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

PLoS Pathog. 2012;8(8):e1002882. doi: 10.1371/journal.ppat.1002882. Epub 2012 Aug 23.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Basidiomycota / genetics
  • Basidiomycota / metabolism*
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism*
  • Glucans / genetics
  • Glucans / metabolism*
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Magnaporthe / enzymology*
  • Magnaporthe / genetics
  • Magnaporthe / pathogenicity
  • Oryza / genetics
  • Oryza / microbiology*
  • Plant Diseases / genetics
  • Plant Diseases / microbiology*
  • Plant Immunity*

Substances

  • Fungal Proteins
  • Glucans
  • Glucosyltransferases

Grant support

This work was financially supported through grants from the Ministry of Agriculture, Forestry and Fisheries of Japan (Genomics for Agricultural Innovation # PMI-0009 and # GMA-0011) to MN and EM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.