The processed C-terminus of AvrRps4 effector suppresses plant immunity via targeting multiple WRKYs.

AvrRps4 WRKY bacterial effector effector‐triggered immunity immune response suppression transcription factor

Journal

Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502

Informations de publication

Date de publication:
13 Jun 2024
Historique:
revised: 03 05 2024
received: 11 10 2023
accepted: 04 05 2024
medline: 13 6 2024
pubmed: 13 6 2024
entrez: 13 6 2024
Statut: aheadofprint

Résumé

Pathogens generate and secrete effector proteins to the host plant cells during pathogenesis to promote virulence and colonization. If the plant carries resistance (R) proteins that recognize pathogen effectors, effector-triggered immunity (ETI) is activated, resulting in a robust immune response and hypersensitive response (HR). The bipartite effector AvrRps4 from Pseudomonas syringae pv. pisi has been well studied in terms of avirulence function. In planta, AvrRps4 is processed into two parts. The C-terminal fragment of AvrRps4 (AvrRps4

Identifiants

pubmed: 38869289
doi: 10.1111/jipb.13710
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Research Foundation of Korea
ID : 2021M3A9I5023695
Organisme : National Research Foundation of Korea
ID : 2021R1I1A3054417
Organisme : National Research Foundation of Korea
ID : 2022R1A5A1031361
Organisme : National Research Foundation of Korea
ID : 2022R1I1A1A01063394
Organisme : National Research Foundation of Korea
ID : RS-2023-00301974
Organisme : Rural Development Administration
ID : RS-2024-00322125

Informations de copyright

© 2024 The Author(s). Journal of Integrative Plant Biology published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.

Références

Andolfo, G., and Ercolano, M.R. (2015). Plant innate immunity multicomponent model. Front. Plant Sci. 6: 987.
Badel, J.L., Piquerez, S.J., Greenshields, D., Rallapalli, G., Fabro, G., Ishaque, N., and Jones, J.D. (2013). In planta effector competition assays detect Hyaloperonospora arabidopsidis effectors that contribute to virulence and localize to different plant subcellular compartments. Mol. Plant Microbe. Interact. 26: 745–757.
Balint‐Kurti, P. (2019). The plant hypersensitive response: Concepts, control and consequences. Mol. Plant Pathol. 20: 1163–1178.
Besseau, S., Li, J., and Palva, E.T. (2012). WRKY54 and WRKY70 co‐operate as negative regulators of leaf senescence in Arabidopsis thaliana. J. Exp. Bot. 63: 2667–2679.
Borrelli, V.M.G., Brambilla, V., Rogowsky, P., Marocco, A., and Lanubile, A. (2018). The enhancement of plant disease resistance using CRISPR/Cas9 technology. Front. Plant Sci. 9: 1245.
Cesari, S. (2018). Multiple strategies for pathogen perception by plant immune receptors. New Phytol. 219: 17–24.
Chen, S., Ding, Y., Tian, H., Wang, S., and Zhang, Y. (2021). WRKY54 and WRKY70 positively regulate SARD1 and CBP60g expression in plant immunity. Plant Signal. Behav. 16: 1932142.
Cheng, C., Gao, X., Feng, B., Sheen, J., Shan, L., and He, P. (2013). Plant immune response to pathogens differs with changing temperatures. Nat. Commun. 4: 2530.
Chisholm, S.T., Coaker, G., Day, B., and Staskawicz, B.J. (2006). Host‐microbe interactions: Shaping the evolution of the plant immune response. Cell 124: 803–814.
Dangl, J.L., Horvath, D.M., and Staskawicz, B.J. (2013). Pivoting the plant immune system from dissection to deployment. Science 341: 746–751.
Eulgem, T. (2005). Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci. 10: 71–78.
Gao, X., Chen, X., Lin, W., Chen, S., Lu, D., Niu, Y., and He, P. (2013). Bifurcation of Arabidopsis NLR immune signaling via Ca(2)(+)‐dependent protein kinases. PLoS Pathog. 9: e1003127.
Gassmann, W., Hinsch, M.E., and Staskawicz, B.J. (1999). The Arabidopsis RPS4 bacterial‐resistance gene is a member of the TIR‐NBS‐LRR family of disease‐resistance genes. Plant J. 20: 265–277.
Go, Y.S., Kim, H., Kim, H.J., and Suh, M.C. (2014). Arabidopsis cuticular wax biosynthesis is negatively regulated by the DEWAX gene encoding an AP2/ERF‐type transcription factor. Plant Cell 26: 1666–1680.
Halane, M.K., Kim, S.H., Spears, B.J., Garner, C.M., Rogan, C.J., Okafor, E.C., and Gassmann, W. (2018). The bacterial type III‐secreted protein AvrRps4 is a bipartite effector. PLoS Pathog. 14: e1006984.
Heidrich, K., Wirthmueller, L., Tasset, C., Pouzet, C., Deslandes, L., and Parker, J.E. (2011). Arabidopsis EDS1 connects pathogen effector recognition to cell compartment‐specific immune responses. Science 334: 1401–1404.
Hinsch, M., and Staskawicz, B. (1996). Identification of a new Arabidopsis disease resistance locus, RPs4, and cloning of the corresponding avirulence gene, avrRps4, from Pseudomonas syringae pv. pisi. Mol. Plant Microbe. Interact. 9: 55–61.
Hsin, K.T., Hsieh, M.C., Lee, Y.H., Lin, K.C., and Cheng, Y.S. (2022). Insight into the phylogeny and binding ability of WRKY transcription factors. Int. J. Mol. Sci. 23: 2895.
Hu, Y., Dong, Q., and Yu, D. (2012). Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci. 185‐186: 288–297.
Jiang, L., Wang, Y., Li, Q.F., Bjorn, L.O., He, J.X., and Li, S.S. (2012). Arabidopsis STO/BBX24 negatively regulates UV‐B signaling by interacting with COP1 and repressing HY5 transcriptional activity. Cell Res. 22: 1046–1057.
Jones, J.D., and Dangl, J.L. (2006). The plant immune system. Nature 444: 323–329.
Kim, K.C., Lai, Z., Fan, B., and Chen, Z. (2008). Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20: 2357–2371.
Lapin, D., and Van den Ackerveken, G. (2013). Susceptibility to plant disease: More than a failure of host immunity. Trends Plant Sci. 18: 546–554.
Le Roux, C., Huet, G., Jauneau, A., Camborde, L., Tremousaygue, D., Kraut, A., and Deslandes, L. (2015). A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161: 1074–1088.
Li, G., Froehlich, J.E., Elowsky, C., Msanne, J., Ostosh, A.C., Zhang, C., and Alfano, J.R. (2014). Distinct Pseudomonas type‐III effectors use a cleavable transit peptide to target chloroplasts. Plant J. 77: 310–321.
Li, J., Zhong, R., and Palva, E.T. (2017). WRKY70 and its homolog WRKY54 negatively modulate the cell wall‐associated defenses to necrotrophic pathogens in Arabidopsis. PLoS One 12: e0183731.
Liu, H., Liu, B., Lou, S., Bi, H., Tang, H., Tong, S., and Liu, J. (2021). CHYR1 ubiquitinates the phosphorylated WRKY70 for degradation to balance immunity in Arabidopsis thaliana. New Phytol. 230: 1095–1109.
Llorca, C.M., Potschin, M., and Zentgraf, U. (2014). bZIPs and WRKYs: Two large transcription factor families executing two different functional strategies. Front. Plant Sci. 5: 169.
Mukhi, N., Brown, H., Gorenkin, D., Ding, P., Bentham, A.R., Stevenson, C.E.M., and Banfield, M.J. (2021). Perception of structurally distinct effectors by the integrated WRKY domain of a plant immune receptor. Proc. Natl. Acad. Sci. U.S.A. 118: e2113996118.
Narusaka, M., Shirasu, K., Noutoshi, Y., Kubo, Y., Shiraishi, T., Iwabuchi, M., and Narusaka, Y. (2009). RRS1 and RPS4 provide a dual resistance‐gene system against fungal and bacterial pathogens. Plant J. 60: 218–226.
Nguyen, Q.M., Iswanto, A.B.B., Son, G.H., and Kim, S.H. (2021). Recent advances in effector‐triggered immunity in plants: New pieces in the puzzle create a different paradigm. Int. J. Mol. Sci. 22: 4709.
Oh, H.S., and Collmer, A. (2005). Basal resistance against bacteria in Nicotiana benthamiana leaves is accompanied by reduced vascular staining and suppressed by multiple Pseudomonas syringae type III secretion system effector proteins. Plant J. 44: 348–359.
Prasad, A., Chirom, O., and Prasad, M. (2022). Shedding light on immune suppression at high temperature. Trends Microbiol. 30: 918–919.
Rushton, P.J., Somssich, I.E., Ringler, P., and Shen, Q.J. (2010). WRKY transcription factors. Trends Plant Sci. 15: 247–258.
Sarris, P.F., Duxbury, Z., Huh, S.U., Ma, Y., Segonzac, C., Sklenar, J., and Jones, J.D.G. (2015). A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161: 1089–1100.
Saucet, S.B., Ma, Y., Sarris, P.F., Furzer, O.J., Sohn, K.H., and Jones, J.D. (2015). Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4. Nat. Commun. 6: 6338.
Schenke, D., and Cai, D. (2020). Applications of CRISPR/Cas to improve crop disease resistance: Beyond inactivation of susceptibility factors. iScience 23: 101478.
Schultink, A., Qi, T., Lee, A., Steinbrenner, A.D., and Staskawicz, B. (2017). Roq1 mediates recognition of the Xanthomonas and Pseudomonas effector proteins XopQ and HopQ1. Plant J. 92: 787–795.
Sheikh, A.H., Eschen‐Lippold, L., Pecher, P., Hoehenwarter, W., Sinha, A.K., Scheel, D., and Lee, J. (2016). Regulation of WRKY46 transcription factor function by mitogen‐activated protein kinases in Arabidopsis thaliana. Front. Plant Sci. 7: 61.
Sohn, K.H., Hughes, R.K., Piquerez, S.J., Jones, J.D., and Banfield, M.J. (2012). Distinct regions of the Pseudomonas syringae coiled‐coil effector AvrRps4 are required for activation of immunity. Proc. Natl. Acad. Sci. U.S.A. 109: 16371–16376.
Sohn, K.H., Segonzac, C., Rallapalli, G., Sarris, P.F., Woo, J.Y., Williams, S.J., and Jones, J.D. (2014). The nuclear immune receptor RPS4 is required for RRS1SLH1‐dependent constitutive defense activation in Arabidopsis thaliana. PLoS Genet. 10: e1004655.
Sohn, K.H., Zhang, Y., and Jones, J.D. (2009). The Pseudomonas syringae effector protein, AvrRPS4, requires in planta processing and the KRVY domain to function. Plant J. 57: 1079–1091.
Su, J., Spears, B.J., Kim, S.H., and Gassmann, W. (2018). Constant vigilance: Plant functions guarded by resistance proteins. Plant J. 93: 637–650.
Ulker, B., and Somssich, I.E. (2004). WRKY transcription factors: From DNA binding towards biological function. Curr. Opin. Plant Biol. 7: 491–498.
Vuong, U.T., Iswanto, A.B.B., Nguyen, Q.M., Kang, H., Lee, J., Moon, J., and Kim, S.H. (2023). Engineering plant immune circuit: Walking to the bright future with a novel toolbox. Plant Biotechnol. J. 21: 17–45.
Wei, C.F., Kvitko, B.H., Shimizu, R., Crabill, E., Alfano, J.R., Lin, N.C., and Collmer, A. (2007). A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1‐1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J. 51: 32–46.
Williams, S.J., Sohn, K.H., Wan, L., Bernoux, M., Sarris, P.F., Segonzac, C., and Jones, J.D. (2014). Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344: 299–303.
Wu, K.L., Guo, Z.J., Wang, H.H., and Li, J. (2005). The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res. 12: 9–26.
Zhou, M., Lu, Y., Bethke, G., Harrison, B.T., Hatsugai, N., Katagiri, F., and Glazebrook, J. (2018). WRKY70 prevents axenic activation of plant immunity by direct repression of SARD1. New Phytol. 217: 700–712.

Auteurs

Quang-Minh Nguyen (QM)

Division of Applied Life Science (BK21 Four Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 52828, Korea.

Arya Bagus Boedi Iswanto (ABB)

Division of Applied Life Science (BK21 Four Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 52828, Korea.

Hobin Kang (H)

Division of Applied Life Science (BK21 Four Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 52828, Korea.

Jiyun Moon (J)

Division of Applied Life Science (BK21 Four Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 52828, Korea.

Kieu Anh Thi Phan (KAT)

Division of Applied Life Science (BK21 Four Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 52828, Korea.

Geon Hui Son (GH)

Division of Applied Life Science (BK21 Four Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 52828, Korea.

Mi Chung Suh (MC)

Department of Life Science, Sogang University, Seoul, 04107, Korea.

Eui-Hwan Chung (EH)

Department of Plant Biotechnology, Korea University, Seoul, 02841, Korea.

Walter Gassmann (W)

Division of Plant Science and Technology, Christopher S. Bond Life Sciences Center and Interdisciplinary Plant Group, University of Missouri, Columbia, 65211, Missouri, USA.

Sang Hee Kim (SH)

Division of Applied Life Science (BK21 Four Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 52828, Korea.
Division of Life Science and Research Institute of Molecular Alchemy, Gyeongsang National University, Jinju, 52828, Korea.

Classifications MeSH