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Transcriptomic Analysis of Trichoderma atroviride Overgrowing Plant-Wilting Verticillium dahliae Reveals the Role of a New M14 Metallocarboxypeptidase CPA1 in Biocontrol.

ABSTRACT: Verticillium dahliae, a vascular-colonizing fungus, causes economically important wilt diseases in many crops, including olive trees. Trichoderma spp. have demonstrated an effective contribution as biocontrol agents against this pathogen through a variety of mechanisms that may involve direct mycoparasitism and antibiosis. However, molecular aspects underlaying Trichoderma-V. dahliae interactions are not well known yet due to the few studies in which this pathogen has been used as a target for Trichoderma. In the present study, Trichoderma atroviride T11 overgrew colonies of V. dahliae on agar plates and inhibited growth of highly virulent defoliating (D) V. dahliae V-138I through diffusible molecules and volatile organic compounds produced before contact. A Trichoderma microarray approach of T11 growing alone (CON), and before contact (NV) or overgrowing (OV) colonies of V-138I, helped to identify 143 genes that differed significantly in their expression level by more than twofold between OV and CON or NV. Functional annotation of these genes indicated a marked up-regulation of hydrolytic, catalytic and transporter activities, and secondary metabolic processes when T11 overgrew V-138I. This transcriptomic analysis identified peptidases as enzymatic activity overrepresented in the OV condition, and the cpa1 gene encoding a putative carboxypeptidase (ID number 301733) was selected to validate this study. The role of cpa1 in strain T11 on antagonism of V-138I was analyzed by a cpa1-overexpression approach. The increased levels of cpa1 expression and protease activity in the cpa1-overexpressed transformants compared to those in wild-type or transformation control strains were followed by significantly higher antifungal activity against V-138I in in vitro assays. The use of Trichoderma spp. for the integrated management of plant diseases caused by V. dahliae requires a better understanding of the molecular mechanisms underlying this interaction that might provide an increase on its efficiency.

SUBMITTER: Moran-Diez ME

PROVIDER: S-EPMC6545926 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Anthracnose disease is a serious threat to red pepper crops in Korea and many other countries, resulting in considerable yield losses. There are now no effective control techniques available except for fungicide sprays, which may directly impact consumers. This study aims to investigate the biological activity of Trichoderma isolates in controlling red pepper anthracnose caused by Colletotrichum acutatum in vitro and in the field. Out of 11 Trichoderma isolates screened for biocontrol agents against three fungal pathogens, including C. acutatum; two effective Trichoderma isolates, T. atroviride ATR697 (ATR697) and T. longibrachiatum LON701 (LON701) were selected for further investigation. Using the overlapping plates experiment, it was discovered that the volatile organic compounds (VOCs) produced by ATR697 strongly inhibited C. acutatum mycelial growth to a larger extent than the isolate LON701. A cellophane membrane experiment has shown that mycelial growth of C. acutatum was inhibited by 36% and 27% when treated with ATR697 and LON701, respectively. Culture filtrates (CFs) of two Trichoderma isolates inhibited the mycelial growth of C. acutatum in vitro. When red peppers were treated with spore suspensions of LON701 and ATR697, the disease severity (%) was 44.1% and 55.8%, respectively, in a curative method; while the disease severity (%) was 5% and 11.6%, in LON701- and ATR697-treated red peppers, respectively, in a preventive method. These results showed the suppression of disease severity (%) was relatively higher in the preventive method than in the curative method. Furthermore, Trichoderma isolates ATR697 and LON701 were resistant to commercial chemical fungicides in vitro, indicating these strains may also be used synergistically with a chemical fungicide (pyraclostrobin) against the growth of C. acutatum. There was no difference in the inhibition rate (%) of the pathogen between the treatment with LON701 alone and LON701+pyraclostrobin. Based on in vitro findings, ATR697 and LON701 played a role in effectively controlling red pepper anthracnose in field conditions, with LON701 treatment resulting in a disease rate of 14% when compared to ATR697, chemical, and non-treated controls. Overall, our study showed the ability of Trichoderma isolates to control red pepper anthracnose and their potential to develop as novel biocontrol agents to replace chemical fungicides for eco-friendly, sustainable agriculture.

Project description:BACKGROUND:Cotton Verticillium wilt is one of the most devastating diseases for cotton production in the world. Although this diseases have been widely studied at the molecular level from pathogens, the molecular basis of V. dahliae interacted with cotton has not been well examined. RESULTS:In this study, RNA-seq analysis was carried out on V. dahliae samples cultured by different root exudates from three cotton cultivars (a susceptible upland cotton cultivar, a tolerant upland cotton cultivar and a resistant island cotton cultivar) and water for 0?h, 6?h, 12?h, 24?h and 48?h. Statistical analysis of differentially expressed genes revealed that V. dahliae responded to all kinds of root exudates but more strongly to susceptible cultivar than to tolerant and resistant cultivars. Go analysis indicated that 'hydrolase activity, hydrolyzing O-glycosyl compounds' related genes were highly enriched in V. dahliae cultured by root exudates from susceptible cotton at early stage of interaction, suggesting genes related to this term were closely related to the pathogenicity of V. dahliae. Additionally, 'transmembrane transport', 'coenzyme binding', 'NADP binding', 'cofactor binding', 'oxidoreductase activity', 'flavin adenine dinucleotide binding', 'extracellular region' were commonly enriched in V. dahliae cultured by all kinds of root exudates at early stage of interaction (6?h and 12?h), suggesting that genes related to these terms were required for the initial steps of the roots infections. CONCLUSIONS:Based on the GO analysis results, the early stage of interaction (6?h and 12?h) were considered as the critical stage of V. dahliae-cotton interaction. Comparative transcriptomic analysis detected that 31 candidate genes response to root exudates from cotton cultivars with different level of V. dahliae resistance, 68 response to only susceptible cotton cultivar, and 26 genes required for development of V. dahliae. Collectively, these expression data have advanced our understanding of key molecular events in the V. dahliae interacted with cotton, and provided a framework for further functional studies of candidate genes to develop better control strategies for the cotton wilt disease.

Dataset Information

Transcriptomic Analysis of Trichoderma atroviride Overgrowing Plant-Wilting Verticillium dahliae Reveals the Role of a New M14 Metallocarboxypeptidase CPA1 in Biocontrol.

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