Transgenic tomato plants overexpressing tyramine N-hydroxycinnamoyltransferase exhibit elevated hydroxycinnamic acid amide levels and enhanced resistance to Pseudomonas syringae

Molecular Plant-Microbe Interactions

Volumn 27, Issue 10, 2014, Pages 1159-1169

  Campos, Laura ^a   Lisón, Purificación ^a   López Gresa, María Pilar ^a   Rodrigo, Ismael ^a   Zacarés, Laura ^a,b   Conejero, Vicente ^a   Bellés, José María ^a  

^a Universitat Politècnica de València   (Spain)

^b ITENE (Packaging Transport and Logistics Research Institute)   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE;

ACYLTRANSFERASE; AMIDE; COUMARIC ACID; DRUG DERIVATIVE; FERULOYLTYRAMINE; HYDROXYCINNAMOYL COA TYRAMINE N (HYDROXYCINNAMOYL)TRANSFERASE; HYDROXYCINNAMOYL-COA-TYRAMINE N-(HYDROXYCINNAMOYL)TRANSFERASE; PATHOGENESIS RELATED PROTEINS, PLANT; PATHOGENESIS-RELATED PROTEINS, PLANT; SALICYLIC ACID; TYRAMINE; VEGETABLE PROTEIN;

ARTICLE; DISEASE RESISTANCE; ENZYMOLOGY; FLOWER; FRUIT; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PSEUDOMONAS SYRINGAE; REPORTER GENE; TOMATO; TRANSGENIC PLANT;

ACYLTRANSFERASES; AMIDES; COUMARIC ACIDS; DISEASE RESISTANCE; FLOWERS; FRUIT; GENE EXPRESSION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; LYCOPERSICON ESCULENTUM; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PSEUDOMONAS SYRINGAE; SALICYLIC ACID; TYRAMINE;

EID: 84907196149     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-04-14-0104-R     Document Type: Article

References (61)

1. Bassard, J. E., Ullmann, P., Bernier, F., and Werck-Reichhart, D. 2010. Phenolamides: Bridging polyamines to the phenolic metabolism. Phytochemistry 71:1808-1824.
2. Bellés, J. M., Garro, R., Fayos, J., Navarro, P., Primo, J., and Conejero, V. 1999. Gentisic acid as a pathogen-inducible signal, additional to salicylic acid for activation of plant defenses in tomato. Mol. Plant-Microbe Interact. 12:227-235.
3. Bellés, J. M., Garro, R., Pallás, V., Fayos, J., Rodrigo, I., and Conejero, V. 2006. Accumulation of gentisic acid as associated with systemic infections but not with the hypersensitive response in plant-pathogen interactions. Planta 223:500-511.
4. Bellés, J. M., López-Gresa, M. P., Fayos, J., Pallás, V., Rodrigo, I., and Conejero, V. 2008. Induction of cinnamate 4-hydroxylase and phenylpropanoids in virus-infected cucumber and melon plants. Plant Sci. 174:524-533.
5. Bottcher, C., von Roepenack-Lahaye, E., Schmidt, J., Schmotz, C., Neumann, S., Scheel, D., and Clemens, S. 2008. Metabolome analysis of biosynthetic mutants reveals a diversity of metabolic changes and allows identification of a large number of new compounds in Arabidopsis. Plant Physiol. 147:2107-2120.
6. Campos, L., Granell, P., Tárraga, S., López-Gresa, M. P., Conejero, V., Bellés, J. M., Rodrigo, I., and Lisón, P. 2014. Salicylic acid and gentisic acid induce RNA silencing-related genes and plant resistance to RNA pathogens. Plant Physiol. Biochem. 77:35-43.
7. Clarke, D. D. 1982. Active defence mechanisms in plants. Pages 321-322 in: The Accumulation of Cinnamic Acid Amides in the Cell Walls of Potato Tissue as an Early Response to Fungal Attack. R. K. S, Wood, ed. Plenum Press, New York.
8. Coego, A., Ramirez, V., Ellul, P., Mayda, E., and Vera, P. 2005. The H2O2-regulated Ep5C gene encodes a peroxidase required for bacterial speck susceptibility in tomato. Plant J. 42:283-293.
9. Collinge, D. B., Milligan, D. E., Dow, J. M., Scofield, G., and Daniels, M. J. 1987. Gene expression in Brassica campestris showing a hypersensitive response to the incompatible pathogen Xanthomonas campestris pv vitians. Plant Mol. Biol. 8:405-414.
10. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gutrella, M., Kessmann, H., Ward, E., and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266:1247-1250.
11. Dempsey, D. A., Shah, J., and Klessig, D. F. 1999. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18:547-575.
12. Ellul, P., Garcia-Sogo, B., Pineda, B., Rios, G., Roig, L., and Moreno, V. 2003. The ploidy level of transgenic plants in Agrobacterium-mediated transformation of tomato cotyledons (Lycopersicon esculentum Mill.) is genotype and procedure dependent Theor. Appl. Genet. 106:231-238.
13. Facchini, P. J., Hagel, J., and Zulak, K. G. 2002. Hydroxycinnamic acid amide metabolism: Physiology and biochemistry. Can. J. Bot. 80:577-589.
14. Fattorusso, E., Lanzotti, V., and Taglialatela-Scafati, O. 1999. Antifungal N-feruloyl amides from roots of two Allium species. Plant Biosyst. 133:199-203.
15. Feldman, J. M., and Lee, E. M. 1985. Serotonin content of foods: Effect on urinary excretion of 5-hydroxyindoleacetic acid. Am. J. Clin. Nutr. 42:639-643.
16. Grandmaison, J., Olah, G. M., Vancalsteren, M. R., and Furlan, V. 1993. Characterization and localization of plant phenolics likely involved in the pathogen resistance expressed by endomycorrhizal roots. Mycorrhiza 3:155-164.
17. Hagel, J. M., and Facchini, P. J. 2005. Elevated tyrosine decarboxylase and tyramine hydroxycinnamoyltransferase levels increase wound-induced tyramine-derived hydroxycinnamic acid amide accumulation in transgenic tobacco leaves. Planta 221:904-914.
18. Hahlbrock, K., and Scheel, D. 1989. Physiology and molecular biology of phenylpropanoid metabolism. Ann. Rev. Plant Physiol. Plant Mol. Biol. 40:347-369.
19. Handrick, V., Vogt, T., and Frolov, A. 2010. Profiling of hydroxycinnamic acid amides in Arabidopsis thaliana pollen by tandem mass spectrometry. Anal. Bioanal. Chem. 398:2789-2801.
20. Hohlfeld, H., Scheel, D., and Strack, D. 1996. Purification of hydroxycinnamoyl-CoA:tyramine hydroxycinnamoyltransferase from cell-suspension cultures of Solanum tuberosum L. cv. Datura. Planta 199:166-168.
21. Kang, K., Lee, K., Sohn, S. O., Park, S., Lee, S., Kim, S. Y., Kim, Y. S., and Back, K. 2009. Ectopic expression of serotonin N-hydroxycinnamoyltransferase and differential production of phenylpropanoid amides in transgenic tomato tissues. Sci. Hortic. 120:504-510.
22. Kang, K., Lee, K., Ishihara, A., Park, S., Kim, Y. S., and Back, K. 2010. Induced synthesis of caffeoylserotonin in pepper fruits upon infection by the anthracnose fungus, Colletotrichum gloeosporioides. Sci. Hortic. 124:290-293.
23. Kang, S., and Back, K. 2006. Enriched production of N-hydroxycinnamic acid amides and biogenic amines in pepper (Capsicum annuum) flowers. Sci. Hortic. 108:337-341.
24. Kawashima, S., Hayashi, M., Takii, T., Kimura, H., Zhang, H. L., Nagatsu, A., Sakakibara, J., Murata, K., Oomoto, Y., and Onozaki, K. 1998. Serotonin derivative, N-(p-coumaroyl) serotonin, inhibits the production of TNF-α, IL-1α, IL-1β, and IL-6 by endotoxin-stimulated human blood monocytes. J. Interferon Cytokine Res. 18:423-428.
25. Keller, H., Hohlfeld, H., Wray, V., Hahlbrock, K., Scheel, D., and Strack, D. 1996. Changes in the accumulation of soluble and cell wall-bound phenolics in elicitor-treated cell suspension cultures and fungusinfected leaves of Solanum tuberosum. Phytochemistry 42:389-396.
26. Lee, D. E., Kang, K., Lee, S. G., and Back, K. 2007. Enhanced synthesis of feruloyltyramine and 4-coumaroyltyramine is associated with tyramine availability in transgenic rice expressing pepper tyramine N-hydroxycinnamoyltransferase. Plant Sci. 172:57-63.
27. Lee, D. G., Park, Y., Kim, M. R., Jung, H. J., Seu, Y. B., Hahm, K. S., and Woo, E. R. 2004. Antifungal effects of phenolic amides isolated from the root bark of Lycium chinense. Biotechnol. Lett. 26:1125-1130.
28. Lisón, P., Rodrigo, I., and Conejero, V. 2006. A novel function for the cathepsin D inhibitor in tomato. Plant Physiol. 142:1329-1339.
29. Liyama, K., Lam, T. B. T., and Stone, B. A. 1994. Covalent cross links in the cell wall. Plant Physiol. 104:315-320.
30. López-Gresa, M. P., Torres, C., Campos, L., Lisón, P., Rodrigo, I., Bellés, J. M., and Conejero, V. 2011. Identification of defence metabolites in tomato plants infected by the bacterial pathogen Pseudomonas syringae. Environ. Exp. Bot. 74:216-228.
31. Luo, J., Fuell, C., Parr, A., Hill, L., Bailey, P., Elliott, K., Fairhurst, S. A., Martin, C., and Michael, A. J. 2009. A novel polyamine acyltransferase responsible for the accumulation of spermidine conjugates in Arabidopsis seed. Plant Cell 21:318-333.
32. Ly, D., Kang, K., Choi, J. Y., Ishihara, A., Back, K., and Lee, S. G. 2008. HPLC analysis of serotonin, tryptamine, tyramine, and the hydroxycinnamic acid amides of serotonin and tyramine in food vegetables. J. Med. Food 11:385-389.
33. Mallona, I., Weiss, J., and Marcos, E. C. 2011. pcrEfficiency: A Web tool for PCR amplification efficiency prediction. BMC Bioinformatics 12:404.
34. Martin-Tanguy, J., Cabanne, F., Perdrizet, E., and Martin, C. 1978. Distribution of hydroxycinnamic acid-amides in flowering plants. Phytochemistry 17:1927-1928.
35. Martin-Tanguy, J., Negrel, J., Paynot, M., and Martin, C. 1987. Hydroxycinnamic acid amides, hypersensitivity, flowering and sexual organogenesis in plants., New York.
36. Métraux, J. P., and Raskin, I. 1993. Role of phenolics in plant disease resistance. Pages 191-209 in: Biotechnology in Plant Disease Control. Wiley-Liss, New York.
37. Muhlenbeck, U., Kortenbusch, A., and Barz, W. 1996. Formation of hydroxycinnamoylamides and α-hydroxyacetovanillone in cell cultures of Solanum khasianum. Phytochemistry 42:1573-1579.
38. Muroi, A., Ishihara, A., Tanaka, C., Ishizuka, A., Takabayashi, J., Miyoshi, H., and Nishioka, T. 2009. Accumulation of hydroxycinnamic acid amides induced by pathogen infection and identification of agmatine coumaroyltransferase in Arabidopsis thaliana. Planta 230:517-527.
39. Muroi, A., Matsui, K., Shimoda, T., Kihara, H., Ozawa, R., Ishihara, A., Nishihara, M., and Arimura, G. 2012. Acquired immunity of transgenic torenia plants overexpressing agmatine coumaroyltransferase to pathogens and herbivore pests. Sci. Rep. 2:689.
40. Nagatsu, A., Zhang, H. L., Mizukami, H., Okuyama, H., Sakakibara, J., Tokuda, H., and Nishino, H. 2000. Tyrosinase inhibitory and anti-tumor promoting activities of compounds isolated from safflower (Carthamus tinctorius L.) and cotton (Gossypium hirsutum L.) oil cakes. Nat. Prod. Lett. 14:153-158.
41. Naranjo, M. A., Romero, C., Bellés, J. M., Montesinos, C., Vicente, O., Serrano, R. 2003. Lithium treatment induces a hypersensitive-like response in tobacco. Panta. 217:417-424.
42. Negrel, J., and Javelle, F. 1997. Purification, characterization and partial amino acid sequencing of hydroxycinnamoyl-CoA: Tyramine N-(hydroxycinnamoyl) transferase from tobacco cell-suspension cultures. Eur. J. Biochem. 247:1127-1135.
43. Negrel, J., and Jeandet, P. 1987. Metabolism of tyramine and feruloyltyramine in TMV inoculated leaves of Nicotiana tabacum. Phytochemistry 26:2185-2190.
44. Negrel, J., and Lherminier, J. 1987. Peroxidase mediated integration of tyramine into xylem cell-walls of tobacco-leaves. Planta 172:494-501.
45. Negrel, J., and Martin, C. 1984. The biosynthesis of feruloyltyramine in Nicotiana tabacum. Phytochemistry 23:2797-2801.
46. Negrel, J., Javelle, F., and Paynot, M. 1993. Wound induced tyramine hydroxycinnamoyl transferase in potato (Solanum tuberosum) tuber disks. J. Plant Physiol. 142:518-524.
47. Newman, M. A., von Roepenack-Lahaye, E., Parr, A., Daniels, M. J., and Dow, J. M. 2001. Induction of hydroxycinnamoyl-tyramine conjugates in pepper by Xanthomonas campestris, a plant defense response activated by hrp gene-dependent and hrp gene-independent mechanisms. Mol. Plant-Microbe Interact. 14:785-792.
48. Park, J. B., and Schoene, N. 2002. Synthesis and characterization of Ncoumaroyltyramine as a potent phytochemical which arrests human transformed cells via inhibiting protein tyrosine kinases. Biochem. Biophys. Res. Commun. 292:1104-1110.
49. Pearce, G., Marchand, P. A., Griswold, J., Lewis, N. G., and Ryan, C. A. 1998. Accumulation of feruloyltyramine and p-coumaroyltyramine in tomato leaves in response to wounding. Phytochemistry 47:659-664.
50. Roh, J. S., Han, J. Y., Kim, J. H., and Hwang, J. K. 2004. Inhibitory effects of active compounds isolated from safflower (Carthamus tinctorius L.) seeds for melanogenesis. Biol. Pharm. Bull. 27:1976-1978.
51. Schmidt, A., Scheel, D., and Strack, D. 1998. Elicitor-stimulated biosynthesis of hydroxycinnamoyltyramines in cell suspension cultures of Solanum tuberosum. Planta 205:51-55.
52. Schmidt, A., Grimm, R., Schmidt, J., Scheel, D., Strack, D., Rosahl, S. 1999. Cloning and expression of a potato cDNA encoding hydroxycinnamoyl-CoA:tyramine N-(hydroxycinnamoyl) transferase. J. Biol. Chem. 274:4273-80.
53. Strack, D. 1997. Phenolic metabolism. Pages 387-416 in: Plant Biochemistry, P. M. Dey and J. B. Harborne, eds. Academic Press, London.
54. Tebayashi, S. I., Horibata, Y., Mikagi, E., Kashiwagi, T., Mekuria, D. B., Dekebo, A., Ishihara, A., and Kim, C. S. 2007. Induction of resistance against the leaffminer, Liriomyza trifolii, by jasmonic acid in sweet pepper. Biosci. Biotechnol. Biochem. 71:1521-1526.
55. Tornero, P., Gadea, J., Conejero, V., and Vera, P. 1997. Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis-related gene during the hypersensitive response and development. Mol Plant Microbe Interact. 10:624-634.
56. van Loon, L. C., Rep, M., and Pieterse, C. M. J. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135-162.
57. Villegas, M., and Brodelius, P. E. 1990. Elicitor induced hydroxycinnamoyl-CoA: Tyramine hydroxycinnamoyltransferase in plant-cell suspension cultures. Physiol Plant. 78:414-420.
58. von Roepenack-Lahaye, E., Newman, M. A., Schornack, S., Hammond-Kosack, K. E., Lahaye, T., Jones, J. D. G., Daniels, M. J., and Dow, J. M. 2003. p-coumaroylnoradrenaline, a novel plant metabolite implicated in tomato defense against pathogens. J. Biol. Chem. 278:43373-43383.
59. Yu, M., and Facchini, P. J. 1999. Purification, characterization, and immunolocalization of hydroxycinnamoyl-CoA:tyramine N-(hydroxycinnamoyl) transferase from opium poppy. Planta 209:33-44.
60. Zacarés, L., López-Gresa, M. P., Fayos, J., Primo, J., Bellés, J. M., and Conejero, V. 2007. Induction of p-coumaroyldopamine and feruloyldopamine, two novel metabolites, in tomato by the bacterial pathogen Pseudomonas syringae. Mol. Plant-Microbe Interact. 20:1439-1448.
61. Zhang, H. L., Nagatsu, A., Watanabe, T., Sakakibara, J., and Okuyama, H. 1997. Antioxidative compounds isolated from safflower (Carthamus tinctorius L.) oil cake. Chem. Pharm. Bull. 45:1910-1914.