A 13-lipoxygenase, TomloxC, is essential for synthesis of C5 flavour volatiles in tomato

Journal of Experimental Botany

Volumn 65, Issue 2, 2014, Pages 419-428

  Shen, Jiyuan ^a,b   Tieman, Denise ^a   Jones, Jeffrey B ^a   Taylor, Mark G ^a   Schmelz, Eric ^c   Huffaker, Alisa ^c   Bies, Dawn ^a   Chen, Kunsong ^b   Klee, Harry J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c CENTER FOR MEDICAL   (United States)

Author keywords

13 lipoxygenase; C5 volatiles; hydroperoxide lyase; jasmonic acid; tomato; wounding; Xanthomonas campestris pv. vesicatoria

Indexed keywords

13 LIPOXYGENASE; 13-LIPOXYGENASE; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; LINOLEIC ACID; LINOLENIC ACID; LIPOXYGENASE; OXYLIPIN; VEGETABLE PROTEIN; VOLATILE ORGANIC COMPOUND;

ARTICLE; BIOSYNTHESIS; C5 VOLATILES; CHEMISTRY; DOWN REGULATION; ENZYMOLOGY; FRUIT; GENE EXPRESSION REGULATION; GENETICS; HYDROPEROXIDE LYASE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; TASTE; TOMATO; TRANSGENIC PLANT; WOUND; XANTHOMONAS; XANTHOMONAS CAMPESTRIS PV. VESICATORIA.;

13-LIPOXYGENASE; C5 VOLATILES; HYDROPEROXIDE LYASE; JASMONIC ACID; TOMATO; WOUNDING; XANTHOMONAS CAMPESTRIS PV. VESICATORIA.;

ALPHA-LINOLENIC ACID; BIOSYNTHETIC PATHWAYS; CYCLOPENTANES; DOWN-REGULATION; FRUIT; GENE EXPRESSION REGULATION, PLANT; LINOLEIC ACID; LIPOXYGENASE; LYCOPERSICON ESCULENTUM; OXYLIPINS; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; TASTE; VOLATILE ORGANIC COMPOUNDS; XANTHOMONAS;

EID: 84893262077     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert382     Document Type: Article

References (45)

1. Allmann S, Halitschke R, Schuurink RC, Baldwin IT. 2010. Oxylipin channelling in Nicotiana attenuata: lipoxygenase 2 supplies substrates for green leaf volatile production. Plant, Cell and Environment 33, 2028-2040.
2. Andreou A, Feussner I. 2009. Lipoxygenases -structure and reaction mechanism. Phytochemistry 70, 1504-1510.
3. Astua-Monge G, Minsavage GV, Stall RE, Davis MJ, Bonas U, Jones JB. 2000. Resistance of tomato and pepper to T3 strains of Xanthomonas campestris pv. vesicatoria is specified by a plantinducible. Molecular Plant-Microbe Interactions 13, 911-921.
4. Bate NJ, Rothstein SJ. 1998. C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. The Plant Journal 16, 561-569.
5. Chauvin A, Caldelari D, Wolfender JL, Farmer EE. 2013. Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. New Phytologist 197, 566-575.
6. Chen GP, Hackett R, Walker D, Taylor A, Lin ZF, Grierson D. 2004. Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant Physiology 136, 2641-2651.
7. Christensen SA, Kolomiets MV. 2011. The lipid language of plantfungal interactions. Fungal Genetics and Biology 48, 4-14.
8. Christensen SA, Nemchenko A, Borrego E, et al. 2013. The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. The Plant Journal 74, 59-73.
9. Croft KPC, Juttner F, Slusarenko AJ. 1993. Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiology 101, 13-24.
10. D'Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J. 2007. Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. The Plant Journal 49, 194-207.
11. Dicke M, Baldwin IT. 2010. The evolutionary context for herbivoreinduced plant volatiles: beyond the 'cry for help'. Trends in Plant Science 15, 167-175.
12. Farmer EE, Almeras E, Krishnamurthy V. 2003. Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Current Opinion in Plant Biology 6, 372-378.
13. Gardner HW, Grove MJ, Salch YP. 1996. Enzymic pathway to ethyl vinyl ketone and 2-pentenal in soybean preparations. Journal of Agricultural and Food Chemistry 44, 882-886.
14. Griffiths A, Prestage S, Linforth R, Zhang JL, Taylor A, Grierson D. 1999. Fruit-specific lipoxygenase suppression in antisense-transgenic tomatoes. Postharvest Biology and Technology 17, 163-173.
15. Goff SA, Klee HJ. 2006. Plant volatile compounds: sensory cues for health and nutritional value? Science 311, 815-819.
16. Halitschke R, Baldwin IT. 2003. Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. The Plant Journal 36, 794-807.
17. Halitschke R, Ziegler J, Keinanen M, Baldwin IT. 2004. Silencing of hydroperoxide lyase and allene oxide synthase reveals substrate and defense signaling crosstalk in Nicotiana attenuata. The Plant Journal 40, 35-46.
18. Howe GA, Jander G. 2008. Plant immunity to insect herbivores. Annual Review of Plant Biology 59, 41-66.
19. Howe GA, Lee GI, Itoh A, Li L, DeRocher AE. 2000. Cytochrome P450-dependent metabolism of oxylipins in tomato. Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase. Plant Physiology 123, 711-724.
20. Kachroo A, Kachroo P. 2009. Fatty acid-derived signals in plant defense. Annual Review of Phytopathology 47, 153-176.
21. Kim ES, Choi E, Kim Y, Cho KW, Lee A, Shim J, Rakwal R, Agrawal GK, Han OS. 2003. Dual positional specificity and expression of non-traditional lipoxygenase induced by wounding and methyl jasmonate in maize seedlings. Plant Molecular Biology 52, 1203-1213.
22. Kishimoto K, Matsui K, Ozawa R, Takabayashi J. 2005. Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant and Cell Physiology 46, 1093-1102.
23. Klee HJ. 2010. Improving the flavor of fresh fruits: genomics, biochemistry, and biotechnology. New Phytologist 187, 44-56.
24. Klee HJ, Tieman DM. 2013. Genetic challenges of flavor improvement in tomato. Trends in Genetics 29, 257-262.
25. Leon J, Royo J, Vancanneyt G, Sanz C, Silkowski H, Griffiths G, Sanchez-Serrano JJ. 2002. Lipoxygenase H1 gene silencing reveals a specific role in supplying fatty acid hydroperoxides for aliphatic aldehyde production. Journal of Biological Chemistry 277, 416-423.
26. Lund ST, Stall RE, Klee HJ. 1998. Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10, 371-382.
27. Mariutto M, Duby F, Adam A, Bureau C, Fauconnier ML, Ongena M, Thonart P, Dommes J. 2011. The elicitation of a systemic resistance by Pseudomonas putida BTP1 in tomato involves the stimulation of two lipoxygenase isoforms. BMC Plant Biology 11, 29.
28. Matsui K, Minami A, Hornung E, Shibata H, Kishimoto K, Ahnert V, Kindl H, Kajiwara T, Feussner I. 2006. Biosynthesis of fatty acid derived aldehydes is induced upon mechanical wounding and its products show fungicidal activities in cucumber. Phytochemistry 67, 649-657.
29. O'Donnell PJ, Schmelz E, Block A, Miersch O, Wasternack C, Jones JB, Klee HJ. 2003. Multiple hormones act sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiology 133, 1181-1189.
30. Park S-W, Li W, Viehhauser A, et al. 2013. Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis. Proceedings of the National Academy of Sciences, USA 110, 9559-9564.
31. Park YS, Kunze S, Ni XZ, Feussner I, Kolomiets MV. 2010. Comparative molecular and biochemical characterization of segmentally duplicated 9-lipoxygenase genes ZmLOX4 and ZmLOX5 of maize. Planta 231, 1425-1437.
32. Porta H, Rocha-Sosa M. 2002. Plant lipoxygenases. Physiological and molecular features. Plant Physiology 130, 15-21.
33. Salas JJ, Garcia-Gonzalez DL, Aparicio R. 2006. Volatile compound biosynthesis by green leaves from an Arabidopsis thaliana hydroperoxide lyase knockout mutant. Journal of Agricultural and Food Chemistry 54, 8199-8205.
34. Salch YP, Grove MJ, Takamura H, Gardner HW. 1995. Characterization of a C-5,13-cleaving enzyme of 13(S)-hydroperoxide of linolenic acid by soybean seed. Plant Physiology 108, 1211-1218.
35. Scala A, Mirabella R, Mugo C, Matsui K, Haring MA, Schuurink RC. 2013. E-2-hexenal promotes susceptibility to Pseudomonas syringae by activating jasmonic acid pathways in Arabidopsis. Frontiers in Plant Science 4, 74.
36. Schaller A, Stintzi A. 2009. Enzymes in jasmonate biosynthesis -structure, function, regulation. Phytochemistry 70, 1532-1538.
37. Schmelz EA, Engelberth J, Tumlinson JH, Block A, Alborn HT. 2004. The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. The Plant Journal 39, 790-808.
38. Schwab W, Davidovich-Rikanati R, Lewinsohn E. 2008. Biosynthesis of plant-derived flavor compounds. The Plant Journal 54, 712-732.
39. Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J. 2006. Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proceedings of the National Academy of Sciences, USA 103, 16672-16676.
40. Speirs J, Lee E, Holt K, Yong-Duk K, Scott NS, Loveys B, Schuch W. 1998. Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiology 117, 1047-1058.
41. Stintzi A, Weber H, Reymond P, Browse J, Farmer EE. 2001. Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proceedings of the National Academy of Sciences, USA 98, 12837-12842.
42. Tieman D, Bliss P, McIntyre LM, et al. 2012. The chemical interactions underlying tomato flavor preferences. Current Biology 22, 1035-1039.
43. Tieman DM, Zeigler M, Schmelz EA, Taylor MG, Bliss P, Kirst M, Klee HJ. 2006. Identification of loci affecting flavour volatile emissions in tomato fruits. Journal of Experimental Botany 57, 887-896.
44. Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castanera P, Sanchez-Serrano JJ. 2001. Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proceedings of the National Academy of Sciences, USA 98, 8139-8144.
45. Weber H. 2002. Fatty acid-derived signals in plants. Trends in Plant Science 7, 217-224.