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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 44; pp. 27685 - 27693
• Main Authors: Xia, Yeqiang, Ma, Zhenchuan, Qiu, Min, Guo, Baodian, Zhang, Qi, Jiang, Haibin, Zhang, Baiyu, Lin, Yachun, Xuan, Mingrun, Sun, Liang, Shu, Haidong, Xiao, Junhua, Ye, Wenwu, Wang, Yan, Wang, Yiming, Dong, Suomeng, Tyler, Brett M., Wang, Yuanchao
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 03.11.2020
• Subjects: Apoplast; Aspartic Acid Endopeptidases - genetics; Aspartic Acid Endopeptidases - metabolism; Aspartic endopeptidase; Binding; Biological Sciences; Cellulase - genetics; Cellulase - metabolism; Disease Resistance - genetics; Endoglucanase; Gene Knockdown Techniques; Glycine max - enzymology; Glycine max - genetics; Glycine max - microbiology; Glycosylation; Host-Pathogen Interactions - genetics; Pathogens; Phytophthora - metabolism; Phytophthora - pathogenicity; Phytophthora sojae; Plant Diseases - microbiology; Plant Proteins - genetics; Plant Proteins - metabolism; Plants, Genetically Modified; Protease; Protein Binding; Protein Processing, Post-Translational; Proteolysis; Soybeans; Virulence; P. sojae; immunity; apoplast; N-glycosylation; aspartic protease
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2012149117

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 posttranslationalmodification in Phytophthora-host coevolutionary conflict.