The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression

Plant Cell

Volumn 15, Issue 7, 2003, Pages 1646-1661

  Li, Chuanyou ^a   Liu, Guanghui ^a   Xu, Changcheng ^a   Lee, Gyu In ^a   Bauer, Petra ^b   Ling, Hong Qing ^c   Ganal, Martin W ^b,d   Howe, Gregg A ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^d TRAITGENETICS GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; FATTY ACIDS; LIPIDS; PLANTS (BOTANY); PROTEINS;

HORNWORMS;

GENES;

EMBRYOPHYTA; LYCOPERSICON ESCULENTUM; MANDUCA SEXTA; NICOTIANA TABACUM; PROKARYOTA; SPHINGIDAE;

EID: 0038380974     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.012237     Document Type: Article

References (103)

1. Allen, K.D. (2002). Assaying gene content in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 9568-9572.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
3. Bate, N.J., and Rothstein, S.J. (1998). C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J. 16, 561-569.
4. Baydoun, E.A.H., and Fry, S.C. (1988). The immobility of pectic substances in injured tomato leaves and its bearing on the identity of the wound hormone. Planta 165, 269-276.
5. Bishop, P.D., Makus, D.J., Pearce, G., and Ryan, C.A. (1981). Proteinase inhibitor-inducing factor activity in tomato leaves resides in oligosaccharides enzymically released from cell walls. Proc. Natl. Acad. Sci. USA 78, 3536-3540.
6. Blechert, S., Bockelmann, C., Füsslein, M., Schrader, T.V., Stelmach, S.B., Niesel, U., and Weiler, E.W. (1999). Structure-activity analyses reveal the existence of two separate groups of active octadecanoids in elicitation of the tendril-coiling response of Bryonia dioica Jacq. Planta 207, 470-479.
7. Blechert, S., Brodschelm, W., Holder, S., Kammerer, L., Kutchan, T.M., Mueller, M.J., Xia, Z.-Q., and Zenk, M.H. (1995). The octadecanoic pathway: Signal molecules for the regulation of secondary pathways. Proc. Natl. Acad. Sci. USA 92, 4099-4105.
8. Browse, J., McCourt, P., and Somerville, C.R. (1986). A mutant of Arabidopsis deficient in C18:3 and C16:3 leaf lipids. Plant Physiol. 81, 859-864.
9. Browse, J., and Somerville, C. (1991). Glycerolipid synthesis: Biochemistry and regulation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 467-506.
10. Budiman, M.A., Mao, L., Wood, T.C., and Wing, R.A. (2000). A deep-coverage tomato BAC library and prospects towards development of an STC framework for genome sequencing. Genome Res. 10, 129-136.
11. Conconi, C., Miquel, M., Browse, J.A., and Ryan, C.A. (1996). Intracellular levels of free linolenic and linoleic acids increase in tomato leaves in response to wounding. Plant Physiol. 111, 797-803.
12. Constabel, C.P., Yip, L., and Ryan, C.A. (1998). Prosystemin from potato, black nightshade, and bell pepper: Primary structure and biological activity of predicted systemin polypeptides. Plant Mol. Biol. 36, 55-62.
13. Doares, S.H., Syrovets, T., Weiler, E.W., and Ryan, C.A. (1995). Oligogalacturonides and chitosan activate plant defense genes through the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 92, 4095-4098.
14. Dörmann, P., Hoffmann-Benning, S., Balbo, I., and Benning, C. (1995). Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell 7, 1801-1810.
15. Eshed, Y., and Zamir, D. (1994). A genomic library of Lycopersicon pennellii in L. esculentum: A tool for fine mapping of genes. Euphytica 79, 175-179.
16. 6-green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61, 545-554.
17. Farmer, E.E., and Ryan, C.A. (1992). Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4, 129-134.
18. Felix, G., and Boller, T. (1995). Systemin induces rapid ion fluxes and ethylene biosynthesis in Lycopersicon peruvianum cells. Plant J. 7, 381-389.
19. Gatehouse, J.A. (2002). Plant resistance towards insect herbivores: A dynamic interaction. New Phytol. 156, 145-169.
20. Gibson, S., Arondel, V., Iba, K., and Somerville, C. (1994). Cloning of a temperature-regulated gene encoding a chloroplast ω-3 desaturase from Arabidopsis thaliana. Plant Physiol. 106, 1615-1621.
21. Graham, J.S., Pearce, G., Merryweather, J., Titani, K., Ericsson, L.H., and Ryan, C.A. (1985). Wound-induced proteinase inhibitors from tomato leaves. II. The cDNA-deduced primary structure of pre-inhibitor II. J. Biol. Chem. 260, 6561-6564.
22. Green, T.R., and Ryan, C.A. (1972). Wound inducible proteinase inhibitors in plant leaves: A possible defense mechanism against insects. Science 175, 776-777.
23. Hamada, T., Nishiuchi, T., Kodama, H., Nishímura, M., and Iba, K. (1996). cDNA cloning of a wounding-inducible gene encoding a plastid ω3 fatty acid desaturase from tobacco. Plant Cell Physiol. 37, 606-611.
24. Hause, B., Stenzel, I., Miersch, O., Maucher, H., Kramell, R., Ziegler, J., and Wasternack, C. (2000). Tissue-specific oxylipin signature of tomato flowers: Allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles. Plant J. 24, 113-126.
25. Hilleren, P., and Parker, R. (1999). Mechanisms of mRNA surveillance in eukaryotes. Annu. Rev. Genet. 33, 229-260.
26. Howe, G.A., Lee, G.I., Itoh, A., Li, L., and DeRocher, A. (2000). Cytochrome P450-dependent metabolism of oxylipins in tomato: Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase. Plant Physiol. 123, 711-724.
27. Howe, G.A., Lightner, J., Browse, J., and Ryan, C.A. (1996). An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8, 2067-2077.
28. Howe, G.A., and Ryan, C.A. (1999). Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153, 1411-1421.
29. Hugly, S., and Somerville, C.R. (1992). A role for membrane lipid polyunsaturation in chloroplast biogenesis at low temperature. Plant Physiol. 99, 197-202.
30. Iba, K., Gibson, S., Nishiuchi, T., Fuse, T., Nishimura, M., Arondel, V., Hugly, S., and Somerville, C. (1993). A gene encoding a chloroplast ω-3 fatty acid desaturase complements alterations in fatty acid desaturation and chloroplast copy number of the fad7 mutant of Arabidopsis thaliana. J. Biol. Chem. 268, 24099-24105.
31. Ishiguro, S., Kawai-Oda, A., Ueda, K., Nishida, I., and Okada, K. (2001). The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13, 2191-2209.
32. Jaglo, K.R., Kleff, S., Amundsen, K.L., Zhang, X., Haake, V., Zhang, J.Z., Deits, T., and Thomashow, M.F. (2001). Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol. 127, 910-917.
33. Jamieson, G.R., and Reid, E.H. (1971). The occurrence of hexadeca7,10,13-trienoic acid in the leaf lipids of angiosperms. Phytochemistry 10, 1837-1843.
34. Karban, R., and Baldwin, I.T. (1997). Induced Response to Herbivory. (Chicago, IL: University of Chicago Press).
35. Keegstra, K., Olesen, L.J., and Theg, S.M. (1989). Chloroplastic precursors and their transport across the envelope membranes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 471-501.
36. Kessler, A., and Baldwin, I.T. (2002). Plant responses to insect herbivory: The emerging molecular analysis. Annu. Rev. Plant Biol. 53, 299-328.
37. Kubigsteltig, I., Laudert, D., and Weiler, E.W. (1999). Structure and regulation of the Arabidopsis thaliana allene oxide synthase gene. Planta 208, 463-471.
38. Kwon, J.H., Lee, Y.M., and An, C.S. (2000). cDNA cloning of chloroplast omega-3 fatty acid desaturase from Capsicum annuum and its expression upon wounding. Mol. Cells 10, 493-497.
39. Lazo, G.R., Stein, P.A., and Ludwig, R.A. (1991). A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Biotechnology 9, 963-967.
40. LeBrasseur, N.D., MacIntosh, G.C., Perez-Amador, M.A., Saitoh, M., and Green, P.J. (2002). Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathway. Plant J. 29, 393-403.
41. Lee, G.I., and Howe, G.A. (2003). The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. Plant J. 33, 567-576.
42. Leon, J., Rojo, E., and Sánchez-Serrano, J.J. (2001). Wound signaling in plants. J. Exp. Bot. 52, 1-9.
43. Li, C., Williams, M.M., Loh, Y.-T., Lee, I.G., and Howe, G.A. (2002a). Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiol. 130, 494-503.
44. Li, L., and Howe, G.A. (2001). Alternative splicing of prosystemin pre-mRNA produces two isoforms that are active as signals in the wound response pathway. Plant Mol. Biol. 46, 409-419.
45. Li, L., Li, C., and Howe, G.A. (2001). Genetic analysis of wound signaling in tomato: Evidence for a dual role of jasmonic acid in defense and female fertility. Plant Physiol. 127, 1414-1417.
46. Li, L., Li, C., Lee, G.I., and Howe, G.A. (2002b). Distinct roles for jasmonic acid synthesis and action in the systemic wound response of tomato. Proc. Natl. Acad. Sci. USA 99, 6416-6421.
47. Liechti, R., and Farmer, E.E. (2002). The jasmonate pathway. Science 296, 1649-1650.
48. Ling, H.-Q., Bauer, P., Bereczky, Z., Keller, B., and Ganal, M. (2002). The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc. Natl. Acad. Sci. USA 99, 13938-13943.
49. Ling, H.Q., Pich, A., Scholz, G., and Ganal, M.W. (1996). Genetic analysis of two tomato mutants affected in the regulation of iron metabolism. Mol. Gen. Genet. 252, 87-92.
50. Liu, Y.G., and Whittier, R.F. (1995). Thermal asymmetric interlaced PCR-automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25, 674-681.
51. Malone, M. (1996). Rapid, long-distance signal transmission in higher plants. Adv. Bot. Res. 22, 163-228.
52. Martín, M., León, J., Dammann, C., Albar, J.-P., Griffiths, G., and Serrano, J.J.S. (1999). Antisense-mediated depletion of potato leaf ω3 fatty acid desaturase lowers linolenic acid content and reduces gene activation in response to wounding. Eur. J. Biochem. 262, 283-290.
53. McConn, M., and Browse, J. (1996). The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8, 403-416.
54. McConn, M., Hugly, S., Browse, J., and Somerville, C. (1994). A mutation at the fad8 locus of Arabidopsis identifies a second chloroplast ω3 desaturase. Plant Physiol. 106, 1609-1614.
55. McCouch, S.R., Kochert, G., Yu, Z.H., Wang, Z.Y., Khush, G.S., Coffman, W.R., and Tanksley, S.D. (1988). Molecular mapping of rice chromosomes. Theor. Appl. Genet. 76, 815-829.
56. McGurl, B., Orozco-Cardenas, M., Pearce, G., and Ryan, C.A. (1994). Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc. Natl. Acad. Sci. USA 91, 9799-9802.
57. McGurl, B., Pearce, G., Orozco-Cardenas, M., and Ryan, C.A. (1992). Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255, 1570-1573.
58. Meindl, T., Boller, T., and Felix, G. (1998). The plant wound hormone systemin binds with the N-terminal part to its receptor but needs the C-terminal part to activate it. Plant Cell 10, 1561-1570.
59. Miquel, M., James, D.J., Dooner, H., and Browse, J. (1993). Arabidopsis requires polyunsaturated lipids for low-temperature survival. Proc. Natl. Acad. Sci. USA 90, 6208-6212.
60. 2+ mobilization from intra- and extracellular compartments. Plant Cell Environ. 21, 1101-1111.
61. Moyen, C., and Johannes, E. (1996). Systemin transiently depolarizes the tomato mesophyll cell membrane and antagonizes fusicoccin-induced extracellular acidification of mesophyll tissue. Plant Cell Environ. 19, 464-470.
62. Narváez-Vásquez, J., Florin-Christensen, J., and Ryan, C.A. (1999). Positional specificity of a phospholipase A activity induced by wounding, systemin, and oligosaccharide elicitors in tomato leaves. Plant Cell 11, 2249-2280.
63. Nishiuchi, T., Hamada, T., Kodoma, H., and Iba, K. (1997). Wounding changes the spatial expression pattern of the Arabidopsis plastid omega-3 fatty acid desaturase gene (FAD7) through different signal transduction pathways. Plant Cell 9, 1701-1712.
64. Novitskaya, G.V., Suvorova, T.A., and Trunova, T.I. (2000). Lipid composition of tomato leaves as related to plant cold tolerance. Russian J. Plant Physiol. 47, 728-733.
65. O'Donnell, P.J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H.M.O., and Bowles, D.J. (1996). Ethylene as a signal mediating the wound response of tomato plants. Science 274, 1914-1917.
66. O'Donnell, P.J., Truesdale, M.R., Calvert, C.M., Dorans, A., Roberts, M.R., and Bowles, D.J. (1998). A novel tomato gene that rapidly responds to wound- and pathogen-related signals. Plant J. 14, 137-142.
67. Orozco-Cárdenas, M., McGurl, B., and Ryan, C.A. (1993). Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larva. Proc. Natl. Acad. Sci. USA 90, 8273-8276.
68. Orozco-Cárdenas, M.L., Narváez-Vásquez, J., and Ryan, C.A. (2001). Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13, 179-191.
69. Ouariti, O., Boussama, N., Zarrouk, M., Cherif, A., and Ghorbal, M.H. (1997). Cadmium- and copper-induced changes in tomato membrane lipids. Phytochemistry 45, 1343-1350.
70. Pearce, G., Moura, D.S., Stratmann, J., and Ryan, C.A. (2001). Production of multiple plant hormones from a single polyprotein precursor. Nature 411, 817-820.
71. Pearce, G., Strydom, D., Johnson, S., and Ryan, C.A. (1991). A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253, 895-898.
72. Rojo, E., León, J., and Sánchez-Serrano, J.J. (1999). Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J. 20, 135-142.
73. 14C]acetate by cell-free preparations from spinach (Spinacia oleracea) chloroplasts. Biochem. J. 188, 17-24.
74. Routaboul, J.M., Fischer, S.F., and Browse, J. (2000). Trienoic fatty acids are required to maintain chloroplast function at low temperatures. Plant Physiol. 124, 1697-1705.
75. Ryan, C.A. (1967). Quantitative determination of soluble cellular proteins by radial diffusion in agar gels containing antibodies. Anat. Biochem. 19, 434-440.
76. Ryan, C.A. (2000). The systemin signaling pathway: Differential activation of plant defensive genes. Biochim. Biophys. Acta 1477, 112-121.
77. Ryan, C.A., and Moura, D.S. (2002). Systemic wound signaling in plants: A new perception. Proc. Natl. Acad. Sci. USA 99, 6519-6520.
78. Ryan, C.A., Pearce, G., Scheer, J., and Moura, D.S. (2002). Polypeptide hormones. Plant Cell 14 (suppl.), S251-S264.
79. Schaller, A., Bergey, D.R., and Ryan, C.A. (1995). Induction of wound response genes in tomato leaves by bestatin, an inhibitor of aminopeptidases. Plant Cell 7, 1893-1898.
80. +-ATPase activity differentially activates wound and pathogen defense responses in tomato ptants. Plant Cell 11, 263-272.
81. Scheer, J.M., and Ryan, C.A. (1999). A 160-kD systemin receptor on the surface of Lycopersicon peruvianum suspension-cultured cells. Plant Cell 11, 1525-1536.
82. Scheer, J.M., and Ryan, C.A. (2002). The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc. Natl. Acad. Sci. USA 99, 9585-9590.
83. Somerville, C.R., and Browse, J. (1991). Plant lipids: Metabolism, mutants and membranes. Science 252, 82-87.
84. Stintzi, A., Weber, H., Reymond, P., Browse, J., and Farmer, E.E. (2001). Plant defense in the absence of jasmonic acid: The role of cyclopentenones. Proc. Natl. Acad. Sci. USA 98, 12837-12842.
85. Strassner, J., Schaller, F., Frick, U.B., Howe, G.A., Weiler, E.W., Amrhein, N., Macheroux, P., and Schaller, A. (2002). Characterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductases reveals differential roles for octadecanoid biosynthesis in the local versus the systemic wound response. Plant J. 32, 585-601.
86. Stratmann, J.W., and Ryan, C.A. (1997). Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. Proc. Natl. Acad. Sci. USA 94, 11085-11089.
87. Tanksley, S.D., et al. (1992). High density molecular linkage maps of the tomato and potato genomes. Genetics 132, 1141-1160.
88. Thomas, C.M., Vos, P., Zabeau, M., Jones, D.A., Norcott, K.A., Chadwick, B.P., and Jones, J.D.G. (1995). Identification of amplified restriction fragment polymorphism (AFLP) markers tightly linked to the tomato Cf-9 gene for resistance to Cladosporium fulvum. Plant J. 8, 785-794.
89. Titarenko, E., Rojo, E., León, J., and Sánchez-Serrano, J.J. (1997). Jasmonic acid-dependent and -independent signaling pathways control wound-induced gene activation in Arabidopsis thaliana. Plant Physiol. 11, 817-826.
90. Trautman, R., Cowan, K.M., and Wagner, C.G. (1971). Data processing for radial immunodiffusion. Immunochemistry 8, 901-916.
91. Turner, J.G., Ellis, C., and Devoto, A. (2002). The jasmonate signal pathway. Plant Cell 14 (suppl.), S153-S164.
92. Vancanneyt, G., Sanz, C., Farmaki, T., Paneque, M., and Ortego, F. (2001). Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc. Natl. Acad. Sci. USA 98, 8139-8144.
93. Van der Hoeven, R., Ronning, C., Giovannoni, J., Martin, G., and Tanksley, S. (2002). Deductions about the number, organization, and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencing. Plant Cell 14, 1441-1456.
94. Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M., and Zabeau, M. (1995). AFLP: A new technique for DNA finger printing. Nucleic Acids Res. 23, 4407-4414.
95. Walling, L.L. (2000). The myriad plant responses to herbivores. J. Plant Growth Regul. 19, 195-216.
96. Wallis, J.G., and Browse, J. (2002). Mutants of Arabidopsis reveal many roles for membrane lipids. Prog. Lipid Res. 41, 254-278.
97. Wasternack, C., and Hause, B. (2002). Jasmonates and octadecanoids: Signals in plant stress responses and development. Prog. Nucleic Acid Res. Mol. Biol. 72, 165-221.
98. Wasternack, C., Ortel, B., Miersch, O., Kramell, R., Beale, M., Greulich, F., Feussner, I., Hause, B., Krumm, T., Boland, W., and Parthier, B. (1998). Diversity in octadecanoid-induced gene expression in tomato. J. Plant Physiol. 152, 345-352.
99. Weber, H. (2002). Fatty acid-derived signals in plants. Trends Plant Sci. 7, 217-224.
100. Weber, H., Vick, B.A., and Farmer, E.E. (1997). Dinor-oxo-phytodienoic acid: A new hexadecanoid signal in the jasmonate family. Proc. Natl. Acad. Sci. USA 94, 10473-10478.
101. Whitaker, B.D. (1986). Fatty-acid composition of polar lipids in fruit and leaf chloroplasts of "16:3" and "18:3" plant species. Planta 169, 313-319.
102. Xu, C., Härtel, H., Wada, H., Hagio, M., Yu, B., Eakin, C., and Benning, C. (2002). The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol. 129, 594-604.
103. Yang, Y.W., Lai, K.N., Tai, P.Y., and Li, W.H. (1999). Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J. Mol. Evol. 48, 597-604.