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http://dx.doi.org/10.14348/molcells.2019.2433

Role of RIN4 in Regulating PAMP-Triggered Immunity and Effector-Triggered Immunity: Current Status and Future Perspectives  

Ray, Sujit Kumar (College of Pharmacy, Research Institute of Pharmaceutical Science, and Plant Molecular Biology and Biotechnology Research Center (PMBBRC), Gyeongsang National University)
Macoy, Donah Mary (College of Pharmacy, Research Institute of Pharmaceutical Science, and Plant Molecular Biology and Biotechnology Research Center (PMBBRC), Gyeongsang National University)
Kim, Woe-Yeon (Division of Applied Life Science (BK21 Plus), Plant Molecular Biology and Biotechnology Research Center (PMBBRC), Research Institute of Life Science (RILS), Gyeongsang National University)
Lee, Sang Yeol (Division of Applied Life Sciences (BK21 Plus), Graduate School of Gyeongsang National University)
Kim, Min Gab (College of Pharmacy, Research Institute of Pharmaceutical Science, and Plant Molecular Biology and Biotechnology Research Center (PMBBRC), Gyeongsang National University)
Publication Information
Molecules and Cells / v.42, no.7, 2019 , pp. 503-511 More about this Journal
Abstract
As sessile organisms, plants have developed sophisticated system to defend themselves against microbial attack. Since plants do not have specialized immune cells, all plant cells appear to have the innate ability to recognize pathogens and turn on an appropriate defense response. The plant innate immune system has two major branches: PAMPs (pathogen associated molecular patterns)-triggered immunity (PTI) and effector-triggered immunity (ETI). The ability to discriminate between self and non-self is a fundamental feature of living organisms, and it is a prerequisite for the activation of plant defenses specific to microbial infection. Arabidopsis cells express receptors that detect extracellular molecules or structures of the microbes, which are called collectively PAMPs and activate PTI. However, nucleotidebinding site leucine-rich repeats (NB-LRR) proteins mediated ETI is induced by direct or indirect recognition of effector molecules encoded by avr genes. In Arabidopsis, plasmamembrane localized multifunctional protein RIN4 (RPM1-interacting protein 4) plays important role in both PTI and ETI. Previous studies have suggested that RIN4 functions as a negative regulator of PTI. In addition, many different bacterial effector proteins modify RIN4 to destabilize plant immunity and several NB-LRR proteins, including RPM1 (resistance to Pseudomonas syringae pv. maculicola 1), RPS2 (resistance to P. syringae 2) guard RIN4. This review summarizes the current studies that have described signaling mechanism of RIN4 function, modification of RIN4 by bacterial effectors and different interacting partner of RIN4 in defense related pathway. In addition, the emerging role of the RIN4 in plant physiology and intercellular signaling as it presents in exosomes will be discussed.
Keywords
AvrB; AvrRpm1; AvrRpt2; effector-triggered immunity; PAMP-triggered immunity; RIN4;
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1 Cui, H., Wang, Y., Xue, L., Chu, J., Yan, C., Fu, J., Chen, M., Innes, R.W., and Zhou, J.M. (2010). Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe 7, 164-175.   DOI
2 Day, B., Dahlbeck, D., Huang, J., Chisholm, S.T., Li, D., and Staskawicz, B.J. (2005). Molecular basis for the RIN4 negative regulation of RPS2 disease resistance. Plant Cell 17, 1292-1305.   DOI
3 Day, B., Dahlbeck, D., and Staskawicz, B.J. (2006). NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 18, 2782-2791.   DOI
4 Desveaux, D., Singer, A.U., Wu, A.J., McNulty, B.C., Musselwhite, L., Nimchuk, Z., Sondek, J., and Dangl, J.L. (2007). Type III effector activation via nucleotide binding, phosphorylation, and host target interaction. PLoS Pathog. 3, e48.   DOI
5 Esch, L. and Schaffrath, U. (2017). An update on jacalin-like lectins and their role in plant defense. Int. J. Mol. Sci. 18, E1592.   DOI
6 Ferreira, P.A., Nakayama, T.A., Pak, W.L., and Travis, G.H. (1996). Cyclophilinrelated protein RanBP2 acts as chaperone for red/green opsin. Nature 383, 637-640.   DOI
7 Geng, X., Shen, M., Kim, J.H., and Mackey, D. (2016). The Pseudomonas syringae type III effectors AvrRpm1 and AvrRpt2 promote virulence dependent on the F-box protein COI1. Plant Cell Rep. 35, 921-932.   DOI
8 Hurley, B., Lee, D., Mott, A., Wilton, M., Liu, J., Liu, Y.C., Angers, S., Coaker, G., Guttman, D.S., and Desveaux, D. (2014). The Pseudomonas syringae type III effector HopF2 suppresses Arabidopsis stomatal immunity. PLoS One 9, e114921.   DOI
9 Jin, P., Wood, M.D., Wu, Y., Xie, Z., and Katagiri, F. (2003). Cleavage of the Pseudomonas syringae type III effector AvrRpt2 requires a host factor(s) common among eukaryotes and is important for AvrRpt2 localization in the host cell. Plant Physiol. 133, 1072-1082.   DOI
10 Johnson, D.R., Bhatnagar, R.S., Knoll, L.J., and Gordon, J.I. (1994). Genetic and biochemical studies of protein N-myristoylation. Annu. Rev. Biochem. 63, 869-914.   DOI
11 Jones, J.D. and Dangl, J.L. (2006). The plant immune system. Nature 444, 323-329.   DOI
12 Kim, H.S., Desveaux, D., Singer, A.U., Patel, P., Sondek, J., and Dangl, J.L. (2005a). The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc. Natl. Acad. Sci. U. S. A. 102, 6496-6501.   DOI
13 Kim, M.G., da Cunha, L., McFall, A.J., Belkhadir, Y., DebRoy, S., Dangl, J.L., and Mackey, D. (2005b). Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121, 749-759.   DOI
14 Lee, D., Bourdais, G., Yu, G., Robatzek, S., and Coaker, G. (2015). Phosphorylation of the plant immune regulator RPM1-INTERACTING PROTEIN4 enhances plant plasma membrane H+-ATPase activity and inhibits flagellin-triggered immune responses in Arabidopsis. Plant Cell 27, 2042-2056.   DOI
15 Robert-Seilaniantz, A., Shan, L., Zhou, J.M., and Tang, X. (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.   DOI
16 Nimchuk, Z., Marois, E., Kjemtrup, S., Leister, R.T., Katagiri, 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.   DOI
17 Oerke, E.C. (2006). Crop losses to pests. J Agric Sci 144, 31-43.   DOI
18 Raffaele, S., Mongrand, S., Gamas, P., Niebel, A., and Ott, T. (2007). Genome-wide annotation of remorins, a plant-specific protein family: evolutionary and functional perspectives. Plant Physiol. 145, 593-600.   DOI
19 Russell, A.R., Ashfield, T., and Innes, R.W. (2015). Pseudomonas syringae effector AvrPphB suppresses AvrB-induced activation of RPM1 but not AvrRpm1-induced activation. Mol. Plant Microbe Interact. 28, 727-735.   DOI
20 Li, M., Ma, X., Chiang, Y.H., Yadeta, K.A., Ding, P., Dong, L., Zhao, Y., Li, X., Yu, Y., Zhang, L., et al. (2014). Proline isomerization of the immune receptorinteracting protein RIN4 by a cyclophilin inhibits effector-triggered immunity in Arabidopsis. Cell Host Microbe 16, 473-483.   DOI
21 Sabol, P., Kulich, I., and Zarsky, V. (2017). RIN4 recruits the exocyst subunit EXO70B1 to the plasma membrane. J. Exp. Bot. 68, 3253-3265.   DOI
22 Sarris, P.F., Duxbury, Z., Huh, S.U., Ma, Y., Segonzac, C., Sklenar, J., Derbyshire, P., Cevik, V., Rallapalli, G., Saucet, S.B., et al. (2015). A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161, 1089-1100.   DOI
23 Nicaise, V., Roux, M., and Zipfel, C. (2009). Recent advances in PAMPtriggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol. 150, 1638-1647.   DOI
24 Schulze-Lefert, P. and Panstruga, R. (2003). Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu. Rev. Phytopathol. 41, 641-667.   DOI
25 Luo, J., Fuell, C., Parr, A., Hill, L., Bailey, P., Elliott, K., Fairhurst, S.A., Martin, C., and Michael, A.J. (2009a). A novel polyamine acyltransferase responsible for the accumulation of spermidine conjugates in Arabidopsis seed. Plant Cell 21, 318-333.   DOI
26 Liu, J., Elmore, J.M., and Coaker, G. (2009a). Investigating the functions of the RIN4 protein complex during plant innate immune responses. Plant Signal. Behav. 4, 1107-1110.   DOI
27 Liu, J., Elmore, J.M., Fuglsang, A.T., Palmgren, M.G., Staskawicz, B.J., and Coaker, G. (2009b). RIN4 functions with plasma membrane $H^+$-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol. 7, e1000139.   DOI
28 Liu, J., Elmore, J.M., Lin, Z.J., and Coaker, G. (2011). A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9, 137-146.   DOI
29 Luo, Y., Caldwell, K.S., Wroblewski, T., Wright, M.E. and Michelmore, R.W. (2009b) Proteolysis of a negative regulator of innate immunity is dependent on resistance genes in tomato and Nicotiana benthamiana and induced by multiple bacterial effectors. The Plant Cell 21, 2458-2472.   DOI
30 Shang, Y., Li, X., Cui, H., He, P., Thilmony, R., Chintamanani, S., Zwiesler-Vollick, J., Gopalan, S., Tang, X., and Zhou, J.M. (2006). RAR1, a central player in plant immunity, is targeted by Pseudomonas syringae effector AvrB. Proc. Natl. Acad. Sci. U. S. A. 103, 19200-19205.   DOI
31 Song, G.C. and Ryu, C.M. (2018). Evidence for volatile memory in plants: boosting defence priming through the recurrent application of plant volatiles. Mol. Cells 41, 724-732.   DOI
32 Tornero, P. and Dangl, J.L. (2001). A high-throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana. Plant J. 28, 475-481.   DOI
33 Wilton, M., Subramaniam, R., Elmore, J., Felsensteiner, C., Coaker, G., and Desveaux, D. (2010). The type III effector HopF2 Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Proc. Natl. Acad. Sci. U. S. A. 107, 2349-2354.   DOI
34 Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R., and Dangl, J.L. (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379-389.   DOI
35 Mackey, D., Holt, B.F., Wiig, A., and Dangl, J.L. (2002). RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743-754.   DOI
36 Muskett, P.R., Kahn, K., Austin, M.J., Moisan, L.J., Sadanandom, A., Shirasu, K., Jones, J.D., and Parker, J.E. (2002). Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. Plant Cell 14, 979-992.   DOI
37 Toruno, T.Y., Shen, M., Coaker, G., and Mackey, D. (2019). Regulated disorder: posttranslational modifications control the RIN4 plant immune signaling hub. Mol. Plant Microbe Interact. 32, 56-64.   DOI
38 van der Hoorn, R.A. and Kamoun, S. (2008). From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20, 2009-2017.   DOI
39 Zhang, J., Li, W., Xiang, T., Liu, Z., Laluk, K., Ding, X., Zou, Y., Gao, M., Zhang, X., Chen, S., et al. (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.   DOI
40 Zipfel, C. and Felix, G. (2005). Plants and animals: a different taste for microbes? Curr. Opin. Plant Biol. 8, 353-360.   DOI
41 Axelsen, K.B., Venema, K., Jahn, T., Baunsgaard, L., and Palmgren, M.G. (1999). Molecular dissection of the C-terminal regulatory domain of the plant plasma membrane H+-ATPase AHA2: mapping of residues that when altered give rise to an activated enzyme. Biochemistry 38, 7227-7234.   DOI
42 Afzal, A.J., da Cunha, L., and Mackey, D. (2011). Separable fragments and membrane tethering of Arabidopsis RIN4 regulate its suppression of PAMP-triggered immunity. Plant Cell 23, 3798-3811.   DOI
43 Allegre, M., Daire, X., Héloir, M.C., Trouvelot, S., Mercier, L., Adrian, M., and Pugin, A. (2007). Stomatal deregulation in Plasmopara viticola‐infected grapevine leaves. New Phytol. 173, 832-840.   DOI
44 Anstead, J.A., Froelich, D.R., Knoblauch, M., and Thompson, G.A. (2012). Arabidopsis P-protein filament formation requires both AtSEOR1 and AtSEOR2. Plant Cell Physiol. 53, 1033-1042.   DOI
45 Chung, E.H., El-Kasmi, F., He, Y., Loehr, A., and Dangl, J.L. (2014). A plant phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 16, 484-494.   DOI
46 Axtell, M.J., Chisholm, S.T., Dahlbeck, D., and Staskawicz, B.J. (2003). Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol. Microbiol. 49, 1537-1546.   DOI
47 Belkhadir, Y., Nimchuk, Z., Hubert, D.A., Mackey, D., and Dangl, J.L. (2004). Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16, 2822-2835.   DOI
48 Cherkis, K.A., Temple, B.R., Chung, E.H., Sondek, J., and Dangl, J.L. (2012). AvrRpm1 missense mutations weakly activate RPS2-mediated immune response in Arabidopsis thaliana. PLoS One 7, e42633.   DOI
49 Chisholm, S.T., Dahlbeck, D., Krishnamurthy, N., Day, B., Sjolander, K., and Staskawicz, B.J. (2005). Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proc. Natl. Acad. Sci. U. S. A. 102, 2087-2092.   DOI
50 Chung, E.H., da Cunha, L., Wu, A.J., Gao, Z., Cherkis, K., Afzal, A.J., Mackey, D., and Dangl, J.L. (2011). Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe 9, 125-136.   DOI
51 Coaker, G., Falick, A., and Staskawicz, B. (2005). Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308, 548-550.   DOI
52 Coppinger, P., Repetti, P.P., Day, B., Dahlbeck, D., Mehlert, A., and Staskawicz, B.J. (2004). Overexpression of the plasma membranelocalized NDR1 protein results in enhanced bacterial disease resistance in Arabidopsis thaliana. Plant J. 40, 225-237.   DOI