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Surface ?-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 ?-1,3-glucan during invasion. Here, we show that the surface ?-1,3-glucan is indispensable for the successful infection of the fungus by interfering with the plant's defense mechanisms. The ?-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 ?-1,3-glucan increased fungal susceptibility towards chitinase, suggesting the protective role of ?-1,3-glucan against plants' antifungal enzymes during infection. Furthermore, rice plants secreting bacterial ?-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 ?-1,3-glucan also concealed cell wall chitin in an infection-specific manner. Treatment with ?-1,3-glucanase in vitro caused fragmentation of infectious hyphae in R. solani but not in M. oryzae or C. miyabeanus, indicating that ?-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 ?-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 ?-1,3-glucan is nondegradable in plants, it is reasonable that many fungal plant pathogens utilize ?-1,3-glucan in the innate immune evasion mechanism and some in maintaining the structures.

SUBMITTER: Fujikawa T

PROVIDER: S-EPMC3426526 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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

Fujikawa Takashi T Sakaguchi Ayumu A Nishizawa Yoko Y Kouzai Yusuke Y Minami Eiichi E Yano Shigekazu S Koga Hironori H Meshi Tetsuo T Nishimura Marie M

PLoS pathogens 20120823 8

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 interf ...[more]

PMID: 22927818

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Dataset Information

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

Publications

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

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