Browse > Article
http://dx.doi.org/10.14348/molcells.2021.0100

Synaptotagmin 5 Controls SYP132-VAMP721/722 Interaction for Arabidopsis Immunity to Pseudomonas syringae pv tomato DC3000  

Kim, Soohong (Department of Molecular Biology, Dankook University)
Kim, Hyeran (Department of Biological Sciences, Kangwon National University)
Park, Keunchun (Department of Molecular Biology, Dankook University)
Cho, Da Jeong (Department of Molecular Biology, Dankook University)
Kim, Mi Kyung (Department of Molecular Biology, Dankook University)
Kwon, Chian (Department of Molecular Biology, Dankook University)
Yun, Hye Sup (Department of Biological Sciences, Konkuk University)
Publication Information
Molecules and Cells / v.44, no.9, 2021 , pp. 670-679 More about this Journal
Abstract
Vesicle-associated membrane proteins 721 and 722 (VAMP721/722) are secretory vesicle-localized arginine-conserved soluble N-ethylmaleimide-sensitive factor attachment protein receptors (R-SNAREs) to drive exocytosis in plants. They are involved in diverse physiological processes in plants by interacting with distinct plasma membrane (PM) syntaxins. Here, we show that synaptotagmin 5 (SYT5) is involved in plant defense against Pseudomonas syringae pv tomato (Pst) DC3000 by regulating SYP132-VAMP721/722 interactions. Calcium-dependent stimulation of in vitro SYP132-VAMP722 interaction by SYT5 and reduced in vivo SYP132-VAMP721/722 interaction in syt5 plants suggest that SYT5 regulates the interaction between SYP132 and VAMP721/722. We interestingly found that disease resistance to Pst DC3000 bacterium but not to Erysiphe pisi fungus is compromised in syt5 plants. Since SYP132 plays an immune function to bacteria, elevated growth of surface-inoculated Pst DC3000 in VAMP721/722-deficient plants suggests that SYT5 contributes to plant immunity to Pst DC3000 by promoting the SYP132-VAMP721/722 immune secretory pathway.
Keywords
plant immunity; Pst DC3000; SYP132; SYT5; VAMP721/722;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Karnahl, M., Park, M., Krause, C., Hiller, U., Mayer, U., Stierhof, Y.D., and Jurgens, G. (2018). Functional diversification of Arabidopsis SEC1-related SM proteins in cytokinetic and secretory membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 115, 6309-6314.   DOI
2 Karnik, R., Grefen, C., Bayne, R., Honsbein, A., Kohler, T., Kioumourtzoglou, D., Williams, M., Bryant, N.J., and Blatt, M.R. (2013). Arabidopsis Sec1/Munc18 protein SEC11 is a competitive and dynamic modulator of SNARE binding and SYP121-dependent vesicle traffic. Plant Cell 25, 1368-1382.   DOI
3 Karnik, R., Zhang, B., Waghmare, S., Aderhold, C., Grefen, C., and Blatt, M.R. (2015). Binding of SEC11 indicates its role in SNARE recycling after vesicle fusion and identifies two pathways for vesicular traffic to the plasma membrane. Plant Cell 27, 675-694.   DOI
4 Kim, H., Kwon, H., Kim, S., Kim, M.K., Botella, M.A., Yun, H.S., and Kwon, C. (2016). Synaptotagmin 1 negatively controls the two distinct immune secretory pathways to powdery mildew fungi in Arabidopsis. Plant Cell Physiol. 57, 1133-1141.   DOI
5 Jahn, R. and Scheller, R.H. (2006). SNAREs--engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643.   DOI
6 Bestwick, C.S., Brown, I.R., Bennett, M.H., and Mansfield, J.W. (1997). Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9, 209-221.   DOI
7 Bohlenius, H., Morch, S.M., Godfrey, D., Nielsen, M.E., and Thordal-Christensen, H. (2010). The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxindependent preinvasive basal defense in barley. Plant Cell 22, 3831-3844.   DOI
8 Kwon, H., Cho, D.J., Lee, H., Nam, M.H., Kwon, C., and Yun, H.S. (2020b). CCOAOMT1, a candidate cargo secreted via VAMP721/722 secretory vesicles in Arabidopsis. Biochem. Biophys. Res. Commun. 524, 977-982.   DOI
9 Koh, S., Andre, A., Edwards, H., Ehrhardt, D., and Somerville, S. (2005). Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J. 44, 516-529.   DOI
10 Kwon, C., Lee, J.H., and Yun, H.S. (2020a). SNAREs in plant biotic and abiotic stress responses. Mol. Cells 43, 501-508.   DOI
11 Lee, E., Santana, B.V.N., Samuels, E., Benitez-Fuente, F., Corsi, E., Botella, M.A., Perez-Sancho, J., Vanneste, S., Friml, J., Macho, A., et al. (2020). Rare earth elements induce cytoskeleton-dependent and PI4P-associated rearrangement of SYT1/SYT5 endoplasmic reticulum-plasma membrane contact site complexes in Arabidopsis. J. Exp. Bot. 71, 3986-3998.   DOI
12 Lewis, J.D. and Lazarowitz, S.G. (2010). Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc. Natl. Acad. Sci. U. S. A. 107, 2491-2496.   DOI
13 Lipka, V., Kwon, C., and Panstruga, R. (2007). SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu. Rev. Cell Dev. Biol. 23, 147-174.   DOI
14 Yi, C., Park, S., Yun, H.S., and Kwon, C. (2013). Vesicle-associated membrane proteins 721 and 722 are required for unimpeded growth of Arabidopsis under ABA application. J. Plant Physiol. 170, 529-533.   DOI
15 Waghmare, S., Lefoulon, C., Zhang, B., Liliekyte, E., Donald, N., and Blatt, M.R. (2019). K+ Channel-SEC11 binding exchange regulates SNARE assembly for secretory traffic. Plant Physiol. 181, 1096-1113.   DOI
16 Wang, H., Han, S., Siao, W., Song, C., Xiang, Y., Wu, X., Cheng, P., Li, H., Jasik, J., Micieta, K., et al. (2015). Arabidopsis synaptotagmin 2 participates in pollen germination and tube growth and is delivered to plasma membrane via conventional secretion. Mol. Plant 8, 1737-1750.   DOI
17 Yamazaki, T., Kawamura, Y., Minami, A., and Uemura, M. (2008). Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20, 3389-3404.   DOI
18 Takemoto, D., Jones, D.A., and Hardham, A.R. (2003). GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J. 33, 775-792.   DOI
19 Schapire, A.L., Voigt, B., Jasik, J., Rosado, A., Lopez-Cobollo, R., Menzel, D., Salinas, J., Mancuso, S., Valpuesta, V., Baluska, F., et al. (2008). Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20, 3374-3388.   DOI
20 Sogawa, A., Yamazaki, A., Yamasaki, H., Komi, M., Manabe, T., Tajima, S., Hayashi, M., and Nomura, M. (2019). SNARE proteins LjVAMP72a and LjVAMP72b are required for root symbiosis and root hair formation in Lotus japonicus. Front. Plant Sci. 9, 1992.   DOI
21 Kim, S., Choi, Y., Kwon, C., and Yun, H.S. (2019). Endoplasmic reticulum stress-induced accumulation of VAMP721/722 requires CALRETICULIN 1 and CALRETICULIN 2 in Arabidopsis. J. Integr. Plant Biol. 61, 974-980.   DOI
22 Yu, X., Lund, S.P., Scott, R.A., Greenwald, J.W., Records, A.H., Nettleton, D., Lindow, S.E., Gross, D.C., and Beattie, G.A. (2013). Transcriptional responses of Pseudomonas syringae to growth in epiphytic versus apoplastic leaf sites. Proc. Natl. Acad. Sci. U. S. A. 110, E425-E434.   DOI
23 Zhang, B., Karnik, R., Alvim, J., Donald, N., and Blatt, M.R. (2019). Dual sites for SEC11 on the SNARE SYP121 implicate a binding exchange during secretory traffic. Plant Physiol. 180, 228-239.   DOI
24 Pajonk, S., Kwon, C., Clemens, N., Panstruga, R., and Schulze-Lefert, P. (2008). Activity determinants and functional specialization of Arabidopsis PEN1 syntaxin in innate immunity. J. Biol. Chem. 283, 26974-26984.   DOI
25 Perez-Sancho, J., Vanneste, S., Lee, E., McFarlane, H.E., Esteban Del Valle, A., Valpuesta, V., Friml, J., Botella, M.A., and Rosado, A. (2015). The Arabidopsis synaptotagmin1 is enriched in endoplasmic reticulum-plasma membrane contact sites and confers cellular resistance to mechanical stresses. Plant Physiol. 168, 132-143.   DOI
26 Reichardt, I., Slane, D., El Kasmi, F., Knoll, C., Fuchs, R., Mayer, U., Lipka, V., and Jurgens, G. (2011). Mechanisms of functional specificity among plasma-membrane syntaxins in Arabidopsis. Traffic 12, 1269-1280.   DOI
27 Sauer, M., Paciorek, T., Benkova, E., and Friml, J. (2006). Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nat. Protoc. 1, 98-103.   DOI
28 Li, Y., Zhang, Y., Wang, Q.X., Wang, T.T., Cao, X.L., Zhao, Z.X., Zhao, S.L., Xu, Y.J., Xiao, Z.Y., Li, J.L., et al. (2018). RESISTANCE TO POWDERY MILDEW8.1 boosts pattern-triggered immunity against multiple pathogens in Arabidopsis and rice. Plant Biotechnol. J. 16, 428-441.   DOI
29 Xing, J., Li, X., Wang, X., Lv, X., Wang, L., Zhang, L., Zhu, Y., Shen, Q., Baluska, F., Samaj, J., et al. (2019). Secretion of phospholipase D functions as a regulatory mechanism in plant innate immunity. Plant Cell 31, 3015-3032.   DOI
30 Yun, H.S. and Kwon, C. (2017). Vesicle trafficking in plant immunity. Curr. Opin. Plant Biol. 40, 34-42.   DOI
31 Levy, A., Zheng, J.Y., and Lazarowitz, S.G. (2015). Synaptotagmin SYTA forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr. Biol. 25, 2018-2025.   DOI
32 Johansson, O.N., Fahlberg, P., Karimi, E., Nilsson, A.K., Ellerstrom, M., and Andersson, M.X. (2014). Redundancy among phospholipase D isoforms in resistance triggered by recognition of the Pseudomonas syringae effector AvrRpm1 in Arabidopsis thaliana. Front. Plant Sci. 5, 639.
33 Kikuma, K., Li, X., Kim, D., Sutter, D., and Dickman, D.K. (2017). Extended synaptotagmin localizes to presynaptic ER and promotes neurotransmission and synaptic growth in Drosophila. Genetics 207, 993-1006.   DOI
34 Kwon, C., Neu, C., Pajonk, S., Yun, H.S., Lipka, U., Humphry, M., Bau, S., Straus, M., Kwaaitaal, M., Rampelt, H., et al. (2008). Co-option of a default secretory pathway for plant immune responses. Nature 451, 835-840.   DOI
35 Lee, M.H., Jeon, H.S., Kim, S.H., Chung, J.H., Roppolo, D., Lee, H.J., Cho, H.J., Tobimatsu, Y., Ralph, J., and Park, O.K. (2019). Lignin-based barrier restricts pathogens to the infection site and confers resistance in plants. EMBO J. 38, e101948.
36 Schreiber, K., Ckurshumova, W., Peek, J., and Desveaux, D. (2008). A high-throughput chemical screen for resistance to Pseudomonas syringae in Arabidopsis. Plant J. 54, 522-531.   DOI
37 Wang, P., Pleskot, R., Zang, J., Winkler, J., Wang, J., Yperman, K., Zhang, T., Wang, K., Gong, J., Guan, Y., et al. (2019). Plant AtEH/Pan1 proteins drive autophagosome formation at ER-PM contact sites with actin and endocytic machinery. Nat. Commun. 10, 5132.   DOI
38 Kalde, M., Nuhse, T.S., Findlay, K., and Peck, S.C. (2007). The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc. Natl. Acad. Sci. U. S. A. 104, 11850-11855.   DOI
39 Khare, S., Singh, N.B., Singh, A., Hussain, I., Niharika, K., Yadav, V., Bano, C., Yadav, R.K., and Amist, N. (2020). Plant secondary metabolites synthesis and their regulations under biotic and abiotic constraints. J. Plant Biol. 63, 203-216.   DOI
40 El Kasmi, F., Krause, C., Hiller, U., Stierhof, Y.D., Mayer, U., Conner, L., Kong, L., Reichardt, I., Sanderfoot, A.A., and Jurgens, G. (2013). SNARE complexes of different composition jointly mediate membrane fusion in Arabidopsis cytokinesis. Mol. Biol. Cell 24, 1593-1601.   DOI
41 Uemura, T., Nakano, R.T., Takagi, J., Wang, Y., Kramer, K., Finkemeier, I., Nakagami, H., Tsuda, K., Ueda, T., Schulze-Lefert, P., et al. (2019). A Golgi-released subpopulation of the trans-Golgi network mediates protein secretion in Arabidopsis. Plant Physiol. 179, 519-532.   DOI
42 Nielsen, M.E., Feechan, A., Bohlenius, H., Ueda, T., and Thordal-Christensen, H. (2012). Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc. Natl. Acad. Sci. U. S. A. 109, 11443-11448.   DOI
43 Park, M., Touihri, S., Muller, I., Mayer, U., and Jurgens, G. (2012). Sec1/Munc18 protein stabilizes fusion-competent syntaxin for membrane fusion in Arabidopsis cytokinesis. Dev. Cell 22, 989-1000.   DOI
44 Saheki, Y. and De Camilli, P. (2017). The extended-synaptotagmins. Biochim. Biophys. Acta Mol. Cell Res. 1864, 1490-1493.   DOI
45 Yamazaki, T., Takata, N., Uemura, M., and Kawamura, Y. (2010). Arabidopsis synaptotagmin SYT1, a type I signal-anchor protein, requires tandem C2 domains for delivery to the plasma membrane. J. Biol. Chem. 285, 23165-23176.   DOI
46 Yun, H.S., Kwaaitaal, M., Kato, N., Yi, C., Park, S., Sato, M.H., Schulze-Lefert, P., and Kwon, C. (2013). Requirement of vesicle-associated membrane protein 721 and 722 for sustained growth during immune responses in Arabidopsis. Mol. Cells 35, 481-488.   DOI
47 Zhang, H., Zhang, L., Gao, B., Fan, H., Jin, J., Botella, M.A., Jiang, L., and Lin, J. (2011). Golgi apparatus-localized synaptotagmin 2 is required for unconventional secretion in Arabidopsis. PLoS One 6, e26477.   DOI
48 Ebine, K., Fujimoto, M., Okatani, Y., Nishiyama, T., Goh, T., Ito, E., Dainobu, T., Nishitani, A., Uemura, T., Sato, M.H., et al. (2011). A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat. Cell Biol. 13, 853-859.   DOI
49 Chezem, W.R., Memon, A., Li, F.S., Weng, J.K., and Clay, N.K. (2017). SG2-Type R2R3-MYB transcription factor MYB15 controls defense-induced lignification and basal immunity in Arabidopsis. Plant Cell 29, 1907-1926.   DOI
50 Collins, N.C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J.L., Huckelhoven, R., Stein, M., Freialdenhoven, A., Somerville, S.C., et al. (2003). SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973-977.   DOI
51 El Kasmi, I., Khadivjam, B., Lackman, M., Duron, J., Bonneil, E., Thibault, P., and Lippe, R. (2018). Extended synaptotagmin 1 interacts with herpes simplex virus 1 glycoprotein M and negatively modulates virus-induced membrane fusion. J. Virol. 92, e01281-17.
52 Ichikawa, M., Hirano, T., Enami, K., Fuselier, T., Kato, N., Kwon, C., Voigt, B., Schulze-Lefert, P., Baluska, F., and Sato, M.H. (2014). Syntaxin of plant proteins SYP123 and SYP132 mediate root hair tip growth in Arabidopsis thaliana. Plant Cell Physiol. 55, 790-800.   DOI
53 Kim, H., O'Connell, R., Maekawa-Yoshikawa, M., Uemura, T., Neumann, U., and Schulze-Lefert, P. (2014). The powdery mildew resistance protein RPW8.2 is carried on VAMP721/722 vesicles to the extrahaustorial membrane of haustorial complexes. Plant J. 79, 835-847.   DOI
54 Ivanov, S., Fedorova, E.E., Limpens, E., De Mita, S., Genre, A., Bonfante, P., and Bisseling, T. (2012). Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc. Natl. Acad. Sci. U. S. A. 109, 8316-8321.   DOI
55 Ishikawa, K., Tamura, K., Fukao, Y., and Shimada, T. (2020). Structural and functional relationships between plasmodesmata and plant endoplasmic reticulum-plasma membrane contact sites consisting of three synaptotagmins. New Phytol. 226, 798-808.   DOI