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.

Chitin and chitin-related compounds in plant–fungal interactions

“…For example, the α-1,3-glucan synthase gene MgAGS1 was not essential for infectious structure development but infection in Magnaporthe 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 (Fujikawa et al 2012). Alternatively, during host colonisation, some fungi convert cell wall chitin by deaminases into chitosan, which is a poor substrate for chitinases and a weak inducer of plant immune responses (El Gueddari et al 2002).…”

N-Glycosylation of Effector Proteins by an α-1,3-Mannosyltransferase Is Required for the Rice Blast Fungus to Evade Host Innate Immunity

“…The outer layer of the fungal cell wall is important for protecting the inner chitins or glucans from recognition by host plants (Fujikawa et al, 2012). Glycoproteins are known to be an important component of the fungal cell wall (Bowman and Free, 2006).…”

“…In response to these defenses, plant pathogens have developed strategies to avoid or overcome PAMP-triggered immunity. The most important structural protection of an invading fungus is the outer layer of the cell wall, by which fungal pathogens can avoid host recognition of inner chitin and glucans (Fujikawa et al, 2012). Pathogens can also counter PAMP-triggered immunity mechanisms by effector-mediated suppression of these immunity responses, leading to effector-triggered susceptibility (Jones and Dangl, 2006).…”

A Review of the Applications of Chitin and Its Derivatives in Agriculture to Modify Plant-Microbial Interactions and Improve Crop Yields

“…It is thought that CEBiP receptors respond to chitin oligomers released from pests and pathogens when they are degraded by chitinases that the plant produces in both the apoplast and symplast [108,109]. While plants do produce chitinases to generate chitin fragments from pests and pathogens, and possess CEBiP receptors to detect the chitin and then activate defenses, it is also the case that pests and pathogens can overcome this mechanism by producing chitin-binding proteins to prevent the detection of chitin fragments by CEBiPs by the host plant and thus attack without defenses being induced [110].…”