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http://dx.doi.org/10.1007/s10059-009-0007-1

The Arabidopsis AtLEC Gene Encoding a Lectin-like Protein Is Up-Regulated by Multiple Stimuli Including Developmental Signal, Wounding, Jasmonate, Ethylene, and Chitin Elicitor  

Lyou, Seoung Hyun (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
Park, Hyon Jin (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
Jung, Choonkyun (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
Sohn, Hwang Bae (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
Lee, Garam (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
Kim, Chung Ho (Department of Food and Nutrition, Seowon University)
Kim, Minkyun (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
Choi, Yang Do (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
Cheong, Jong-Joo (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
Abstract
The Arabidopsis gene AtLEC (At3g15356) gene encodes a putative 30-kDa protein with a legume lectin-like domain. Likely to classic legume lectin family of genes, AtLEC is expressed in rosette leaves, primary inflorescences, and roots, as observed in Northern blot analysis. The accumulation of AtLEC transcript is induced very rapidly, within 30 min, by chitin, a fungal wall-derived oligosaccharide elictor of the plant defense response. Transgenic Arabidopsis carrying an AtLEC promoter-driven ${\beta}$-glucuronidase (GUS) construct exhibited GUS activity in the leaf veins, secondary inflorescences, carpel heads, and silique receptacles, in which no expression could be seen in Northern blot analysis. This observation suggests that AtLEC expression is induced transiently and locally during developmental processes in the absence of an external signal such as chitin. In addition, mechanically wounded sites showed strong GUS activity, indicating that the AtLEC promoter responds to jasmonate. Indeed, methyl jasmonate and ethylene exposure induced AtLEC expression within 3-6 h. Thus, the gene appears to play a role in the jasmonate-/ethylene-responsive, in addition to the chitin-elicited, defense responses. However, chitin-induced AtLEC expression was also observed in jasmonate-insensitive (coi1) and ethylene-insensitive (etr1-1) Arabidopsis mutants. Thus, it appears that chitin promotes AtLEC expression via a jasmonate- and/or ethylene-independent pathway.
Keywords
Arabidopsis; chitin; ethylene; jasmonate; lectin;
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1 Anderson, J.P., Badruzsaufari, E., Schenk, P.M., Manners, J.M., Desmond, O.J., Ehlert, C.E., Maclean, D.J., Ebert, P.R., and Kazan, K. (2004). Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16, 3460-3479   DOI   PUBMED   ScienceOn
2 Becker, W., and Apel, K. (1992). Isolation and characterization of a cDNA clone encoding a novel jasmonate-induced protein of barley (Hordeum vulgare L.). Plant Mol. Biol. 19, 1065-1067   DOI   PUBMED
3 Bleecker, A.B., and Patterson, S.E. (1997). Last exit: senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9, 1169-1179   DOI   PUBMED   ScienceOn
4 Campbell, E.J., Schenk, P.M., Kazan, K., Penninckx, I.A.M.A., Anderson, J.P., Maclean, D.J., Cammue, B.P.A., Ebert, P.R., and Manners, J.M. (2003). Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiol. 133, 1271-1284   DOI   PUBMED   ScienceOn
5 Chandra, N.R., Kumar, N., Jeyakani, J., Singh, D.D., Gowda, S.B., and Prathima, M.N. (2006) Lectindb: a plant lectin database. Glycobiology. 16, 938-946   DOI   PUBMED   ScienceOn
6 Chini, A., Fonseca, S., Fernandez, G., Adie, B., Chico, J.M., Lorenzo, O., Garcia-Casado, G., Lopez-Vidriero, I., Lozano, F.M., Ponce, M.R., et al. (2007). The JAZ family of repressors is the missing link in jasmonate signaling. Nature 448, 666-671   DOI   PUBMED   ScienceOn
7 Creelman, R.A., and Mullet, J.E. (1995). Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc. Natl. Acad. Sci. USA 92, 4114-4119   DOI   ScienceOn
8 De Souza Filho, G.A., Ferreira, B.S., Dias, J.M., Queiroz, K.S., Branco, A.T., Bressan-Smith, R.E., Oliveira, J.G., and Garcia, A.B. (2003). Accumulation of SALT protein in rice plants as a response to environmental stresses. Plant Sci. 164, 623-628   DOI   ScienceOn
9 Doares, S.H., Syrovelts, T., Weiler, E.W., and Ryan, C.A. (1995). Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 93, 4095-4098   DOI   ScienceOn
10 Farmer, E.E., and Ryan, C.A. (1992). Octadecanoid jasmonate precursors activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4, 129-134   DOI   PUBMED
11 Guo, H., and Ecker, J.R. (2003). Plant responses to ethylene gas are mediated by $SCF^{EBF1/EBF2}$-dependent proteolysis of EIN3 transcription factor. Cell 115, 667-677   DOI   ScienceOn
12 Herve, C., Serres, J., Dabos, P., Canut, H., Barre, A., Rouge, P., and Lescure, B. (1999). Characterization of the Arabidopsis lecRK-a genes: members of a superfamily encoding putative receptors with an extracellular domain homologous to legume lectins. Plant Mol. Biol. 39, 671-682   DOI   ScienceOn
13 Libault, M., Wan, J., Czechowski, T., Udvardi, M., and Stacey, G. (2007). Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol. Pant-Microbe Interact. 20, 900-911   DOI   ScienceOn
14 Moreno, F.B.M.B., De Oliveira, T.M., Martil, D.E., Vicoti, M.M., Bezerra, G.A., Abrego, J.R.B., Cavada, B.S., and De Azevedo Jr., W.F. (2008). Identification of a new quaternary association for legume lectins. J. Struct. Biol. 161, 133-143   DOI   ScienceOn
15 Rudiger, H., and Gabius, H.-J. (2001). Plant lectins: Occurrence, biochemistry, functions and applications. Glycoconjugate J. 18, 589-613   DOI   ScienceOn
16 Ueda, J., Miyamoto, K., and Hashimoto, M. (1996). Jasmonates promote abscission in bean petiole explants: Its relationship to the metabolism of cell wall polysaccharides and cellulose activity. J. Plant Growth Regul. 15, 189-195   DOI   ScienceOn
17 Sharon, N., and Lis, H. (2004). History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14, 53R-62R   DOI   PUBMED   ScienceOn
18 Xie, D.-X., Feys, B.F., James, S., Nieto-Rostro, M., and Turner, J.G. (1998). `lfN: An Arabidopsis gene required for jasmonateregulated defense and fertility. Science 280, 1091-1094   DOI   PUBMED
19 Benavente, L.M., and Alonso, J.M. (2006). Molecular mechanisms of ethylene signaling in Arabidopsis. Mol. BioSyst. 2, 165-173   DOI   PUBMED   ScienceOn
20 Schaller, G.E., and Bleecker, A.B. (1995). Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science 270, 1809-1811   DOI   PUBMED   ScienceOn
21 Jung, C., Lyou, S.H., Yeu, S.Y., Kim, M.A., Rhee, S., Kim, M., Lee, J.S., Choi, Y.D., and Cheong, J.-J. (2007a). Microarray-based screening of jasmonate-responsive genes in Arbidopsis thaliana. Plant Cell Rep. 26, 1053-1063   DOI   ScienceOn
22 Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: $\beta$-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907   PUBMED
23 Komath, S.S., Kavitha, M., and Swamy, M.J. (2006). Beyond carbohydrate binding: new directions in plant lectin research. Org. Biomol. Chem. 4, 973-988   DOI   ScienceOn
24 Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743   DOI   PUBMED   ScienceOn
25 Ito, Y., Kaku, H., and Shibuya, N. (1997). Identification of a highaffinity binding protein for k-acetylchitooligosaccharide elicitor in the plasma membrane of suspension-cultured rice cells by affinity labeling. Plant J. 12, 347-356   DOI   PUBMED   ScienceOn
26 Binder, B.M., Walker, J.M., Gagne, J.M., Emborg, T.J., Hemmann, G., Bleecker, A.B., and Vierstra, R.D. (2007). The Arabidopsis EIN3 binding F-box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell 19, 509-523   DOI   PUBMED   ScienceOn
27 Carpenter, C.D., and Simon, A.E. (1998). Preparation of RNA. Methods Mol. Biol. 82, 85-89   PUBMED
28 Chen, Y., Peumans, W.J., Hause, B., Bras, J., Kumar, M., Proost, P., Barre, A., Rougé, P., and Van Damme, E.J.M. (2002). Jasmonic acid methyl ester induces the synthesis of a cytoplasmic/nuclear chito-oligosaccharide binding lectin in tobacco leaves. FASEB J. 16, 905-907   DOI   PUBMED   ScienceOn
29 Del Campillo, E., and Lewis, L.N. (1992). Identification and kinetics of accumulation of proteins induced by ethylene in bean abscission zones. Plant Physiol. 98, 955-961   DOI   PUBMED   ScienceOn
30 Lim, M.A.G., Kelly, P., Sexton, R., and Trewavas, A.J. (1987). Identification of chitinase mRNA in abscission zones from bean. Plant Cell Environ. 10, 741-746   DOI
31 Xu, L., Liu, F., Lechner, E., Genschik, P., Crosby, W.L., Ma, H., Peng, W., Huang, D., and Xie, D. (2002). The $SCF^{COI1}$ ubiquitinligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14, 1919-1935   DOI   ScienceOn
32 Andresen, I., Becker, W., Schlüter, K., Burges, J., Parthier, B., and Apel, K. (1992). The identification of leaf thionin as one of the main jasmonate-induced proteins of barley (Hordeum vulagre). Plant Mol. Biol. 19, 193-204   DOI   PUBMED
33 Chang, C., Kwok, S.F., Bleecker, A.B., and Meyerowitz, E.M. (1993). Arabidopsis ethylene-response gene bqoN: Similarity of product to two-component regulators. Science 262, 539-544   DOI   PUBMED
34 Penninckx, I.A.M.A., Thomma, B.P.H.J., Buchala, A., Métraux, J.-P., and Broekaert, W.F. (1998). Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10, 2103-2113   DOI   ScienceOn
35 Zhang, B., Ramonell, K., Somerville, S., and Stacey, G. (2002). Characterization of early, chitin-induced gene expression in Arabidopsis. Mol. Plant-Microbe Interact. 15, 963-970   DOI   ScienceOn
36 Hahn, M.G. (1996) Microbial elicitors and their receptors in plants. Annu. Rev. Phytopathol. 34, 387-412   DOI   PUBMED   ScienceOn
37 Jung, C., Yeu, S.Y., Koo, Y.J., Kim, M., Choi, Y.D., and Cheong, J.- J. (2007b). Transcript profile of transgenic Arabidopsis constitutively producing methyl jasmonate. J. Plant Biol. 50, 12-17   DOI   ScienceOn
38 Peumans, W.J., Annick, B., Qiang, H., Pierre, R., and Van Damme, E.J.M. (2000). Higher plants developed structurally different motifsto recognize foreign glycans. Trends Glycosci. Glycotechnol. 12, 83-101   DOI   ScienceOn
39 Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G.A., and Browse, J. (2007). JAZ repressor proteins are targets of the $SCF^{COI1}$ complex during jasmonate signaling. Nature 448, 661-665   DOI   ScienceOn
40 Chrispeels, M.J., and Raikhel, N.V. (1991) Lectins, lectin genes, and their role in plant defense. Plant Cell 3, 1-9   DOI   PUBMED
41 Potuschak, T., Lechner, E., Parmentier, Y., Yanagisawa, S., Grava, S., Koncz, C., and Genschik, P. (2003). EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115, 679-689   DOI   ScienceOn
42 Ebel, J. (1998). Oligoglucoside elicitor-mediated activation of plant defense. Bioessays 20, 569-576   DOI   ScienceOn
43 Mueller, J.M., Brodschelm, W., Spannagl, E., and Zenk, M.H. (1993). Signaling in the elicitation process is mediated through the octadecanoid pathway leading to jasmonic acid. Proc. Natl. Acad. Sci. USA 90, 7490-7494   DOI   ScienceOn
44 Zhang, W., Peumans, W.J., Barre, A., Houles-Astoul, C., Rovira, P., Rouge, P., Proost, P., Truffa-Bachi, P., Jalali, A.A.H., and Van Damme, E.J.M. (2000). Isolation and characterization of a jacalin-related mannose-binding lectin from salt-stressed rice (Oryza sativa) plants. Planta 210, 970-978   DOI   ScienceOn
45 Ramonell, K.M., Zhang, B., Ewing, R.M., Chen, Y., Xu, D., Stacey, G., and Somerville, S. (2002). Microarray Analysis of Chitin Elictation in Arabiolopis thaliana. Mol. Plant Pathol. 3, 301-311   DOI   ScienceOn
46 Van Damme, E.J.M., Lannoo, N., Fouquaert, E., and Peumans, W.J. (2004). The identification of inducible cytoplasmic/nuclear carbohydrate-binding proteins urges to develop novel concepts about the role of plant lectins. Glycoconjugate J. 20, 449-460   PUBMED
47 Wasternack, C., and Hause, B. (2002). Jasmonates and octadecanoids: signals in plant stress responses and development. Progr. Nucl. Acid Res. Mol. Biol. 72, 165-221   DOI
48 Coupe, S.A., Taylor, J.E., and Roberts, J.A. (1997). Temporal and spatial expression of mRNAs encoding pathogenesis-related proteins during ethylene-promoted leaflet abscission in Sambucus nigra. Plant Cell Environ. 20, 1517-1524   DOI   ScienceOn
49 Roberts, J.A., Elliott, K.A., and Gonzalez-Carranza, Z.H. (2002). Abscission, dehiscence, and other cell separation processes. Annu. Rev. Plant Biol. 53, 131-158   DOI   PUBMED
50 Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., Minami, E., and Shibuya, N. (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA 103, 11086-11091   DOI   ScienceOn
51 Feys, B.J.F., Benedetti, C.E., Penfold, C.N., and Turner, J.G. (1994). Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6, 751-759   DOI   PUBMED
52 Herve, C., Dabos, P., Galaud, J.-P., Rouge, P., and Lescure, B. (1996). Characterization of an Arabidopsis thaliana gene that defines a new class of putative plant receptor kinases with an extracellular lectin-like domain. J. Mol. Biol. 258, 778-788   DOI   PUBMED   ScienceOn
53 Rojo, E., Leon, J., and Sanchez-Serrano, J.J. (1999). Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J. 20, 135-142   DOI   ScienceOn
54 Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C., and Manners, J.M. (2000). Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 97, 11655-11660   DOI   ScienceOn
55 Berrocal-Lobo, M., Molina, A., and Solano, R. (2002). Constitutive expression of ETHYLENE-RESPONSIVE-FACTOR1, in Aravidopsis confers resistance to several necrotrophic fungi. Plant J. 29, 23-32   DOI   PUBMED   ScienceOn
56 Bezerra, G.A., Oliveira, T.M., Moreno, F.B.M.B., De Souza, E.P., Da Rocha, B.A.M., Benevides, R.G., Delatorre, P., De Azevedo Jr., W.F., and Cavada, B.S. (2007). Structural analysis of Canavalia maritima and Canavalia gladiata lectins complexed with different dimannosides: New insights into the understanding of the structure-biological activity relationship in legume lectins. J. Struct. Biol. 160, 168-176   DOI   PUBMED   ScienceOn
57 Lannoo, N., Vandenborre, G., Miersch, O., Smagghe, G., Wasternack, C., Peumans, W.J., and Van Damme, E.J.M. (2007). The jasmonate-induced expression of the Nicotiana tabacum leaf lectin. Plant Cell Physiol. 48, 1207-1218   DOI   ScienceOn
58 Penninckx, I.A.M.A., Eggermont, K., Terras, F.R., Thomma, B.P.H.J., De Samblanx, G.W., Buchala, A., MEtraux, J.-P.,Manners, J.M., and Broekaert, W.F. (1996). Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8, 2309-2323   DOI   ScienceOn
59 Saniewski, M., Ueda, J., and Miyamoto, K. (2000). Methyl jasmonate induces the formation of secondary abscission zone in stem of Bryophyllum calycinum Salisb. Acta Physiol. Plant. 22, 17-23   DOI   ScienceOn
60 Saniewski, M., and Wegrzynowicz-Lesiak, E. (1995). Methyl jasmonate- induced leaf abscission in Kalanchoe blossfeldiana. Acta Hortic. 394, 315-324