Traumatin- and dinortraumatin-containing galactolipids in arabidopsis: Their formation in tissue-disrupted leaves as counterparts of green leaf volatiles

Journal of Biological Chemistry

Volumn 288, Issue 36, 2013, Pages 26078-26088

  Nakashima, Anna ^a   Von Reuss, Stephan H ^b   Tasaka, Hiroyuki ^a   Nomura, Misaki ^a   Mochizuki, Satoshi ^a   Iijima, Yoko ^c,d   Aoki, Koh ^c,e   Shibata, Daisuke ^c   Boland, Wilhelm ^b   Takabayashi, Junji ^f   Matsui, Kenji ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c KAZUSA DNA RESEARCH INSTITUTE   (Japan)

^d KANAGAWA INSTITUTE OF TECHNOLOGY   (Japan)

^e Osaka Prefecture University   (Japan)

^f KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; BIOSYNTHETIC PATHWAY; FREE FATTY ACID; GALACTOLIPIDS; GREEN LEAF VOLATILES; HYDROPEROXIDE LYASE; OXO-ACIDS; PLANT DEFENSE;

BIOCHEMISTRY;

BIOLOGY;

ALDEHYDE; DINORTRAUMATIN; GALACTOLIPID; GALACTOSYLDIACYLGLYCEROL; HYDROPEROXIDE LYASE; LYASE; OXYLIPIN; TRAUMATIN; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CABBAGE; CHEMICAL STRUCTURE; ENZYME DEGRADATION; ENZYME MECHANISM; ENZYME SYNTHESIS; NONHUMAN; PHASEOLUS VULGARIS; PLANT LEAF; PLANT TISSUE; PRIORITY JOURNAL; TOBACCO; TOMATO;

GLYCOLIPIDS; GREEN LEAF VOLATILES; HYDROPEROXIDE LYASE; LIPID PEROXIDATION; LIPOXYGENASE PATHWAY; MASS SPECTROMETRY (MS); PLANT BIOCHEMISTRY;

ALDEHYDE-LYASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSICA; CYTOCHROME P-450 ENZYME SYSTEM; FATTY ACIDS, MONOUNSATURATED; GALACTOLIPIDS; LYCOPERSICON ESCULENTUM; OILS, VOLATILE; OXYLIPINS; PHASEOLUS; PLANT LEAVES; TOBACCO;

EID: 84883702446     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.487959     Document Type: Article

References (52)

1. Matsui, K. (2006) Green leaf volatiles. Hydroperoxide lyase pathway of oxylipin metabolism. Curr. Opin. Plant Biol. 9, 274-280
2. D'Auria, J. C., Pichersky, E., Schaub, A., Hansel, A., and Gershenzon, J. (2007) Characterization of BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J. 49, 194-207
3. Allmann, S., and Baldwin, I. T. (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329, 1075-1078
4. Hammond, D. G., Rangel, S., and Kubo, I. (2000) Volatile aldehydes are promising broad-spectrum postharvest insecticides. J. Agric. Food Chem. 48, 4410-4417
5. Nakamura, S., and Hatanaka, A. (2002) Green-leaf-derived C6 aroma compounds with potent antibacterial action that act on both gram-negative and gram-positive bacteria. J. Agric. Food Chem. 50, 7639-7644
6. Kishimoto, K., Matsui, K., Ozawa, R., and Takabayashi, J. (2008) Direct fungicidal activities of C6-aldehydes are important constituents for defense responses in Arabidopsis against Botrytis cinerea. Phytochemistry 69, 2127-2132
7. Hubert, J., Münzbergová, Z., and Santino, A. (2008) Plant volatile aldehydes as natural insecticides against stored-product beetles. Pest Manag. Sci. 64, 57-64
8. Matsui, K., Sugimoto, K., Mano, J., Ozawa, R., and Takabayashi, J. (2012) Differential metabolisms of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements. PLoS One 7, e36433
9. Arimura, G., Matsui, K., and Takabayashi, J. (2009) Chemical and molecular ecology of herbivore-induced plant volatiles. Proximate factors and their ultimate functions. Plant Cell Physiol. 50, 911-923
10. Grechkin, A. N., and Hamberg, M. (2004) The "heterolytic hydroperoxide lyase" is an isomerase producing a short-lived fatty acid hemiacetal. Biochim. Biophys. Acta 1636, 47-58
11. Mosblech, A., Feussner, I., and Heilmann, I. (2009) Oxylipins. Structurally diverse metabolites from fatty acid oxidation. Plant Physiol. Biochem. 47, 511-517
12. Stelmach, B. A., Müller, A., Hennig, P., Gebhardt, S., Schubert-Zsilavecz, M., and Weiler, E. W. (2001) A novel class of oxylipins, sn1-O-(12-oxophytodienoyl)- sn2-O-(hexadecatrienoyl)-monogalactosyl diglyceride, from Arabidopsis thaliana. J. Biol. Chem. 276, 12832-12838
13. Buseman, C. M., Tamura, P., Sparks, A. A., Baughman, E. J., Maatta, S., Zhao, J., Roth, M. R., Esch, S. W., Shah, J., Williams, T. D., and Welti, R. (2006) Wounding stimulates the accumulation of glycerolipids containing oxophytodienoic acid and dinor-oxophytodienoic acid in Arabidopsis leaves. Plant Physiol. 142, 28-39
14. Nilsson, A. K., Fahlberg, P., Ellerström, M., and Andersson, M. X. (2012) Oxo-phytodienoic acid (OPDA) is formed on fatty acids esterified to galactolipids after tissue disruption in Arabidopsis thaliana. FEBS Lett. 586, 2483-2487
15. Glauser, G., Dubugnon, L., Mousavi, S. A., Rudaz, S., Wolfender, J.-L., Farmer, E. E. (2009) Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J. Biol. Chem. 284, 34506-34513
16. Chechetkin, I. R., Mukhitova, F. K., Blufard, A. S., Yarin, A. Y., Antsygina, L. L., and Grechkin, A. N. (2009) Unprecedented pathogen-inducible complex oxylipins from flax. Linolipins A and B. FEBS J. 276, 4463-4472
17. Farmer, E. E., and Mueller, M. J. (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annu. Rev. Plant Biol. 64, 429-450
18. Mene-Saffrane, L., Dubugnon, L., Chételat, A., Stolz, S., Gouhier-Darimont, C., and Farmer, E. E. (2009) Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J. Biol. Chem. 284, 1702-1708
19. Ibrahim, A., Schültz, A.-L., Galano, J.-M., Herrfurth, C., Feussner, K., Durand, T., Brodhun, F., and Feussner, I. (2011) The alphabet of galactolipids in Arabidopsis thaliana. Front. Plant Sci. 2, 95
20. Zoeller, M., Stingl, N., Krischke, M., Fekete, A., Waller, F., Berger, S., and Mueller, M. J. (2012) Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes. Biogenesis of pimelic and azelaic acid. Plant Physiol. 160, 365-378
21. Zimmerman D. C., and Coudron, C. A. (1979) Identification of traumatin, a wound hormone, as 12-oxo-trans-10-dodecenoic acid. Plant Physiol. 63, 536-541
22. Kallenbach, M., Gilardoni, P. A., Allmann, S., Baldwin, I. T., and Bonaventure, G. (2011) C12 derivatives of the hydroperoxide lyase pathway are produced by product recycling through lipoxygenase-2 in Nicotiana attenuata leaves. New Phytol. 191, 1054-1068
23. Duan, H., Huang, M. Y., Palacio, K., and Schuler, M. A. (2005) Variations in CYP74B2 (hydroperoxide lyase) gene expression differentially affect hexenal signaling in the Columbia and Landsberg erecta ecotypes of Arabidopsis. Plant Physiol. 139, 1529-1544
24. Li-Beisson, Y., Shorrosh, B., Beisson, F., Andersson, M. X., Arondel, V., Bates, P. D., Baud, S., Bird, D., Debono, A., Durrett, T. P., Franke, R. B., Graham, I. A., Katayama, K., Kelly, A. A., Larson, T., Markham, J. E., Miquel, M., Molina, I., Nishida, I., Rowland, O., Samuels, L., Schmid, K. M., Wada, H., Welti, R., Xu, C., Zallot, R., and Ohlrogge, J. (2010) Acyl-lipid Metabolism. Arabidopsis Book 8, e0133
25. Park, J. H., Halitschke, R., Kim, H. B., Baldwin, I. T., Feldmann, K. A., and Feyereisen, R. (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J. 31, 1-12
26. Shiojiri, K., Ozawa, R., Matsui, K., Sabelis, M. W., and Takabayashi, J., (2012) Intermittent exposure to traces of green leaf volatiles triggers a plant response. Sci. Rep. 2, 378
27. Noordermeer, M. A., Feussner, I., Kolbe, A., Veldink, G. A., and Vliegenthart, J. F. G. (2000) Oxygenation of (3Z)-alkenals to 4-hydroxy-(2E)-alkenals in plant extracts. A nonenzymatic process. Biochem. Biophys. Res. Commun. 277, 112-116
28. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
29. Nakashima, A., Iijima, Y., Aoki, K., Shibata, D., Sugimoto, K., Takabayashi, J., and Matsui, K. (2011) Monogalactosyl diacylglycerol is a substrate for lipoxygenase: Its implications for oxylipin formation directly from lipids. J. Plant Interact. 6, 93-97
30. Matsui, K., Shibutani, M., Hase, T., Kajiwara, T. (1996) Bell pepper fruit fatty acid hydroperoxide lyase is a cytochrome P450 (CYP74B). FEBS Lett. 394, 21-24
31. Sakaki, T., Saito, K., Kawaguchi, A., Kondo, N., and Yamada, M. (1990) Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozonefumigated spinach leaves. Plant Physiol. 94, 766-772
32. Matsui, K., Sugimoto, K., Kakumyan, P., Khorobrykh, S. A., and Mano, J. (2009) Volatile oxylipins and related compounds formed under stress in plants. Methods Mol. Biol. 580, 17-28
33. Esterbauer, H., and Weger, W. (1967) Über die Wirkungen von Aldehyden auf gesunde und maligne Zellen, Mitt.: Synthese von homologen 4-Hydroxy-2-alkenalen, II. Monatsh. Chem. 98, 1994-2000
34. Sias, B., Ferrato, F., Grandval, P., Lafont, D., Boullanger, P., De Caro, A., Leboeuf, B., Verger, R., and Carriere, F. (2004) Human pancreatic lipaserelated protein 2 is a galactolipase. Biochemistry 43, 10138-10148
35. Nakanishi, H., Iida, Y., Shimizu, T., and Taguchi, R. (2010) Separation and quantification of sn-1 and sn-2 fatty acid positional isomers in phosphatidylcholine by RPLC-ESIMS/MS. J. Biochem. 147, 245-256
36. Hisamatsu Y., Goto, N., Hasegawa, K., and Shigemori, H. (2006) A glycolipid involved in flower bud formation of Arabidopsis thaliana. Bot. Stud. 47, 45-50
37. Komisarski, M., Kaczmarska, Z., and Kusmierek, J. T. (2009) Practical highly enantioselective synthesis of (R)- and (S)-(E)-4-hydroxynon-2- enal. Acta Biochim. Pol. 56, 189-193
38. Böttcher, C., and Weiler, E. W. (2007) Cyclo-oxylipin-galactolipids in plants. occurrence and dynamics. Planta 226, 629-637
39. Kandzia, R., Stumpe, M., Berndt, E., Szalata, M., Matsui, K., and Feussner, I., (2003) On the specificity of lipid hydroperoxide fragmentation by fatty acid hydroperoxide lyase from Arabidopsis thaliana. J. Plant Physiol. 160, 803-809
40. Hughes, R. K., Belfield, E. J., and Casey, R. (2006) CYP74C3 and CYP74A1, plant cytochrome P450 enzymes whose activity is regulated by detergent micelle association, and proposed new rules for the classification of CYP74 enzymes. Biochem. Soc. Trans. 34, 1223-1227
41. Bochkov, V. N., Oskolkova, O. V., Birukov, K. G., Levonen, A.-L., Binder, C. J., and Stöckl, J. (2010) Generation and biological activities of oxidized phospholipids. Antioxid. Redox Signal. 12, 1009-1059
42. Farmer, E. E., and Davoine, C. (2007) Reactive electrophile species. Curr. Opin. Plant Biol. 10, 380-386
43. Seltmann, M. A., Stingl, N. E., Lautenschlaeger, J. K., Krischke, M., Mueller, M. J., and Berger, S. (2010) Differential impact of lipoxygenase 2 and jasmonates on natural and stress-induced senescence in Arabidopsis. Plant Physiol. 152, 1940-1950
44. Ishiguro, S., Kawai-Oda, A., Ueda, J., 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
45. Bonaventure, G., Schuck, S., and Baldwin, I. T. (2011) Revealing complexity and specificity in the activation of lipase-mediated oxylipin biosynthesis. Aspecific role of the Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves and roots. Plant Cell Environ. 34, 1507-1520
46. Rose, U., Manukian, A., Heath, R. R., and Tumlinson, J. H. (1996) Volatile semiochemicals released from undamaged cotton leaves. A systemic response of living plants to caterpillar damage. Plant Physiol. 111, 487-495
47. Piesik, D., Lemnczyk, G., Skoczek, A., Lamparski, R., Bocianowski, J., Kotwica, K., and Delaney, K. J. (2011) Fusarium infection in maize. Volatile induction of infected and neighboring uninfected plants has the potential to attract a pest cereal leaf beetle, Oulema melanopus. J. Plant Physiol. 168, 1534-1542
48. Loreto, F., Barta, C., Brilli, F., and Nogues, I. (2006) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant Cell Environ. 29, 1820-1828
49. Engelberth, J., Alborn, H. T., Schmelz, E. A., and Tumlinson, J. H. (2004) Airborne signals prime plants against insect herbivore attack. Proc. Natl. Acad. Sci. U.S.A. 101, 1781-1785
50. Liu, X., Li, F., Tang, J., Wang, W., Zhang, F., Wang, G., Chu, J., Yan, C., Wang, T., Chu, C., and Li, C. (2012) Activation of the jasmonic acid pathway by depletion of the hydroperoxide lyase OsHPL3 reveals crosstalk between the HPL and AOS branches of the oxylipin pathway in rice. PLoS One 7, e50089
51. Deng, Y., Salomon, R. G. (1998) Total synthesis of -hydroxy, -unsaturated aldehydic esters of cholesterol and 2-lysophosphatidylcholine. J. Org. Chem. 63, 7779-7794
52. Podrez, E. A., Poliakov, E., Shen, Z., Zhang, R., Deng, Y., Sun, M., Finton, P. J., Shan, L., Febbraio, M., Hajjar, D. P., Silverstein, R. L., Hoff, H. F., Salomon, R. G., and Hazen, S. L. (2002) A novel family of atherogenic oxidized phospholipids promotes macrophage foam cell formation via the scavenger receptor CD36 and is enriched in atherosclerotic lesions. J. Biol. Chem. 277, 38517-38523