Browse > Article
http://dx.doi.org/10.14348/molcells.2020.0007

SNAREs in Plant Biotic and Abiotic Stress Responses  

Kwon, Chian (Department of Molecular Biology, Dankook University)
Lee, Jae-Hoon (Department of Biology Education, Pusan National University)
Yun, Hye Sup (Department of Biological Sciences, Konkuk University)
Abstract
In eukaryotes, membraneous cellular compartmentation essentially requires vesicle trafficking for communications among distinct organelles. A donor organelle-generated vesicle releases its cargo into a target compartment by fusing two distinct vesicle and target membranes. Vesicle fusion, the final step of vesicle trafficking, is driven intrinsically by complex formation of soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs). Although SNAREs are well-conserved across eukaryotes, genomic studies revealed that plants have dramatically increased the number of SNARE genes than other eukaryotes. This increase is attributed to the sessile nature of plants, likely for more sensitive and harmonized responses to environmental stresses. In this review, we therefore try to summarize and discuss the current understanding of plant SNAREs function in responses to biotic and abiotic stresses.
Keywords
abiotic stress; biotic stress; plant; SNARE; trafficking;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Wang, P., Sun, Y., Pei, Y., Li, X., Zhang, X., Li, F., and Hou, Y. (2018). GhSNAP33, a t-SNARE protein from Gossypium hirsutum, mediates resistance to Verticillium dahliae infection and tolerance to drought stress. Front. Plant Sci. 9, 896.
2 Hanson, P.I., Heuser, J.E., and Jahn, R. (1997). Neurotransmitter release - four years of SNARE complexes. Curr. Opin. Neurobiol. 7, 310-315.   DOI
3 Heese, M., Gansel, X., Sticher, L., Wick, P., Grebe, M., Granier, F., and Jurgens, G. (2001). Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J. Cell Biol. 155, 239-249.   DOI
4 Hong, W. (2005). SNAREs and traffic. Biochim. Biophys. Acta 1744, 120-144.   DOI
5 Honsbein, A., Sokolovski, S., Grefen, C., Campanoni, P., Pratelli, R., Panaque, M., Chen, Z., Johansson, I., and Blatt, M.R. (2009). A tripartite SNARE-$K^+$ channel complex mediates in channel-dependent $K^+$ nutrition in Arabidopsis. Plant Cell 21, 2859-2877.   DOI
6 Jahn, R. and Scheller, R.H. (2006). SNAREs--engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643.   DOI
7 Jones, J.D. and Dangl, J.L. (2006). The plant immune system. Nature 444, 323-329.   DOI
8 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
9 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
10 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
11 Wang, P., Zhang, X., Ma, X., Sun, Y., Liu, N., Li, F., and Hou, Y. (2017). Identification of CkSNAP33, a gene encoding synaptosomal-associated protein from Cynanchum komarovii, that enhances Arabidopsis resistance to Verticillium dahliae. PLoS One 12, e0178101.   DOI
12 Xu, Q.J., Wang, Y.L., Wei, Z.X., Yuan, H.J., Zeng, X.Q., and Tashi, N. (2017). Cloning and functional characterization of the HbSYR1 gene encoding a syntaxin-related protein in Tibetan hulless barley (Hordeum vulgare L. var. nudum HK. f.). Genet. Mol. Res. 16, gmr16038909.
13 Xue, Y., Yang, Y., Yang, Z., Wang, X., and Guo, Y. (2018). VAMP711 is required for abscisic acid-mediated inhibition of plasma membrane H(+)- ATPase activity. Plant Physiol. 178, 1332-1343.   DOI
14 Yang, X., Liao, C.Y., Tang, J., and Bassham, D.C. (2019). Overexpression of trans-Golgi network t-SNAREs rescues vacuolar trafficking and TGN morphology defects in a putative tethering factor mutant. Plant J. 99, 703-716.   DOI
15 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
16 Yun, H.S., Kwaaitaal, M., Kato, N., Yi, C., Park, S., Sato, M.H., Schulze-Lefert, P., and Kwon, C. (2013a). Requirement of vesicle-associated membrane protein 721 and 722 for sustained growth during immune responses in Arabidopsis. Mol. Cells 35, 481-488.   DOI
17 Kwon, C., Bednarek, P., and Schulze-Lefert, P. (2008a). Secretory pathways in plant immune responses. Plant Physiol. 147, 1575-1583.   DOI
18 Yun, H.S. and Kwon, C. (2017). Vesicle trafficking in plant immunity. Curr. Opin. Plant Biol. 40, 34-42.   DOI
19 Yun, H.S., Yi, C., Kwon, H., and Kwon, C. (2013b). Model for regulation of VAMP721/722-mediated secretion: growth vs. stress responses. Plant Signal. Behav. 8, e27116.   DOI
20 Kim, S.J. and Bassham, D.C. (2011). TNO1 is involved in salt tolerance and vacuolar trafficking in Arabidopsis. Plant Physiol. 156, 514-526.   DOI
21 Kwon, C., Neu, C., Pajonk, S., Yun, H.S., Lipka, U., Humphry, M., Bau, S., Straus, M., Kwaaitaal, M., Rampelt, H., et al. (2008b). Co-option of a default secretory pathway for plant immune responses. Nature 451, 835-840.   DOI
22 Kwon, H., Cho, D.J., Lee, H., Nam, M.H., Kwon, C., and Yun, H.S. (2020). CCOAOMT1, a candidate cargo secreted via VAMP721/722 secretory vesicles in Arabidopsis. Biochem. Biophys. Res. Commun. 524, 977-982.   DOI
23 Lauber, M.H., Waizenegger, I., Steinmann, T., Schwarz, H., Mayer, U., Hwang, I., Lukowitz, W., and Jurgens, G. (1997). The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485-1493.   DOI
24 Leshem, Y., Golani, Y., Kaye, Y., and Levine, A. (2010). Reduced expression of the v-SNAREs AtVAMP71/AtVAMP7C gene family in Arabidopsis reduces drought tolerance by suppression of abscisic acid-dependent stomatal closure. J. Exp. Bot. 61, 2615-2622.   DOI
25 Lin, R.C. and Scheller, R.H. (2000). Mechanisms of synaptic vesicle exocytosis. Annu. Rev. Cell Dev. Biol. 16, 19-49.   DOI
26 Zhang, B., Karnik, R., Wang, Y., Wallmeroth, N., Blatt, M.R., and Grefen, C. (2015). The Arabidopsis R-SNARE VAMP721 interacts with KAT1 and KC1 $K^+$ channels to moderate $K^+$ current at the plasma membrane. Plant Cell 27, 1697-1717.   DOI
27 Zhang, X., Zhao, H., Gao, S., Wang, W.C., Katiyar-Agarwal, S., Huang, H.D., Raikhel, N., and Jin, H. (2011). Arabidopsis Argonaute 2 regulates innate immunity via miRNA393(*)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol. Cell 42, 356-366.   DOI
28 Zhu, J., Gong, Z., Zhang, C., Song, C.P., Damsz, B., Inan, G., Koiwa, H., Zhu, J.K., Hasegawa, P.M., and Bressan, R.A. (2002). OSM1/SYP61: a syntaxin protein in Arabidopsis controls abscisic acid-mediated and non-abscisic acid-mediated responses to abiotic stress. Plant Cell 14, 3009-3028.   DOI
29 Leshem, Y., Melamed-Book, N., Cagnac, O., Ronen, G., Nishri, Y., Solomon, M., Cohen, G., and Levine, A. (2006). Suppression of Arabidopsis vesicle- SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc. Natl. Acad. Sci. U. S. A. 103, 18008-18013.   DOI
30 Leyman, B., Geelen, D., Quintero, F.J., and Blatt, M.R. (1999). A tobacco syntaxin with a role in hormonal control of guard cell ion channels. Science 283, 537-540.   DOI
31 Chung, K.P., Zeng, Y., Li, Y., Ji, C., Xia, Y., and Jiang, L. (2018). Signal motifdependent ER export of the Qc-SNARE BET12 interacts with MEMB12 and affects PR1 trafficking in Arabidopsis. J. Cell Sci. 131, jcs202838.   DOI
32 Antonin, W., Fasshauer, D., Becker, S., Jahn, R., and Schneider, T.R. (2002). Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat. Struct. Biol. 9, 107-111.   DOI
33 Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., Landtag, J., Brandt, W., Rosahl, S., Scheel, D., et al. (2005). Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310, 1180-1183.   DOI
34 Liu, M., Peng, Y., Li, H., Deng, L., Wang, X., and Kang, Z. (2016). TaSYP71, a Qc-SNARE, contributes to wheat resistance against Puccinia striiformis f. sp. tritici. Front. Plant Sci. 7, 544.
35 Lukowitz, W., Mayer, U., and Jurgens, G. (1996). Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84, 61-71.   DOI
36 Assaad, F.F., Qiu, J.L., Youngs, H., Ehrhardt, D., Zimmerli, L., Kalde, M., Wanner, G., Peck, S.C., Edwards, H., Ramonell, K., et al. (2004). The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol. Biol. Cell 15, 5118-5129.   DOI
37 Bock, J.B., Matern, H.T., Peden, A.A., and Scheller, R.H. (2001). A genomic perspective on membrane compartment organization. Nature 409, 839-841.   DOI
38 Cao, W.L., Yu, Y., Li, M.Y., Luo, J., Wang, R.S., Tang, H.J., Huang, J., Wang, J.F., Zhang, H.S., and Bao, Y.M. (2019). OsSYP121 accumulates at fungal penetration sites and mediates host resistance to rice blast. Plant Physiol. 179, 1330-1342.   DOI
39 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
40 Dodds, P.N. and Rathjen, J.P. (2010). Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548.   DOI
41 Pant, S.R., Matsye, P.D., McNeece, B.T., Sharma, K., Krishnavajhala, A., Lawrence, G.W., and Klink, V.P. (2014). Syntaxin 31 functions in Glycine max resistance to the plant parasitic nematode Heterodera glycines. Plant Mol. Biol. 85, 107-121.   DOI
42 Muller, I., Wagner, W., Volker, A., Schellmann, S., Nacry, P., Kuttner, F., Schwarz-Sommer, Z., Mayer, U., and Jurgens, G. (2003). Syntaxin specificity of cytokinesis in Arabidopsis. Nat. Cell Biol. 5, 531-534.   DOI
43 Nisa, Z.U., Mallano, A.I., Yu, Y., Chen, C., Duan, X., Amanullah, S., Kousar, A., Baloch, A.W., Sun, X., Tabys, D., et al. (2017). GsSNAP33, a novel Glycine soja SNAP25-type protein gene: improvement of plant salt and drought tolerances in transgenic Arabidopsis thaliana. Plant Physiol. Biochem. 119, 9-20.   DOI
44 Pan, L., Yu, X., Shao, J., Liu, Z., Gao, T., Zheng, Y., Zeng, C., Liang, C., and Chen, C. (2019). Transcriptomic profiling and analysis of differentially expressed genes in asparagus bean (Vigna unguiculata ssp. sesquipedalis) under salt stress. PLoS One 14, e0219799.   DOI
45 Park, M., Krause, C., Karnahl, M., Reichardt, I., El Kasmi, F., Mayer, U., Stierhof, Y.D., Hiller, U., Strompen, G., Bayer, M., et al. (2018). Concerted action of evolutionarily ancient and novel SNARE complexes in floweringplant cytokinesis. Dev. Cell 44, 500-511.   DOI
46 Singh, D., Yadav, N.S., Tiwari, V., Agarwal, P.K., and Jha, B. (2016). A SNARElike superfamily protein SbSLSP from the halophyte Salicornia brachiata confers salt and drought tolerance by maintaining membrane stability, K(+)/Na(+) ratio, and antioxidant cachinery. Front. Plant Sci. 7, 737.
47 Piofczyk, T., Jeena, G., and Pecinka, A. (2015). Arabidopsis thaliana natural variation reveals connections between UV radiation stress and plant pathogen-like defense responses. Plant Physiol. Biochem. 93, 34-43.   DOI
48 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
49 Sanderfoot, A. (2007). Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol. 144, 6-17.   DOI
50 Singh, B., Khurana, P., Khurana, J.P., and Singh, P. (2018). Gene encoding vesicle-associated membrane protein-associated protein from Triticum aestivum (TaVAP) confers tolerance to drought stress. Cell Stress Chaperones 23, 411-428.   DOI
51 Sollner, T., Whiteheart, S.W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P., and Rothman, J.E. (1993). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.   DOI
52 Stein, M., Dittgen, J., Sanchez-Rodriguez, C., Hou, B.H., Molina, A., Schulze- Lefert, P., Lipka, V., and Somerville, S. (2006). Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18, 731-746.   DOI
53 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
54 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
55 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
56 Ebine, K., Okatani, Y., Uemura, T., Goh, T., Shoda, K., Niihama, M., Morita, M.T., Spitzer, C., Otegui, M.S., Nakano, A., et al. (2008). A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell 20, 3006-3021.   DOI
57 Eisenach, C., Chen, Z.H., Grefen, C., and Blatt, M.R. (2012). The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K(+) channel activity with vegetative growth. Plant J. 69, 241-251.   DOI
58 Fasshauer, D., Sutton, R.B., Brunger, A.T., and Jahn, R. (1998). Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl. Acad. Sci. U. S. A. 95, 15781-15786.   DOI
59 Fuchs, R., Kopischke, M., Klapprodt, C., Hause, G., Meyer, A.J., Schwarzlander, M., Fricker, M.D., and Lipka, V. (2016). Immobilized subpopulations of leaf epidermal mitochondria mediate PENETRATION2-dependent pathogen entry control in Arabidopsis. Plant Cell 28, 130-145.   DOI
60 Hachez, C., Laloux, T., Reinhardt, H., Cavez, D., Degand, H., Grefen, C., De Rycke, R., Inze, D., Blatt, M.R., Russinova, E., et al. (2014). Arabidopsis SNAREs SYP61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2;7 to modulate the cell membrane water permeability. Plant Cell 26, 3132-3147.   DOI
61 van Loon, L.C., Rep, M., and Pieterse, C.M. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135-162.   DOI
62 Sutton, R.B., Fasshauer, D., Jahn, R., and Brunger, A.T. (1998). Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395, 347-353.   DOI
63 Uemura, T., Kim, H., Saito, C., Ebine, K., Ueda, T., Schulze-Lefert, P., and Nakano, A. (2012). Qa-SNAREs localized to the trans -Golgi network regulate multiple transport pathways and extracellular disease resistance in plants. Proc. Natl. Acad. Sci. U. S. A. 109, 1784-1789.   DOI
64 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 Golgireleased subpopulation of the trans-Golgi network mediates protein secretion in Arabidopsis. Plant Physiol. 179, 519-532.   DOI
65 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
66 Waghmare, S., Liliekyte, E., Karnik, R., Goodman, J.K., Blatt, M.R., and Jones, A.M.E. (2018). SNAREs SYP121 and SYP122 mediate the secretion of distinct cargo subsets. Plant Physiol. 178, 1679-1688.   DOI
67 Wang, D., Weaver, N.D., Kesarwani, M., and Dong, X. (2005). Induction of protein secretory pathway is required for systemic acquired resistance. Science 308, 1036-1040.   DOI