A novel plastidial lipoxygenase of maize (Zea mays) ZmLOX6 encodes for a fatty acid hydroperoxide lyase and is uniquely regulated by phytohormones and pathogen infection

Agrawal GK, Tamogami S, Han O, Iwahashi H, Rakwal R (2004) Rice octadecanoid pathway. Biochem Biophys Res Commun 317:1–15 Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479 Bachmann A, Hause B, Maucher H, Garbe E, Voros K, Weichert H, Wasternack C, Feussner I (2002) Jasmonate-induced lipid peroxidation in barley leaves initiated by distinct 13-LOX forms of chloroplasts. Biol Chem 383:1645–1657 Berger S, Bell E, Mullet JE (1996) Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiol 111:525–531 Blee E (1998) Phytooxylipins and plant defense reactions. Prog Lipid Res 37:33–72 Bohland C, Balkenhohl T, Loers G, Feussner I, Grambow HJ (1997) Differential induction of lipoxygenase isoforms in wheat upon treatment with rust fungus elicitor, chitin oligosaccharides, chitosan, and methyl jasmonate. Plant Physiol 114:679–685 Brash AR (1999) Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J Biol Chem 274:23679–23682 Cacas JL, Vailleau F, Devoine C, Ennar N, Agnel JP, Tronchet M, Ponchet M, Blein JP, Roby D, Triantaphylides C, Montillet JL (2005) The combined action of 9 lipoxygenase and galactolipase is sufficient to bring about programmed cell death during tobacco hypersensitive response. Plant Cell Environ 28:1367–1378 Davoine C, Falletti O, Douki T, Iacazio G, Ennar N, Montillet JL, Triantaphylides C (2006) Adducts of oxylipin electrophiles to glutathione reflect a 13 specificity of the downstream lipoxygenase pathway in the tobacco hypersensitive response. Plant Physiol 140:1484–1493 Doares SH, Narvaez-Vasquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746 Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297 Fisher AJ, Grimes HD, Fall R (2003) The biochemical origin of pentenol emissions from wounded leaves. Phytochemistry 62:159–163 Gao X, Shim W-B, Göbel C, Kunze S, Feussner I, Meeley R, Balint-Kurti P, Kolomiets M (2007) Disruption of a maize 9-lipoxygenase results in increased resistance to fungal pathogens and reduced levels of contamination with mycotoxin fumonisin. Mol Plant Microbe Interact 20:922–933 Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann Rev Phytopathol 43:205–207 Glazebrook J, Chen WJ, Estes B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217–228 Göbel C, Feussner I, Hamberg M, Rosahl S (2002) Oxylipin profiling in pathogen-infected potato leaves. Biochim Biophys Acta 1584:55–64 Halitschke R, Baldwin IT (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J 36:794–807 Han O, Kim E, Choi E (2001) Methyl jasmonate induces biphasic accumulation of lipoxygenase mRNA in maize seedlings. FASEB J 15:A194–A194 Hause B, Voros K, Kogel KH, Besser K, Wasternack C (1999) A jasmonate-responsive lipoxygenase of barley leaves is induced by plant activators but not by pathogens. J Plant Physiol 154:459–462 Heck S, Grau T, Buchala A, Metraux JP, Nawrath C (2003) Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the Arabidopsis–Pseudomonas syringae pv. tomato interaction. Plant J 36:342–352 Hornung E, Walther M, Kuhn H, Feussner I (1999) Conversion of cucumber linoleate 13-lipoxygenase to a 9-lipoxygenating species by site-directed mutagenesis. Proc Natl Acad Sci USA 96:4192–4197 Howe GA, Schilmiller AL (2002) Oxylipin metabolism in response to stress. Curr Opin Plant Biol 5:230–236 Isakeit T, Gao X, Kolomiets M (2007) Increased resistance of a maize mutant lacking the 9-lipoxigenase gene, ZmLOX3, to root rot caused by Exserohilum pedicellatum. J Phytopathol. doi:10.1111/j.1439-0434.2007.01301.x Itoh A, Howe GA (2001) Molecular cloning of a divinyl ether synthase—identification as a CYP74 cytochrome P-450. J Biol Chem 276:3620–3627 Jensen AB, Poca E, Rigaud M, Freyssinet G, Pages M (1997) Molecular characterization of L2 lipoxygenase from maize embryos. Plant Mol Biol 33:605–614 Kim ES, Back K, Baik M, Choi E, Han O (2001) Sequence of the wound-responsive lipoxygenase gene from maize seedlings. J Biochem Mol Biol 34:259–261 Kim ES, Kim H, Park RD, Lee Y, Han O (2002) Dual positional specificity of wound-responsive lipoxygenase from maize seedlings. J Plant Physiol 159:1263–1265 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 Mol Biol 52:1203–1213 Kolomiets MV, Chen H, Gladon RJ, Braun EJ, Hannapel DJ (2000) A leaf lipoxygenase of potato induced specifically by pathogen infection. Plant Physiol 124:1121–1130 Kolomiets MV, Hannapel DJ, Chen H, Tymeson M, Gladon RJ (2001) Lipoxygenase is involved in the control of potato tuber development. Plant Cell 13:613–626 Kolomiets M, Navarro P, Zhang J, Yalpani N, Simmons C, Meeley B, Duvick J (2004) Identification and characterization of the lipoxygenase gene family of maize. Mycopathologia 157:501 Liavonchanka A, Feussner N (2006) Lipoxygenases: occurrence, functions and catalysis. J Plant Physiol 163:348–357 Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 8:532–540 Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178 Majeran W, Cai Y, Sun Q, Klaas J, van Wijk KJ (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17:3111–3140 Meeley RB, Johal GS, Briggs SP, Walton JD (1992) A biochemical phenotype for a disease resistance gene of maize. Plant Cell 4:71–77 Molik S, Karnauchov I, Weidlich C, Herrmann RG, Klösgen RB (2001) The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J Biol Chem 276:42761–42766 Montillet JL, Agnel JP, Ponchet M, Vailleau F, Roby D, Triantaphylides C (2002) Lipoxygenase-mediated production of fatty acid hydroperoxides is a specific signature of the hypersensitive reaction in plants. Plant Physiol Biochem 40:633–639 Moons A, Prinsen E, Bauw G, Van Montagu M (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9:2243–2259 Multani DS, Meeley RB, Paterson AH, Gray J, Briggs SP, Johal GS (1998) Plant–pathogen microevolution: molecular basis for the origin of a fungal disease in maize. Proc Natl Acad Sci USA 95:1686–1691 Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262 Nemchenko A, Kunze S, Feussner I, Kolomiets M (2006) Duplicate maize 13-lipoxygenase genes are differentially regulated by circadian rhythm, cold stress, wounding, pathogen infection, and hormonal treatments. J Exp Bot 57:3767–3779 Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol 39:500–507 O’Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 13:1914–1917 Ongena M, Duby F, Rossignol F, Fauconnier ML, Dommes J, Thonart P (2004) Stimulation of the lipoxygenase pathway is associated with systemic resistance induced in bean by a nonpathogenic Pseudomonas strain. Mol Plant Microbe Interact 17:1009–1018 Peña-Cortés H, Albrecht T, Prat S, Weiler EW, Willmitzer L (1993) Aspirin prevents wound-induced gene-expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128 Penninckx IA, Thomma BP, Buchala A, Métraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113 Prigge ST, Boyington JC, Gaffney BJ, Amzel LM (1996) Structure conservation in lipoxygenases: structural analysis of soybean lipoxygenase-1 and modeling of human lipoxygenases. Proteins 24:275–291 Prost I, Dhondt S, Rothe G, Vicente J, Rodriguez MJ, Kift N, Carbonne F, Griffiths G, Esquerre-Tugaye MT, Rosahl S, Castresana C, Hamberg M, Fournier J (2005) Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol 139:1902–1913 Rojo E, Leon J, Sanchez-Serrano JJ (1999) Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20:135–142 Rojo E, Solano R, Sanchez-Serrano JJ (2003) Interactions between signaling compounds involved in plant defense. J Plant Grow Regul 22:82–98 Salch YP, Grove MJ, Takamura H, Gardner HW (1995) Characterization of a C-5, 13-cleaving enzyme of H(S)-hydroperoxide of linolenic acid by soybean seed. Plant Physiol 108:1211–1218 Siedow JN (1991) Plant lipoxygenase—structure and function. Annu Rev Plant Physiol Plant Mol Biol 42:145–188 Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, Van Loon LC, Dong XN, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770 Stumpe M, Feussner I (2006) Formation of oxylipins by CYP74 enzymes. Phytochem Rev 5:347–357 Thaler JS, Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85:48–58 Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TC (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26 Veronico P, Giannino D, Melillo MT, Leone A, Reyes A, Kennedy MW, Bleve-Zacheo T (2006) A novel lipoxygenase in pea roots. Its function in wounding and biotic stress. Plant Physiol 141:1045–1055 Vörös K, Feussner I, Kuhn H, Lee J, Graner A, Lobler M, Parthier B, Wasternack C (1998) Characterization of a methyljasmonate-inducible lipoxygenase from barley (Hordeum vulgare cv. Salome) leaves. Eur J Biochem 251:36–44 Wilson RA, Gardner HW, Keller NP (2001) Cultivar-dependent expression of a maize lipoxygenase responsive to seed infesting fungi. Mol Plant Microbe Interact 14:980–987 Xu Y, Chang P, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077–1085 Yu Z, Schneider C, Boeglin WE, Marnett LJ, Brash AR (2003) The lipoxygenase gene ALOXE3 implicated in skin differentiation encodes a hydroperoxide isomerase. Proc Natl Acad Sci USA 100:9162–9167 Zabbai F, Jarosch B, Schaffrath U (2004) Over-expression of chloroplastic lipoxygenase RCI1 causes PR1 transcript accumulation in transiently transformed rice. Physiol Mol Plant Pathol 64:37–43 Zhang J, Simmons C, Yalpani N, Crane V, Wilkinson H, Kolomiets M (2005) Genomic analysis of the 12-oxo-phytodienoic acid reductase gene family of Zea mays. Plant Mol Biol 59:323–343