and secrete cutinase is required for dismantling the cuticle of the host plant and, therefore, crucial to the necrotrophic phase of their infection strategy. In vitro bioassays using different lipid substrates confirmed the ability of C. truncatum and C. brevisporum isolates from green and red bell peppers to secrete cutinase. The diversity, structure and organization and synteny of the cutinase gene were determined among different Colletotrichum species. Cluster analysis indicated a low level of nucleotide variation among C. truncatum sequences. Nucleotide sequences of C. brevisporum were more related to C. truncatum cutinase nucleotide sequences than to C. gloeosporioides. Cluster patterns coincided with haplotype and there was evidence of significant positive selection with no recombination signatures. The structure of the cutinase gene included two exons with one intervening intron and, therefore, one splice variant. Although amino acid sequences were highly conserved among C. truncatum isolates, diversity “hot spots” were revealed when the 66‐amino acid coding region of 200 fungal species was compared. Twenty cutinase orthologues were detected among different fungal species, whose common ancestor is Pezizomycotina and it is purported that these orthologues arose through a single gene duplication event prior to speciation. The cutinase domain was retained both in structure and arrangement among 34 different Colletotrichum species. The order of aligned genomic blocks between species and the arrangement of flanking protein domains were also conserved and shared for those domains immediately located at the N‐ and C‐terminus of the cutinase domain. Among these were an RNA recognition motif, translation elongation factor, signal peptide, pentatricopeptide repeat, and Hsp70 family of chaperone proteins, all of which support the expression of the cutinase gene. The findings of this study are important to understanding the evolution of the cutinase gene in C. truncatum as a key component of the biotrophic–necrotrophic switch which may be useful in developing gene‐targeting strategies to decrease the pathogenic potential of Colletotrichum species.

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“…In order to successfully invade into host plant, plant pathogenic fungi are expected to produce and secrete multiple extracellular degrading enzymes such as cutinase for the degradation of cuticle [33], cell wall degrading enzymes (pectinase, cellulase and hemicellulase) [34], and cytomembrane and cell inclusion degrading enzymes (protease and lipase) [35,36]. 9 cutinases were identified both in HGCC, CCP and UM591 genomes (Table S1).…”

Section: Protein Families Involved In Degrading Plant Cuticle Cell Wmentioning

confidence: 99%

Genome sequence and spore germination associated transcriptome analysis of Corynespora cassiicola from cucumber

Gao

Zeng

Suo

et al. 2019

Preprint

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Corynespora cassiicola as a necrotrophic plant pathogenic ascomycetes fungus can infect hundreds of species of plants, and also rarely cause human disease. The pathogen infects cucumber and causes cucumber target spot, which has given rise to great yield loss of cucumber in China recently. Genome sequence and spore germination associated transcriptome analysis will contribute to the understanding of the molecular mechanism of pathogenicity and spore germination of C. cassiicola .Results Firstly, we reported the draft genome sequences of a cucumber-sampled C. cassiicola isolate HGCC with high virulence. Although being conspecific, HGCC had distinct difference with a rubber-sampled isolate (CCP) and a human-sampled isolate (UM591) in genome sequences. The proportion of secreted proteins was 7.4% in HGCC. 28.6% of HGCC predicted genes were highly homologous to experimentally proven virulence-associated genes, which was close to that in CCP, UM591 and some plant fungal pathogens, but far more than 21.9% in Phaeosphaeria nodorum and 19.6% in Botrytis cinerea . Thousands of putative virulence-associated genes in various pathways or families were identified in HGCC. Secondly, a global view of the transcriptome of C. cassiicola spores during germination was evaluated using RNA sequencing (RNA-seq). A total of 3,288 differentially expressed genes (DEGs) were identified. The majority of KEGG annotated DEGs were involved in metabolism, genetic information processing, cellular processes, organismal system, human diseases and environmental information processing.Conclusions These results not only facilitated the exploration of the molecular pathogenic mechanism of C. cassiicola to cucumber and the understanding of molecular and cellular processes during spore germination, but also laid the foundation for the disease control.

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A Verticillium dahliae Extracellular Cutinase Modulates Plant Immune Responses

Cited by 50 publications

References 95 publications

Functional analyses of small secreted cysteine‐rich proteins identified candidate effectors in Verticillium dahliae

Functional analyses of small secreted cysteine‐rich proteins identified candidate effectors in Verticillium dahliae

Diversity, structure, and synteny of the cutinase gene ofColletotrichumspecies

Genome sequence and spore germination associated transcriptome analysis of Corynespora cassiicola from cucumber

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