Genus-wide analysis of Trichoderma antagonism toward Pythium and Globisporangium plant pathogens and the contribution of cellulases to the antagonism

Author:

Chen Siqiao12ORCID,Daly Paul2ORCID,Anjago Wilfred Mabeche2,Wang Rong2,Zhao Yishen23,Wen Xian23,Zhou Dongmei2,Deng Sheng2,Lin Xisha4,Voglmeir Josef4,Cai Feng1ORCID,Shen Qirong1ORCID,Druzhinina Irina S.5ORCID,Wei Lihui2ORCID

Affiliation:

1. Key Lab of Organic-based Fertilizers of China and Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Nanjing Agricultural University, Nanjing, China

2. Key Lab of Food Quality and Safety of Jiangsu Province—State Key Laboratory Breeding Base, Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, China

3. College of Food and Bioengineering, Henan University of Science and Technology, Luoyang, China

4. Glycomics and Glycan Bioengineering Research Center (GGBRC), College of Food Science and Technology, Nanjing Agricultural University, Nanjing, China

5. Department of Accelerated Taxonomy, The Royal Botanic Gardens Kew, London, United Kingdom

Abstract

ABSTRACT Parasitism is an important lifestyle in the Trichoderma genus but has not been studied in a genus-wide way toward Pythium and Globisporangium hosts. Our approach screened a genus-wide set of 30 Trichoderma species in dual culture assays with two soil-borne Pythium and three Globisporangium plant-parasitic species and used exo-proteomic analyses, with the aim to correlate Trichoderma antagonism with potential strategies for attacking Pythium and Globisporangium . The Trichoderma spp. showed a wide range of antagonism from strong to weak, but the same Trichoderma strain showed similar levels toward all the Pythium and Globisporangium species. The Trichoderma enzymes from strong ( Trichoderma asperellum , Trichoderma atroviride , and Trichoderma virens ), moderate ( Trichoderma cf. guizhouense and Trichoderma reesei ), and weak ( Trichoderma parepimyces ) antagonists were induced by the autoclaved mycelia of one of the screened Pythium species, Pythium myriotylum . The variable proportions of putative cellulases, proteases, and redox enzymes suggested diverse as well as shared strategies amongst the antagonists. There was a partial positive correlation between antagonism from microscopy and the cellulase activity induced by autoclaved P. myriotylum mycelia in different Trichoderma species. The deletion of the cellulase transcriptional activator XYR1 in T. reesei led to lower antagonism toward Pythium and Globisporangium . The antagonism of Pythium and Globisporangium appears to be a generic property of Trichoderma as most of the Trichoderma species were at least moderately antagonistic. While a role for cellulases in the antagonism was uncovered, cellulases did not appear to make a major contribution to T. reesei antagonism, and other factors are also likely contributing. IMPORTANCE Trichoderma is an important genus widely distributed in nature with broad ecological impacts and applications in the biocontrol of plant diseases. The Pythium and Globisporangium genera of fungus-like water molds include many important soil-borne plant pathogens that cause various diseases. Most of the Trichoderma species showed at least a moderate ability to compete with or antagonize the Pythium and Globisporangium hosts, and microscopy showed examples of parasitism (a slow type of killing) and predation (a fast type of killing). Hydrolytic enzymes such as cellulases and proteases produced by Trichoderma likely contribute to the antagonism. A mutant deficient in cellulase activity had reduced antagonism. Interestingly, Pythium and Globisporangium species contain cellulose in their cell walls (unlike true fungi such as Trichoderma ), and the cellulolytic ability of Trichoderma appears beneficial for antagonism of water molds.

Funder

China Agricultural Research System

Jiangsu Agricultural Science and Technology Innovation Fund

MOST | National Natural Science Foundation of China

Publisher

American Society for Microbiology

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