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N-Glycosylation Shields Phytophthora Sojae Apoplastic Effector Psxeg1 from a Specific Host Aspartic Protease

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N-Glycosylation Shields Phytophthora Sojae Apoplastic Effector Psxeg1 from a Specific Host Aspartic Protease N-glycosylation shields Phytophthora sojae apoplastic effector PsXEG1 from a specific host aspartic protease Yeqiang Xiaa,b,c, Zhenchuan Maa,b,c, Min Qiua,b,c, Baodian Guoa,b,c, Qi Zhanga,b,c, Haibin Jianga,b,c, Baiyu Zhanga,b,c, Yachun Lina,b,c, Mingrun Xuana,b,c, Liang Suna,b,c, Haidong Shua,b,c, Junhua Xiaoa,b,c, Wenwu Yea,b,c, Yan Wanga,b,c, Yiming Wanga,b,c, Suomeng Donga,b,c, Brett M. Tylerd,e, and Yuanchao Wanga,b,c,1,2 aDepartment of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China; bKey Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China cThe Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China; dCenter for Genome Research and Biocomputing, Oregon State University, Corvallis, OR 97331; and eDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331 Edited by Sheng Yang He, Duke University, Durham, NC, and approved September 17, 2020 (received for review June 12, 2020) Hosts and pathogens are engaged in a continuous evolutionary also attenuates the binding by the inhibitor GmGIP1. The decoy struggle for physiological dominance. A major site of this struggle PsXLP1 binds more tightly to GmGIP1 than PsXEG1 due to its is the apoplast. In Phytophthora sojae–soybean interactions, lack of glycosylation sites and escapes from GmAP5 degradation PsXEG1, a pathogen-secreted apoplastic endoglucanase, is a key by a C-terminal deletion. The crucial role of N-glycosylation focal point of this struggle, and the subject of two layers of host across multiple layers of defense and counterdefense centered defense and pathogen counterdefense. Here, we show that on PsXEG1 highlights the importance of posttranslational N-glycosylation of PsXEG1 represents an additional layer of this modification of a pathogen virulence factor in tipping the bal- coevolutionary struggle, protecting PsXEG1 against a host apo- ance of an arms race in this host–pathogen conflict. plastic aspartic protease, GmAP5, that specifically targets PsXEG1. This posttranslational modification also attenuated binding by the Results previously described host inhibitor, GmGIP1. N-glycosylation of PsXEG1 Is Degraded in the Apoplast. Immunoblot analysis of PsXEG1 at N174 and N190 inhibited binding and degradation by PsXEG1 protein produced during P. sojae infection suggested GmAP5 and was essential for PsXEG1’s full virulence contribution, degradation of this key effector (Fig. 1A). Two isoforms of except in GmAP5-silenced soybeans. Silencing of GmAP5 reduced PsXEG1 could be detected, of which the smaller form was much PLANT BIOLOGY P. sojae PsXEG1 soybean resistance against WT but not against more sensitive to degradation than the larger form, suggesting P. sojae. deletion strains of The crucial role of N-glycosylation that the larger form was posttranslationally modified (Fig. 1 A– within the three layers of defense and counterdefense centered C). The protein synthesis inhibitor cycloheximide (CHX) was on PsXEG1 highlight the critical importance of this conserved apoplas- used to assay PsXEG1-HA (hemagglutinin) stability in the Phytophthora tic effector and its posttranslational modification in -host apoplast of Nicotiana benthamiana leaves; the results showed coevolutionary conflict. that transiently expressed PsXEG1-HA was rapidly degraded after CHX blocked new protein synthesis (Fig. 1B and SI apoplast | P. sojae | N-glycosylation | aspartic protease | immunity Significance icrobial plant pathogens have evolved a variety of strate- gies to attack plant hosts to cause disease (1, 2). Early M The apoplastic space is the initial battlefield in plant–microbe interactions between plant pathogens and their hosts occur in the interactions. However, the molecular mechanisms underlying extracellular space (apoplast) (3), where many kinds of molec- how apoplastic immunity controls pathogen invasion is still largely ular interactions, including attacking enzymes and counteracting unknown. Here, we show that soybean secretes an apoplastic inhibitors from both sides, play an important role in determining aspartic protease, GmAP5, that binds to and degrades PsXEG1 to the overall outcome of infection (4, 5). The struggle for physi- block its contribution to virulence. Phytophthora sojae, however, ological dominance in the apoplast engages multiple layers of employs N-glycosylation as a shield to protect PsXEG1 from deg- defense and counterdefense between hosts and pathogens. radation by GmAP5. N-glycosylation of PsXEG1 also attenuates the Phytophthora sojae, the agent of soybean (Glycine max) root binding by the inhibitor GmGIP1. Our result uncovers an additional and stem rot, causes substantial worldwide soybean production layer of defense and counterdefense centered on PsXEG1, high- losses (6). Previously, we found that the apoplastic xyloglucan- lightinganexampleinwhichN-glycosylation of a pathogen viru- specific endoglucanase PsXEG1 of P. sojae is subject to two lence factor tips the balance of an arms race in host–pathogen layers of defense and counterdefense (7–9). Recognition of conflicts. PsXEG1 by the soybean pattern recognition machinery can block P. sojae infection; however, the PsXEG1-triggered immune re- Author contributions: Y.X., Z.M., and Yuanchao Wang designed research; Y.X., Z.M., sponse is, in turn, suppressed by multiple intracellular effectors M.Q., B.G., Q.Z., H.J., B.Z., Y.L., M.X., L.S., H.S., J.X., W.Y., S.D., B.M.T., and Yuanchao (7, 8). PsXEG1 is also targeted by a second defense layer, the Wang performed research; Y.X., Z.M., M.Q., B.G., Q.Z., H.J., H.S., W.Y., Yan Wang, Yiming Wang, B.M.T., and Yuanchao Wang analyzed data; and Y.X., Z.M., M.Q., Yan Wang, apoplastic inhibitor protein GmGIP1, which binds to PsXEG1 to Yiming Wang, S.D., B.M.T., and Yuanchao Wang wrote the paper. inhibit its enzyme activity and, thereby, reducing P. sojae viru- The authors declare no competing interest. lence; however, PsXEG1 is protected by a paralogous decoy, This article is a PNAS Direct Submission. PsXLP1, which has evolved to bind more tightly to GmGIP1 This open access article is distributed under Creative Commons Attribution-NonCommercial- than PsXEG1 (8). NoDerivatives License 4.0 (CC BY-NC-ND). Here, we show that PsXEG1 is subject to an additional layer 1Present address: No.1 Weigang, Department of Plant Pathology, Nanjing Agricultural host defense. PsXEG1 is degraded by the soybean aspartic University, 210095 Nanjing, China. protease GmAP5. However, N-glycosylation acts as a shield to 2To whom correspondence may be addressed. Email: [email protected]. protect PsXEG1 from degradation by GmAP5, which has This article contains supporting information online at https://www.pnas.org/lookup/suppl/ evolved to specifically target PsXEG1, constituting an additional doi:10.1073/pnas.2012149117/-/DCSupplemental. layer of defense and counterdefense. N-glycosylation of PsXEG1 First published October 20, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2012149117 PNAS | November 3, 2020 | vol. 117 | no. 44 | 27685–27693 Downloaded by guest on September 29, 2021 Appendix, Fig. S1). The smaller isoform of PsXEG1 was partic- Fig. 1C) and the other ∼26 kDa, with different sensitivities to ularly sensitive to degradation. To further examine the degra- degradation. These two isoforms were also present in P. sojae dation of PsXEG1 by soybean apoplastic proteins, we incubated transformants overexpressing PsXEG1 (SI Appendix, Fig. S5) PsXEG1 protein purified from P. sojae with soybean apoplast and after transient expression in N. benthamiana leaves (Fig. 1 B fluid (AF), in the presence of various protease inhibitors mixture and E and SI Appendix, Fig. S6 A and B). Treatment with (PIs) for 1 h at 25 °C in vitro. Again, the smaller isoform of peptide-N-glycosidases (PNGase) A or F reduced the ∼34-kDa PsXEG1 was sensitive to degradation. However, the degradation PsXEG1 isoform to ∼26 kDa (Fig. 2A and SI Appendix, Fig. of PsXEG1 was substantially inhibited by the aspartic protease S6C). Endoglycosidase H (EndoH) produced a slight reduction inhibitor Pepstatin A (Pep A) as well as by the PIs mix (Fig. 1C). while O-glycosidase produced no reduction (Fig. 2A and SI Ap- This result suggested that the apoplastic aspartic protease(s) pendix, Fig. S6C). Consistent with that observation, the larger were involved in PsXEG1 degradation. isoform of PsXEG1 stained positively for glycosyl groups, whereas the smaller isoform and PNGase A-treated PsXEG1 did Soybean GmAP5 Degrades PsXEG1 and Confers Host Resistance not (SI Appendix, Fig. S6D). In line with this, only the smaller Against P. sojae. The apoplast-localized PsXEG1 inhibitor, isoform of PsXEG1 was detected when PsXEG1 was transiently GmGIP1, is a nonactive aspartic protease-like protein (8, expressed in N. benthamiana in the presence of the N-linked 10),which directly interacts with PsXEG1. To determine whether glycosylation inhibitor tunicamycin (TM) (Fig. 2B). These enzyme-active homolog(s) of GmGIP1 target PsXEG1 for deg- results demonstrated that the larger isoform represented radation, genome-wide analysis was performed to identify N-glycosylated PsXEG1 while the smaller isoform represented GmGIP1 homologs as putative active aspartic proteases (Dataset unglycosylated PsXEG1. S1). RNA sequencing showed that two of these homologs, Gly- To pinpoint the N-glycosylation sites, PNGases-treated ma.11G215200.1 and Glyma.03G200900.1, exhibited similar PsXEG1 purified from the P. sojae overexpression trans- timing of transcript accumulation as PsXEG1, with a peak at ∼ formant OT17 (SI Appendix, Fig. S5) was analyzed using nano- 0.5 h postinoculation (hpi) during early infection by P. sojae scale liquid chromatography-tandem MS (LC-MS/MS) (Fig. 2C). (Fig. 1D and SI Appendix, Fig. S2A). To test the interaction N174 and N190 are identified as potential glycosylation sites between PsXEG1 and these two protease candidates, we per- (Fig. 2D, SI Appendix, Figs. S7 and S8, and Dataset S2). Both formed in planta coimmunoprecipitation (Co-IP) assays after N174 and N190 are located in the N-glycosylation NxS/T (Asn-x- transient coexpression of these proteins in N.
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