A DNase from a Fungal Phytopathogen Is a Virulence Factor Likely Deployed as Counter Defense against Host-Secreted Extracellular DNA

ABSTRACT Histone-linked extracellular DNA (exDNA) is a component of neutrophil extracellular traps (NETs). NETs have been shown to play a role in immune response to bacteria, fungi, viruses, and protozoan parasites. Mutation of genes encoding group A Streptococcus extracellular DNases (exDNases) res...

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Autores principales:	Hee-Jin Park, Weiwei Wang, Gilberto Curlango-Rivera, Zhongguo Xiong, Zeran Lin, David A. Huskey, Martha C. Hawes, Hans D. VanEtten, B. Gillian Turgeon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	NETs extracellular DNA fungi virulence determinants Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/abab718eb8294da5b920b98073c95b7e
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spelling	oai:doaj.org-article:abab718eb8294da5b920b98073c95b7e2021-11-15T15:55:26ZA DNase from a Fungal Phytopathogen Is a Virulence Factor Likely Deployed as Counter Defense against Host-Secreted Extracellular DNA10.1128/mBio.02805-182150-7511https://doaj.org/article/abab718eb8294da5b920b98073c95b7e2019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02805-18https://doaj.org/toc/2150-7511ABSTRACT Histone-linked extracellular DNA (exDNA) is a component of neutrophil extracellular traps (NETs). NETs have been shown to play a role in immune response to bacteria, fungi, viruses, and protozoan parasites. Mutation of genes encoding group A Streptococcus extracellular DNases (exDNases) results in reduced virulence in animals, a finding that implies that exDNases are deployed as counter defense against host DNA-containing NETs. Is the exDNA/exDNase mechanism also relevant to plants and their pathogens? It has been demonstrated previously that exDNA is a component of a matrix secreted from plant root caps and that plants also carry out an extracellular trapping process. Treatment with DNase I destroys root tip resistance to infection by fungi, the most abundant plant pathogens. We show that the absence of a single gene encoding a candidate exDNase results in significantly reduced virulence of a fungal plant pathogen to its host on leaves, the known infection site, and on roots. Mg2+-dependent exDNase activity was demonstrated in fungal culture filtrates and induced when host leaf material was present. It is speculated that the enzyme functions to degrade plant-secreted DNA, a component of a complex matrix akin to neutrophil extracellular traps of animals. IMPORTANCE We document that the absence of a single gene encoding a DNase in a fungal plant pathogen results in significantly reduced virulence to a plant host. We compared a wild-type strain of the maize pathogen Cochliobolus heterostrophus and an isogenic mutant lacking a candidate secreted DNase-encoding gene and demonstrated that the mutant is reduced in virulence on leaves and on roots. There are no previous reports of deletion of such a gene from either an animal or plant fungal pathogen accompanied by comparative assays of mutants and wild type for alterations in virulence. We observed DNase activity, in fungal culture filtrates, that is Mg2+ dependent and induced when plant host leaf material is present. Our findings demonstrate not only that fungi use extracellular DNases (exDNases) for virulence, but also that the relevant molecules are deployed in above-ground leaves as well as below-ground plant tissues. Overall, these data provide support for a common defense/counter defense virulence mechanism used by animals, plants, and their fungal and bacterial pathogens and suggest that components of the mechanism might be novel targets for the control of plant disease.Hee-Jin ParkWeiwei WangGilberto Curlango-RiveraZhongguo XiongZeran LinDavid A. HuskeyMartha C. HawesHans D. VanEttenB. Gillian TurgeonAmerican Society for MicrobiologyarticleNETsextracellular DNAfungivirulence determinantsMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	NETs extracellular DNA fungi virulence determinants Microbiology QR1-502
spellingShingle	NETs extracellular DNA fungi virulence determinants Microbiology QR1-502 Hee-Jin Park Weiwei Wang Gilberto Curlango-Rivera Zhongguo Xiong Zeran Lin David A. Huskey Martha C. Hawes Hans D. VanEtten B. Gillian Turgeon A DNase from a Fungal Phytopathogen Is a Virulence Factor Likely Deployed as Counter Defense against Host-Secreted Extracellular DNA
description	ABSTRACT Histone-linked extracellular DNA (exDNA) is a component of neutrophil extracellular traps (NETs). NETs have been shown to play a role in immune response to bacteria, fungi, viruses, and protozoan parasites. Mutation of genes encoding group A Streptococcus extracellular DNases (exDNases) results in reduced virulence in animals, a finding that implies that exDNases are deployed as counter defense against host DNA-containing NETs. Is the exDNA/exDNase mechanism also relevant to plants and their pathogens? It has been demonstrated previously that exDNA is a component of a matrix secreted from plant root caps and that plants also carry out an extracellular trapping process. Treatment with DNase I destroys root tip resistance to infection by fungi, the most abundant plant pathogens. We show that the absence of a single gene encoding a candidate exDNase results in significantly reduced virulence of a fungal plant pathogen to its host on leaves, the known infection site, and on roots. Mg2+-dependent exDNase activity was demonstrated in fungal culture filtrates and induced when host leaf material was present. It is speculated that the enzyme functions to degrade plant-secreted DNA, a component of a complex matrix akin to neutrophil extracellular traps of animals. IMPORTANCE We document that the absence of a single gene encoding a DNase in a fungal plant pathogen results in significantly reduced virulence to a plant host. We compared a wild-type strain of the maize pathogen Cochliobolus heterostrophus and an isogenic mutant lacking a candidate secreted DNase-encoding gene and demonstrated that the mutant is reduced in virulence on leaves and on roots. There are no previous reports of deletion of such a gene from either an animal or plant fungal pathogen accompanied by comparative assays of mutants and wild type for alterations in virulence. We observed DNase activity, in fungal culture filtrates, that is Mg2+ dependent and induced when plant host leaf material is present. Our findings demonstrate not only that fungi use extracellular DNases (exDNases) for virulence, but also that the relevant molecules are deployed in above-ground leaves as well as below-ground plant tissues. Overall, these data provide support for a common defense/counter defense virulence mechanism used by animals, plants, and their fungal and bacterial pathogens and suggest that components of the mechanism might be novel targets for the control of plant disease.
format	article
author	Hee-Jin Park Weiwei Wang Gilberto Curlango-Rivera Zhongguo Xiong Zeran Lin David A. Huskey Martha C. Hawes Hans D. VanEtten B. Gillian Turgeon
author_facet	Hee-Jin Park Weiwei Wang Gilberto Curlango-Rivera Zhongguo Xiong Zeran Lin David A. Huskey Martha C. Hawes Hans D. VanEtten B. Gillian Turgeon
author_sort	Hee-Jin Park
title	A DNase from a Fungal Phytopathogen Is a Virulence Factor Likely Deployed as Counter Defense against Host-Secreted Extracellular DNA
title_short	A DNase from a Fungal Phytopathogen Is a Virulence Factor Likely Deployed as Counter Defense against Host-Secreted Extracellular DNA
title_full	A DNase from a Fungal Phytopathogen Is a Virulence Factor Likely Deployed as Counter Defense against Host-Secreted Extracellular DNA
title_fullStr	A DNase from a Fungal Phytopathogen Is a Virulence Factor Likely Deployed as Counter Defense against Host-Secreted Extracellular DNA
title_full_unstemmed	A DNase from a Fungal Phytopathogen Is a Virulence Factor Likely Deployed as Counter Defense against Host-Secreted Extracellular DNA
title_sort	dnase from a fungal phytopathogen is a virulence factor likely deployed as counter defense against host-secreted extracellular dna
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/abab718eb8294da5b920b98073c95b7e
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A DNase from a Fungal Phytopathogen Is a Virulence Factor Likely Deployed as Counter Defense against Host-Secreted Extracellular DNA

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