N - glycosylation shields Phytophthora sojae apoplastic effector PsXEG1 from a specific host aspartic protease

Abstract

Hosts and pathogens are engaged in a continuous evolutionary struggle for physiological dominance. A major site of this struggle is the apoplast. In Phytophthora sojae–soybean interactions, PsXEG1, a pathogen-secreted apoplastic endoglucanase, is a key focal point of this struggle, and the subject of two layers of host defense and pathogen counterdefense. Here, we show that N-glycosylation of PsXEG1 represents an additional layer of this coevolutionary struggle, protecting PsXEG1 against a host apoplastic aspartic protease, GmAP5, that specifically targets PsXEG1. This posttranslational modification also attenuated binding by the previously described host inhibitor, GmGIP1. N-glycosylation of PsXEG1 at N174 and N190 inhibited binding and degradation by GmAP5 and was essential for PsXEG1’s full virulence contribution, except in GmAP5-silenced soybeans. Silencing of GmAP5 reduced soybean resistance against WT P. sojae but not against PsXEG1 deletion strains of P. sojae. The crucial role of N-glycosylation within the three layers of defense and counterdefense centered on PsXEG1 highlight the critical importance of this conserved apoplastic effector and its posttranslational modification in Phytophthora-host coevolutionary conflict.

Comparative Label-Free Quantitative Proteomics Analysis Reveals the Essential Roles of N-Glycans in Salt Tolerance by Modulating Protein Abundance in Arabidopsis

“…In plants, N-glycosylation is involved in many biological processes, including ER-quality control of steroid hormone receptor (Jin et al, 2007;Hong et al, 2008), gametophyte recognition (Lindner et al, 2015;Muller et al, 2016), subcellular transport (Rips et al, 2014;Shen et al, 2014), plant innate immunity (Li et al, 2009;Nekrasov et al, 2009;Haweker et al, 2010;Xia et al, 2020), and stomatal development (Jiao et al, 2020) by regulating the stability, function, or sub-localization of the substrate protein. Moreover, several studies also establish the association of N-glycosylation with salt tolerance in Arabidopsis (Koiwa et al, 2003;Kang et al, 2008;Nagashima et al, 2018).…”

Thinopyrum intermediumTiAP1 interacts with a chitin deacetylase fromBlumeria graminisf. sp.triticiand increases the resistance toBgtin wheat

“…When the pathogen invades the host, an extremely complex and precise arms race of 'attack and defence' occurs in the apoplastic space. Xia et al (2020) also proposed a 'multi-layered immune model' of the plants against pathogens in the extracellular region when studying the mechanism of action of PsXEG1 against Phytophthora sojae. Therefore, this study revealed the complexity of the interaction between pathogens and hosts as well as provided a theoretical basis to further study the role of TiAP1 in resistance mechanisms.…”

Protein glycosylation during infection by plant pathogenic fungi

“…Interestingly, bioinformatics prediction of N‐ glycosylation suggests that many other effector proteins may also be N‐ glycosylated, and this may be important in their ability to suppress host immune responses. Recently, for example, it was found that in the oomycete pathogen Phytophthora sojae , N‐ glycosylation also shields an effector PsXEG1 against degradation by host aspartate proteases (Xia et al ., 2020).…”