Surface α-1,3-Glucan Facilitates Fungal Stealth Infection by Interfering with Innate Immunity in Plants

Takashi Fujikawa, Ayumu Sakaguchi, Yoko Nishizawa, Yusuke Kouzai, Eiichi Minami, Shigekazu Yano, Hironori Koga, Tetsuo Meshi, Marie Nishimura

Research output: Contribution to journalArticle

81 Citations (Scopus)

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.

Original languageEnglish
Article numbere1002882
JournalPLoS Pathogens
Volume8
Issue number8
DOIs
Publication statusPublished - Aug 2012
Externally publishedYes

Fingerprint

Glucans
Mycoses
Innate Immunity
Cell Wall
Ascomycota
Chitin
Infection
Magnaporthe
Oryza
Rhizoctonia
Immune Evasion
Chitinases
Basidiomycota
Hyphae
Enzymes
Masks
Starvation
Immunity
Fungi

ASJC Scopus subject areas

  • Microbiology
  • Parasitology
  • Virology
  • Immunology
  • Genetics
  • Molecular Biology

Cite this

Fujikawa, T., Sakaguchi, A., Nishizawa, Y., Kouzai, Y., Minami, E., Yano, S., ... Nishimura, M. (2012). Surface α-1,3-Glucan Facilitates Fungal Stealth Infection by Interfering with Innate Immunity in Plants. PLoS Pathogens, 8(8), [e1002882]. https://doi.org/10.1371/journal.ppat.1002882

Surface α-1,3-Glucan Facilitates Fungal Stealth Infection by Interfering with Innate Immunity in Plants. / Fujikawa, Takashi; Sakaguchi, Ayumu; Nishizawa, Yoko; Kouzai, Yusuke; Minami, Eiichi; Yano, Shigekazu; Koga, Hironori; Meshi, Tetsuo; Nishimura, Marie.

In: PLoS Pathogens, Vol. 8, No. 8, e1002882, 08.2012.

Research output: Contribution to journalArticle

Fujikawa, T, Sakaguchi, A, Nishizawa, Y, Kouzai, Y, Minami, E, Yano, S, Koga, H, Meshi, T & Nishimura, M 2012, 'Surface α-1,3-Glucan Facilitates Fungal Stealth Infection by Interfering with Innate Immunity in Plants', PLoS Pathogens, vol. 8, no. 8, e1002882. https://doi.org/10.1371/journal.ppat.1002882
Fujikawa, Takashi ; Sakaguchi, Ayumu ; Nishizawa, Yoko ; Kouzai, Yusuke ; Minami, Eiichi ; Yano, Shigekazu ; Koga, Hironori ; Meshi, Tetsuo ; Nishimura, Marie. / Surface α-1,3-Glucan Facilitates Fungal Stealth Infection by Interfering with Innate Immunity in Plants. In: PLoS Pathogens. 2012 ; Vol. 8, No. 8.
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