Lipoxygenase in singlet oxygen generation as a response to wounding: in vivo imaging in Arabidopsis thaliana

. 2017 Aug 29 ; 7 (1) : 9831. [epub] 20170829

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28851974
Odkazy

PubMed 28851974
PubMed Central PMC5575249
DOI 10.1038/s41598-017-09758-1
PII: 10.1038/s41598-017-09758-1
Knihovny.cz E-zdroje

Wounding, one of the most intensive stresses influencing plants ontogeny and lifespan, can be induced by herbivory as well as by physical factors. Reactive oxygen species play indispensable role both in the local and systemic defense reactions which enable "reprogramming" of metabolic pathways to set new boundaries and physiological equilibrium suitable for survival. In our current study, we provide experimental evidence on the formation of singlet oxygen (1O2) after wounding of Arabidopsis leaves. It is shown that 1O2 is formed by triplet-triplet energy transfer from triplet carbonyls to molecular oxygen. Using lipoxygenase inhibitor catechol, it is demonstrated that lipid peroxidation is initiated by lipoxygenase. Suppression of 1O2 formation in lox2 mutant which lacks chloroplast lipoxygenase indicates that lipoxygenase localized in chloroplast is predominantly responsible for 1O2 formation. Interestingly, 1O2 formation is solely restricted to chloroplasts localized at the wounding site. Data presented in this study might provide novel insight into wound-induced signaling in the local defense reaction.

Zobrazit více v PubMed

Foyer CH, Lelandais M, Kunert KJ. Photooxidative stress in plants. Physiol. Plant. 1994;92:696–717. doi: 10.1111/j.1399-3054.1994.tb03042.x. DOI

Liu YD, et al. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant Journal. 2007;51:941–954. doi: 10.1111/j.1365-313X.2007.03191.x. PubMed DOI

Cramer, G. R., Urano, K., Delrot, S., Pezzotti, M. & Shinozaki, K. Effects of abiotic stress on plants: a systems biology perspective. Bmc Plant Biology11, doi:10.1186/1471-2229-11-163 (2011). PubMed PMC

Garces H, Durzan D, Pedroso MC. Mechanical stress elicits nitric oxide formation and DNA fragmentation in Arabidopsis thaliana. Annals of Botany. 2001;87:567–574. doi: 10.1006/anbo.2000.1356. DOI

Lin CC, et al. Nitric oxide activates superoxide dismutase and ascorbate peroxidase to repress the cell death induced by wounding. Plant molecular biology. 2011;77:235–249. doi: 10.1007/s11103-011-9805-x. PubMed DOI

Jankanpaa HJ, et al. Non-Photochemical Quenching Capacity in Arabidopsis thaliana Affects Herbivore Behaviour. Plos One. 2013;8 PubMed PMC

Arimura G-i, Kost C, Boland W. Herbivore-induced, indirect plant defences. Biochimica et biophysica acta. 2005;1734:91–111. doi: 10.1016/j.bbalip.2005.03.001. PubMed DOI

War AR, et al. Mechanisms of plant defense against insect herbivores. Plant Signaling & Behavior. 2012;7:1306–1320. doi: 10.4161/psb.21663. PubMed DOI PMC

Reymond P, Weber H, Damond M, Farmer EE. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell. 2000;12:707–719. doi: 10.1105/tpc.12.5.707. PubMed DOI PMC

Rehrig, E. M., Appel, H. M., Jones, A. D. & Schultz, J. C. Roles for jasmonate- and ethylene-induced transcription factors in the ability of Arabidopsis to respond differentially to damage caused by two insect herbivores. Frontiers in Plant Science5, doi:10.3389/fpls.2014.00407 (2014). PubMed PMC

Savatin, D. V., Gramegna, G., Modesti, V. & Cervone, F. Wounding in the plant tissue: the defense of a dangerous passage. Frontiers in Plant Science5, doi:10.3389/fpls.2014.00470 (2014). PubMed PMC

Thapa R, Poudyal G, Maharjan N, Bernstein PS. Demographics and awareness of diabetic retinopathy among diabetic patients attending the vitreo-retinal service at a tertiary eye care center in Nepal. Nepal J Ophthalmol. 2012;4:10–16. PubMed

Hernández-Oñate MA, Herrera-Estrella A. Damage response involves mechanisms conserved across plants, animals and fungi. Current Genetics. 2015;61:359–372. doi: 10.1007/s00294-014-0467-5. PubMed DOI

McDowell RE, Amsler MO, Li Q, Lancaster JR, Amsler CD. The Immediate Wound-Induced Oxidative Burst of Saccharina Latissima Depends on Light Via Photosynthetic Electron Transport. J. Phycol. 2015;51:431–441. doi: 10.1111/jpy.12302. PubMed DOI

Hlaváčková V, et al. Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta. 2006;225 doi: 10.1007/s00425-006-0325-x. PubMed DOI

Oyarce P, Gurovich L. Evidence for the transmission of information through electric potentials in injured avocado trees. Journal of Plant Physiology. 2011;168:103–108. doi: 10.1016/j.jplph.2010.06.003. PubMed DOI

Roach T, et al. A proposed interplay between peroxidase, amine oxidase and lipoxygenase in the wounding-induced oxidative burst in Pisum sativum seedlings. Phytochemistry. 2015;112:130–138. doi: 10.1016/j.phytochem.2014.06.003. PubMed DOI

Pohnert G. Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiology. 2002;129:103–111. doi: 10.1104/pp.010974. PubMed DOI PMC

de Bruxelles GL, Roberts MR. Signals regulating multiple responses to wounding and herbivores. Critical Reviews in Plant Sciences. 2001;20:487–521. doi: 10.1080/07352689.2001.10131828. DOI

Schaller A, Stintzi A. Enzymes in jasmonate biosynthesis - Structure, function, regulation. Phytochemistry. 2009;70:1532–1538. doi: 10.1016/j.phytochem.2009.07.032. PubMed DOI

Mochizuki S, Sugimoto K, Koeduka T, Matsui K. Arabidopsis lipoxygenase 2 is essential for formation of green leaf volatiles and five-carbon volatiles. Febs Letters. 2016;590:1017–1027. doi: 10.1002/1873-3468.12133. PubMed DOI

Bannenberg G, Martinez M, Hamberg M, Castresana C. Diversity of the Enzymatic Activity in the Lipoxygenase Gene Family of Arabidopsis thaliana. Lipids. 2009;44:85–95. doi: 10.1007/s11745-008-3245-7. PubMed DOI

Andreou A, Brodhun F, Feussner I. Biosynthesis of oxylipins in non-mammals. Progress in Lipid Research. 2009;48:148–170. doi: 10.1016/j.plipres.2009.02.002. PubMed DOI

Zhao YY, Qian CL, Chen JC, Peng Y, Mao LC. Responses of phospholipase D and lipoxygenase to mechanical wounding in postharvest cucumber fruits. Journal of Zhejiang University-Science B. 2010;11:443–450. doi: 10.1631/jzus.B0900357. PubMed DOI PMC

Halliwell, B. & Gutteridge, J. Free Radicals in Biology and Medicine, Ed 4. (Oxford University Press, 2007).

Miyamoto S, Martinez GR, Medeiros MHG, Di Mascio P. Singlet molecular oxygen generated by biological hydroperoxides. Journal of photochemistry and photobiology B: Biology. 2014;139:24–33. doi: 10.1016/j.jphotobiol.2014.03.028. PubMed DOI

Pospíšil P, Prasad A, Rác M. Role of reactive oxygen species in ultra-weak photon emission in biological systems. Journal of Photochemistry and Photobiology B-Biology. 2014;139:11–23. doi: 10.1016/j.jphotobiol.2014.02.008. PubMed DOI

Cilento G, Adam W. From free radicals to electronically excited species. Free radical biology & medicine. 1995;19:103–114. doi: 10.1016/0891-5849(95)00002-F. PubMed DOI

Miyamoto, S. & Di Mascio, P. in Lipid Hydroperoxide-Derived Modification of Biomolecules Vol. 77 Subcellular Biochemistry (ed Y. Kato) 3-20 (2014).

Fedorova, G. F., Trofimov, A. V., Vasil’ev, R. F. & Veprintsev, T. L. Peroxy-radical-mediated chemiluminescence: mechanistic diversity and fundamentals for antioxidant assay. Arkivoc, 163-215 (2007).

Flors C, et al. Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green. J Exp Bot. 2006;57:1725–1734. doi: 10.1093/jxb/erj181. PubMed DOI

Cilento G, Nascimento ALTO. Generation of Electronically Excited Triplet Species at the Cellular-Level - a Potential Source of Genotoxicity. Toxicology Letters. 1993;67:17–28. doi: 10.1016/0378-4274(93)90043-W. PubMed DOI

Prasad, A., Ferretti, U., Sedlářová, M. & Pospíšil, P. Singlet oxygen production in Chlamydomonas reinhardtii under heat stress. Scientific Reports6, doi:10.1038/srep20094 (2016). PubMed PMC

Biles CL, et al. Differential chlorate inhibition of Chaetomium globosum germination, hyphal growth, and perithecia synthesis. Mycopathologia. 2012;174:475–487. doi: 10.1007/s11046-012-9572-5. PubMed DOI

Wang YH, Irving HR. Developing a model of plant hormone interactions. Plant Signaling & Behavior. 2011;6:494–500. doi: 10.4161/psb.6.4.14558. PubMed DOI PMC

Prasad A, Pospíšil P. Towards the two-dimensional imaging of spontaneous ultra-weak photon emission from microbial, plant and animal cells. Scientific Reports. 2013;3 doi: 10.1038/srep01211. PubMed DOI PMC

Flor-Henry M, McCabe TC, de Bruxelles GL, Roberts MR. Use of a highly sensitive two-dimensional luminescence imaging system to monitor endogenous bioluminescence in plant leaves. BMC Plant Biology. 2004;4:19–19. doi: 10.1186/1471-2229-4-19. PubMed DOI PMC

Birtic S, et al. Using spontaneous photon emission to image lipid oxidation patterns in plant tissues. Plant J. 2011;67:1103–1115. doi: 10.1111/j.1365-313X.2011.04646.x. PubMed DOI

Orozco-Cardenas M, Ryan CA. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. P Natl Acad Sci USA. 1999;96:6553–6557. doi: 10.1073/pnas.96.11.6553. PubMed DOI PMC

Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA. 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. 2001;13:179–191. doi: 10.1105/tpc.13.1.179. PubMed DOI PMC

Wu, J. Q. & Baldwin, I. T. in Annual Review of Genetics, Vol 44 Vol. 44 Annual Review of Genetics (eds A. Campbell, M. Lichten, & G. Schupbach) 1-24 (2010).

Morker KH, Roberts MR. Light as both an input and an output of wound-induced reactive oxygen formation in Arabidopsis leaves. Plant Signaling & Behavior. 2011;6:1087–1089. doi: 10.4161/psb.6.8.15823. PubMed DOI PMC

Beneloujaephajri, E., Costa, A., L’Haridon, F., Metraux, J. P. & Binda, M. Production of reactive oxygen species and wound-induced resistance in Arabidopsis thaliana against Botrytis cinerea are preceded and depend on a burst of calcium. Bmc Plant Biology13, doi:10.1186/1471-2229-13-160 (2013). PubMed PMC

Zimmerman GL, Snyder HE. Role of Calcium in Activating Soybean Lipoxygenase-2. Journal of Agricultural and Food Chemistry. 1974;22:802–805. doi: 10.1021/jf60195a006. PubMed DOI

Wang X. Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiology. 2005;139:566–573. doi: 10.1104/pp.105.068809. PubMed DOI PMC

Bargmann BO, Munnik T. The role of phospholipase D in plant stress responses. Current Opinion in Plant Biology. 2006;9:515–522. doi: 10.1016/j.pbi.2006.07.011. PubMed DOI

Bargmann BOR, et al. Reassessing the role of phospholipase D in the Arabidopsis wounding response. Plant Cell and Environment. 2009;32:837–850. doi: 10.1111/j.1365-3040.2009.01962.x. PubMed DOI

Kanofsky JR. Singlet Oxygen Production From the Reactions of Alkylperoxy Radicals - Evidence from 1268-Nm Chemiluminescence. Journal of Organic Chemistry. 1986;51:3386–3388. doi: 10.1021/jo00367a032. DOI

Kochevar IE. Singlet oxygen signaling: from intimate to global. Science’s STKE: signal transduction knowledge environment. 2004;2004 PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...