title: Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants.
abstract: 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.
authors.affiliation: National Institute of Agrobiological Sciences-NIAS, Tsukuba, Ibaraki, Japan.
authors.forename: Takashi
authors.initials: T
authors.lastname: Fujikawa
authors.forename: Ayumu
authors.initials: A
authors.lastname: Sakaguchi
authors.forename: Yoko
authors.initials: Y
authors.lastname: Nishizawa
authors.forename: Yusuke
authors.initials: Y
authors.lastname: Kouzai
authors.forename: Eiichi
authors.initials: E
authors.lastname: Minami
authors.forename: Shigekazu
authors.initials: S
authors.lastname: Yano
authors.forename: Hironori
authors.initials: H
authors.lastname: Koga
authors.forename: Tetsuo
authors.initials: T
authors.lastname: Meshi
authors.forename: Marie
authors.initials: M
authors.lastname: Nishimura
mesh_terms: D001487:Basidiomycota / Q000235:genetics / Q000378:metabolism*; D005656:Fungal Proteins / Q000235:genetics / Q000378:metabolism*; D005936:Glucans / Q000235:genetics / Q000378:metabolism*; D005964:Glucosyltransferases / Q000235:genetics / Q000378:metabolism; D020082:Magnaporthe / Q000201:enzymology* / Q000235:genetics / Q000472:pathogenicity; D012275:Oryza / Q000235:genetics / Q000382:microbiology*; D010935:Plant Diseases / Q000235:genetics / Q000382:microbiology*; D057865:Plant Immunity
chemical_list: D005656:Fungal Proteins; D005936:Glucans; D005964:Glucosyltransferases