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Role of Dicer-Dependent RNA Interference in Regulating Mycoparasitic Interactions

Piombo, Edoardo and Vetukuri, Ramesh and Broberg, Anders and Kalyandurg, Pruthvi Balachandra and Kushwaha, Sandeep Kumar and Jensen, Dan Funck and Karlsson, Magnus and Dubey, Mukesh (2021). Role of Dicer-Dependent RNA Interference in Regulating Mycoparasitic Interactions. . 9 , e01099-21
[Research article]

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Abstract

Dicer-like proteins (DCLs) play a vital role in RNA interference (RNAi), by cleaving RNA filament into small RNAs. Although DCL-mediated RNAi can regulate interspecific communication between pathogenic/mutualistic organisms and their hosts, its role in mycoparasitic interactions is yet to be investigated. In this study, we deleted dcl genes in the mycoparasitic fungus Clonostachys rosea and characterize the functions of DCL-dependent RNAi in mycoparasitism. Deletion of dcl2 resulted in a mutant with reduced secondary metabolite production, antagonism toward the plant-pathogenic fungus Botrytis cinerea, and reduced ability to control Fusarium foot rot disease on wheat, caused by Fusarium graminearum. Transcriptome sequencing of the in vitro interaction between the C. rosea Delta dcl2 strain and B. cinerea or F. graminearum identified the downregulation of genes coding for transcription factors, membrane transporters, hydrolytic enzymes, and secondary metabolites biosynthesis enzymes putatively involved in antagonistic interactions, in comparison with the C. rosea wild-type interaction. A total of 61 putative novel microRNA-like RNAs (milRNAs) were identified in C. rosea, and 11 were downregulated in the Delta dcl2 mutant. In addition to putative endogenous gene targets, these milRNAs were predicted to target B. cinerea and F. graminearum virulence factor genes, which showed an increased expression during interaction with the Delta dcl2 mutant incapable of producing the targeting milRNAs. In summary, this study constitutes the first step in elucidating the role of RNAi in mycoparasitic interactions, with important implications for biological control of plant diseases, and poses the base for future studies focusing on the role of cross-species RNAi regulating mycoparasitic interactions.IMPORTANCE Small RNAs mediated RNA interference (RNAi) known to regulate several biological processes. Dicer-like endoribonucleases (DCLs) play a vital role in the RNAi pathway by generating sRNAs. In this study, we investigated a role of DCL-mediated RNAi in interference interactions between mycoparasitic fungus Clonostachys rosea and the two fungal pathogens Botrytis cinerea and Fusarium graminearum (here called mycohosts). We found that the dcl mutants were not able to produce 11 sRNAs predicted to finetune the regulatory network of genes known to be involved in production of hydrolytic enzymes, antifungal compounds, and membrane transporters needed for antagonistic action of C. rosea. We also found C. rosea sRNAs putatively targeting known virulence factors in the mycohosts, indicating RNAi-mediated cross-species communication. Our study expanded the understanding of underlying mechanisms of cross-species communication during interference interactions and poses a base for future works studying the role of DCL-based cross-species RNAi in fungal interactions.

Authors/Creators:Piombo, Edoardo and Vetukuri, Ramesh and Broberg, Anders and Kalyandurg, Pruthvi Balachandra and Kushwaha, Sandeep Kumar and Jensen, Dan Funck and Karlsson, Magnus and Dubey, Mukesh
Title:Role of Dicer-Dependent RNA Interference in Regulating Mycoparasitic Interactions
Year of publishing :2021
Volume:9
Article number:e01099-21
Number of Pages:31
Publisher:AMER SOC MICROBIOLOGY
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Microbiology (Microbiology in the medical area to be 30109)
Keywords:antagonism, biocontrol, Clonostachys rosea, gene regulation, mycoparasitism, RNA interference, small RNA
URN:NBN:urn:nbn:se:slu:epsilon-p-115201
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-115201
Additional ID:
Type of IDID
DOI10.1128/Spectrum.01099-21
Web of Science (WoS)000728629300151
ID Code:26675
Faculty:NJ - Fakulteten för naturresurser och jordbruksvetenskap
LTV - Fakulteten för landskapsarkitektur, trädgårds- och växtproduktionsvetenskap
Department:(NL, NJ) > Dept. of Forest Mycology and Plant Pathology
(S) > Dept. of Forest Mycology and Plant Pathology

(LTJ, LTV) > Department of Plant Breeding (from 130101)
(NL, NJ) > Department of Molecular Sciences
Deposited By: SLUpub Connector
Deposited On:10 Jan 2022 15:25
Metadata Last Modified:10 Jan 2022 15:31

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