Abstract
Receptor-like kinases (RLKs) play important roles in plant immunity signaling; thus, many are hijacked by pathogen effectors to promote successful pathogenesis. Xanthomonas oryzae pv. oryzae (Xoo) is the causal agent of rice leaf blight disease. The strain PXO99A has 18 non-TAL (transcription activation-like) effectors; however, their mechanisms of action and host target proteins remain largely unknown. Although the effector XopR from the Xoo strain MAFF311018 was shown to suppress PAMP-triggered immune responses in Arabidopsis, its target has not yet been identified. Here, we show that PXO99A XopR interacts with BIK1 at the plasma membrane. BIK1 is a receptor-like cytoplasmic kinase (RLCK) belonging to the RLK family of proteins and mediates PAMP-triggered stomatal immunity. In turn, BIK1 phosphorylates XopR. Furthermore, XopR suppresses PAMP-triggered stomatal closure in transgenic Arabidopsis expressing XopR. In addition, XopR is able to associate with RLCKs other than BIK1. These results suggest that XopR likely suppresses plant immunity by targeting BIK1 and other RLCKs.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Akimoto-Tomiyama, C., Furutani, A., Tsuge, S., Washington, E.J., Nishizawa, Y., Minami, E., and Ochiai, H. (2012). XopR, a type III effector secreted by Xanthomonas oryzae pv. oryzae, suppresses microbe-associated molecular pattern-triggered immunity in Arabidopsis thaliana. Mol Plant Microbe Interact 25, 505–514.
Anderson, J.C., Pascuzzi, P.E., Xiao, F., Sessa, G., and Martin, G.B. (2006). Host-mediated phosphorylation of type III effector AvrPto promotes Pseudomonas virulence and avirulence in tomato. Plant Cell 18, 502–514.
Arnaud, D., and Hwang, I. (2015). A sophisticated network of signaling pathways regulates stomatal defenses to bacterial pathogens. Mol Plant 8, 566–581.
Boch, J., and Bonas, U. (2010). Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48, 419–436.
Boller, T., and Felix, G. (2009). A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern- recognition receptors. Annu Rev Plant Biol 60, 379–406.
Boller, T., and He, S.Y. (2009). Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324, 742–744.
Chinchilla, D., Bauer, Z., Regenass, M., Boller, T., and Felix, G. (2006). The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18, 465–476.
Cook, D.E., Mesarich, C.H., and Thomma, B.P. (2015). Understanding plant immunity as a surveillance system to detect invasion. Annu Rev Phytopathol 53, 541–563.
Feng, F., Yang, F., Rong, W., Wu, X., Zhang, J., Chen, S., He, C., and Zhou, J.M. (2012). A Xanthomonas uridine 5’-monophosphate transferase inhibits plant immune kinases. Nature 485, 114–118.
Feng, F., and Zhou, J.M. (2012). Plant-bacterial pathogen interactions mediated by type III effectors. Curr Opin Plant Biol 15, 469–476.
Furutani, A., Takaoka, M., Sanada, H., Noguchi, Y., Oku, T., Tsuno, K., Ochiai, H., and Tsuge, S. (2009). Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 22, 96–106.
Gimenez-Ibanez, S., Hann, D.R., Ntoukakis, V., Petutschnig, E., Lipka, V., and Rathjen, J.P. (2009). AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 19, 423–429.
Göhre, V., Spallek, T., Häweker, H., Mersmann, S., Mentzel, T., Boller, T., de Torres, M., Mansfield, J.W., and Robatzek, S. (2008). Plant pattern- recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol 18, 1824–1832.
Gomez-Gomez, L., and Boller, T. (2000). FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5, 1003–1011.
He, P., Shan L., Lin, N.C., Martin, G.B., Kemmerling, B., Nürnberger, T., and Sheen, J. (2006). Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125, 563–575.
Kadota, Y., Sklenar, J., Derbyshire, P., Stransfeld, L., Asai, S., Ntoukakis, V., Jones, J.D., Shirasu, K., Menke, F., Jones, A., and Zipfel, C. (2014). Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54, 43–55.
Kim, J.G., Li, X., Roden, J.A., Taylor, K.W., Aakre, C.D., Su, B., Lalonde, S., Kirik, A., Chen, Y., Baranage, G., McLane, H., Martin, G.B., and Mudgett, M.B. (2009). Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor- like kinase and TFT1. Plant Cell 21, 1305–1323.
Kim, J.G., Stork, W., and Mudgett, M.B. (2013). Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth. Cell Host Microbe 13, 143–154.
Li, L., Li, M., Yu, L., Zhou, Z., Liang, X., Liu, Z., Cai, G., Gao, L., Zhang, X., Wang, Y., Chen, S., and Zhou, J.M. (2014). The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15, 329–338.
Liebrand, T.W., van den Burg, H.A., and Joosten, M.H. (2014). Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 19, 123–132.
Lin, W., Li, B., Lu, D., Chen, S., Zhu, N., He, P., and Shan, L. (2014). Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediates Arabidopsis innate immunity. Proc Natl Acad Sci USA 111, 3632–3637.
Lu, D., Wu, S., Gao, X., Zhang, Y., Shan, L., and He, P. (2010). A receptor- like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 107, 496–501.
Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., Narusaka, Y., Kawakami, N., Kaku, H., and Shibuya, N. (2007). CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104, 19613–19618.
Nimchuk, Z., Marois, E., Kiemtrup, S., Leister, R.T., Kataqiri, F., and Dangl, J.L. (2000). Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell 101, 353–363.
Robert-Seilaniantz, A., Shan, L., Zhou, J.M., and Tang, X.Y. (2006). The Pseudomonas syringae pv. tomato DC3000 type III effector HopF2 has a putative myristoylation site required for its avirulence and virulence functions. Mol Plant Microbe Interact 19, 130–138.
Shan, L., Thara, V.K., Martin, G.B., Zhou, J. M., and Tang, X.Y. (2000). The pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 12, 2323–2338.
Shi, H., Shen, Q., Qi, Y., Yan, H., Nie, H., Chen, Y., Zhao, T., Katagiri, F., and Tang, D. (2013). BR-SIGNALING KINASE1 physically associates with FLAGELLIN SENSING2 and regulates plant innate immunity in Arabidopsis. Plant Cell 25, 1143–1157.
Shiu, S.H., and Bleecker, A.B. (2001). Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98, 10763–10768.
Song, C., and Yang, B. (2010). Mutagenesis of 18 type III effectors reveals virulence function of XopZ (PXO99) in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 23, 893–902.
Sun, Y., Li, L., Macho, A.P., Han, Z., Hu, Z., Zipfel, C., Zhou, J.M., and Chai, J. (2013). Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342, 624–628.
Üstün, S., Bartetzko, V., and Börnke, F. (2013). The Xanthomonas campestris type III effector XopJ targets the host cell proteasome to suppress salicylic-acid mediated plant defence. PLoS Pathog 9, e1003427.
Wu, Y., and Zhou, J.M. (2013). Receptor-like kinases in plant innate immunity. J Integr Plant Biol 55, 1271–1286.
Xiang, T., Zong, N., Zou, Y., Wu, Y., Zhang, J., Xing, W., Li, Y., Tang, X., Zhu, L., Chai, J., and Zhou, J.M. (2008). Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18, 74–80.
Xiao, F., Giavalisco, P., and Martin, G.B. (2007). Pseudomonas syringae type III effector AvrPtoB is phosphorylated in plant cells on serine 258, promoting its virulence activity. J Biol Chem 282, 30737–30744.
Zhang, J., Li, W., Xiang, T., Liu, Z., Laluk, K., Ding, X., Zou, Y., Gao, M., Zhang, X., Chen, S., Mengiste, T., Zhang, Y., Zhou, J.M. (2010). Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7, 290–301.
Zhang, J., and Zhou, J.M. (2010). Plant immunity triggered by microbial molecular signatures. Mol Plant 3, 783–793.
Zhang, Y., Su, J.B., Duan, S., Ao, Y., Dai, J.R., Liu, J., Wang, P., Li, Y.G., Liu, B., Feng, D.R., Wang, J.F., and Wang, H.B. (2011). A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods 7, 30.
Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J.D.G., Boller, T., and Felix, G. (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749–760.
Zuo, J.R., Niu, Q.W., and Chua, N.H. (2000). An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24, 265–273.
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at springerlink.fh-diploma.de
Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0), which permits use, duplication, adaptation, distribution, and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Wang, S., Sun, J., Fan, F. et al. A Xanthomonas oryzae pv. oryzae effector, XopR, associates with receptor-like cytoplasmic kinases and suppresses PAMP-triggered stomatal closure. Sci. China Life Sci. 59, 897–905 (2016). https://doi.org/10.1007/s11427-016-5106-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-016-5106-6