Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.

Plants evoke innate immunity against microbial challenges upon recognition of pathogen-associated molecular patterns (PAMPs), such as fungal cell wall chitin. Nevertheless, pathogens may circumvent the host PAMP-triggered immunity. We previously reported that the ascomycete Magnaporthe oryzae, a fam...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Takashi Fujikawa, Ayumu Sakaguchi, Yoko Nishizawa, Yusuke Kouzai, Eiichi Minami, Shigekazu Yano, Hironori Koga, Tetsuo Meshi, Marie Nishimura
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2012
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/9c64c8f54487495abd2c6909008ac357
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:9c64c8f54487495abd2c6909008ac357
record_format	dspace
spelling	oai:doaj.org-article:9c64c8f54487495abd2c6909008ac3572021-11-18T06:04:02ZSurface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.1553-73661553-737410.1371/journal.ppat.1002882https://doaj.org/article/9c64c8f54487495abd2c6909008ac3572012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22927818/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Plants evoke innate immunity against microbial challenges upon recognition of pathogen-associated molecular patterns (PAMPs), such as fungal cell wall chitin. Nevertheless, pathogens may circumvent the host PAMP-triggered immunity. We previously reported that the ascomycete Magnaporthe oryzae, a famine-causing rice pathogen, masks cell wall surfaces with α-1,3-glucan during invasion. Here, we show that the surface α-1,3-glucan is indispensable for the successful infection of the fungus by interfering with the plant's defense mechanisms. The α-1,3-glucan synthase gene MgAGS1 was not essential for infectious structure development but was required for infection in M. oryzae. Lack or degradation of surface α-1,3-glucan increased fungal susceptibility towards chitinase, suggesting the protective role of α-1,3-glucan against plants' antifungal enzymes during infection. Furthermore, rice plants secreting bacterial α-1,3-glucanase (AGL-rice) showed strong resistance not only to M. oryzae but also to the phylogenetically distant ascomycete Cochlioborus miyabeanus and the polyphagous basidiomycete Rhizoctonia solani; the histocytochemical analysis of the latter two revealed that α-1,3-glucan also concealed cell wall chitin in an infection-specific manner. Treatment with α-1,3-glucanase in vitro caused fragmentation of infectious hyphae in R. solani but not in M. oryzae or C. miyabeanus, indicating that α-1,3-glucan is also involved in maintaining infectious structures in some fungi. Importantly, rapid defense responses were evoked (a few hours after inoculation) in the AGL-rice inoculated with M. oryzae, C. miyabeanus and R. solani as well as in non-transgenic rice inoculated with the ags1 mutant. Taken together, our results suggest that α-1,3-glucan protected the fungal cell wall from degradative enzymes secreted by plants even from the pre-penetration stage and interfered with the release of PAMPs to delay innate immune defense responses. Because α-1,3-glucan is nondegradable in plants, it is reasonable that many fungal plant pathogens utilize α-1,3-glucan in the innate immune evasion mechanism and some in maintaining the structures.Takashi FujikawaAyumu SakaguchiYoko NishizawaYusuke KouzaiEiichi MinamiShigekazu YanoHironori KogaTetsuo MeshiMarie NishimuraPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 8, Iss 8, p e1002882 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Takashi Fujikawa Ayumu Sakaguchi Yoko Nishizawa Yusuke Kouzai Eiichi Minami Shigekazu Yano Hironori Koga Tetsuo Meshi Marie Nishimura Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.
description	Plants evoke innate immunity against microbial challenges upon recognition of pathogen-associated molecular patterns (PAMPs), such as fungal cell wall chitin. Nevertheless, pathogens may circumvent the host PAMP-triggered immunity. We previously reported that the ascomycete Magnaporthe oryzae, a famine-causing rice pathogen, masks cell wall surfaces with α-1,3-glucan during invasion. Here, we show that the surface α-1,3-glucan is indispensable for the successful infection of the fungus by interfering with the plant's defense mechanisms. The α-1,3-glucan synthase gene MgAGS1 was not essential for infectious structure development but was required for infection in M. oryzae. Lack or degradation of surface α-1,3-glucan increased fungal susceptibility towards chitinase, suggesting the protective role of α-1,3-glucan against plants' antifungal enzymes during infection. Furthermore, rice plants secreting bacterial α-1,3-glucanase (AGL-rice) showed strong resistance not only to M. oryzae but also to the phylogenetically distant ascomycete Cochlioborus miyabeanus and the polyphagous basidiomycete Rhizoctonia solani; the histocytochemical analysis of the latter two revealed that α-1,3-glucan also concealed cell wall chitin in an infection-specific manner. Treatment with α-1,3-glucanase in vitro caused fragmentation of infectious hyphae in R. solani but not in M. oryzae or C. miyabeanus, indicating that α-1,3-glucan is also involved in maintaining infectious structures in some fungi. Importantly, rapid defense responses were evoked (a few hours after inoculation) in the AGL-rice inoculated with M. oryzae, C. miyabeanus and R. solani as well as in non-transgenic rice inoculated with the ags1 mutant. Taken together, our results suggest that α-1,3-glucan protected the fungal cell wall from degradative enzymes secreted by plants even from the pre-penetration stage and interfered with the release of PAMPs to delay innate immune defense responses. Because α-1,3-glucan is nondegradable in plants, it is reasonable that many fungal plant pathogens utilize α-1,3-glucan in the innate immune evasion mechanism and some in maintaining the structures.
format	article
author	Takashi Fujikawa Ayumu Sakaguchi Yoko Nishizawa Yusuke Kouzai Eiichi Minami Shigekazu Yano Hironori Koga Tetsuo Meshi Marie Nishimura
author_facet	Takashi Fujikawa Ayumu Sakaguchi Yoko Nishizawa Yusuke Kouzai Eiichi Minami Shigekazu Yano Hironori Koga Tetsuo Meshi Marie Nishimura
author_sort	Takashi Fujikawa
title	Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.
title_short	Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.
title_full	Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.
title_fullStr	Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.
title_full_unstemmed	Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.
title_sort	surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.
publisher	Public Library of Science (PLoS)
publishDate	2012
url	https://doaj.org/article/9c64c8f54487495abd2c6909008ac357
work_keys_str_mv	AT takashifujikawa surfacea13glucanfacilitatesfungalstealthinfectionbyinterferingwithinnateimmunityinplants AT ayumusakaguchi surfacea13glucanfacilitatesfungalstealthinfectionbyinterferingwithinnateimmunityinplants AT yokonishizawa surfacea13glucanfacilitatesfungalstealthinfectionbyinterferingwithinnateimmunityinplants AT yusukekouzai surfacea13glucanfacilitatesfungalstealthinfectionbyinterferingwithinnateimmunityinplants AT eiichiminami surfacea13glucanfacilitatesfungalstealthinfectionbyinterferingwithinnateimmunityinplants AT shigekazuyano surfacea13glucanfacilitatesfungalstealthinfectionbyinterferingwithinnateimmunityinplants AT hironorikoga surfacea13glucanfacilitatesfungalstealthinfectionbyinterferingwithinnateimmunityinplants AT tetsuomeshi surfacea13glucanfacilitatesfungalstealthinfectionbyinterferingwithinnateimmunityinplants AT marienishimura surfacea13glucanfacilitatesfungalstealthinfectionbyinterferingwithinnateimmunityinplants
_version_	1718424620764233728

Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.

Ejemplares similares