The final publication is available at link.springer.com.
The online version of this article (doi:10.1007/s11103-013-0144-y) contains supplementary material, which is available to authorized users.
All documents in ORBi are protected by a user license.
[en] The rhizobacterium Pseudomonas putida BTP1 stimulates induced systemic resistance (ISR) in tomato. A previous work showed that the resistance is associated in leaves with the induction of the first enzyme of the oxylipin pathway, the lipoxygenase (LOX), leading to a faster accumulation of its product, the free 13-hydroperoxy octadecatrienoic acid (13-HPOT), 2 days after Botrytis cinerea inoculation. In the present study, we further investigated the stimulation of the oxylipin pathway: metabolites and enzymes of the pathway were analyzed to understand the fate of the 13-HPOT in ISR. Actually the stimulation began upstream the LOX: free linolenic acid accumulated faster in P. putida BTP1-treated plants than in control. Downstream, the LOX products 13-fatty acid hydroperoxides esterified to galactolipids and phospholipids were more abundant in bacterized plants than in control before infection. These metabolites could constitute a pool that will be used after pathogen attack to produce free fungitoxic metabolites through the action of phospholipase A2, which is enhanced in bacterized plants upon infection. Enzymatic branches which can use as substrate the fatty acid hydroperoxides were differentially regulated in bacterized plants in comparison to control plants, so as to lead to the accumulation of the most fungitoxic compounds against B. cinerea. Our study, which is the first to demonstrate the accumulation of an esterified defense metabolite during rhizobacteria-mediated induced systemic resistance, showed that the oxylipin pathway is differentially regulated. It suggests that this allows the plant to prepare to a future infection, and to respond faster and in a more effective way to B. cinerea invasion.
Ahn I-P, Lee S-W, Suh S-C (2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Mol Plant Microbe Interact 20: 759-768.
Andersson MX, Hamberg M, Kourtchenko O, Brunnström A, McPhail KL, Gerwick WH, Göbel C, Feussner I, Ellerström M (2006) Oxo-phytodienoic acid-containing galactolipids in Arabidopsis: jasmonate signaling dependence. J Biol Chem 281: 31528-31537.
Andreou A, Feussner I (2009) Lipoxygenase-structure and reaction mechanism. Phytochemistry 70: 13-14.
Aprea E, Gika H, Carlin S, Theodoridis G, Vrhovsek U, Mattivi F (2011) Metabolite profiling on apple volatile content based on solid phase microextraction and gas-chromatography time of flight mass spectrometry. J Chromatogr A 1218: 4517-4524.
Audenaert K, De Meyer GB, Höfte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol 128: 491-501.
Bate NJ, Rothstein SJ (1998) C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J 16: 561-569.
Bent E (2006) Induced systemic resistance mediated by plant growth-promoting rhizobactera (PGPR) and fungi (PGPF). In: Tuzun S and Bent E (eds) Multigenic and induced systemic resistance in plants. Springer, New York, p 225-258.
Blée E (2002) Impact of phyto-oxylipins in plant defense. Trends Plant Sci 7: 315-322.
Chechetkin IR, Mukhitova FK, Blufard AS, Yarin AY, Antsygina LL, Grechkin AN (2009) Unprecedented pathogen-inducible complex oxylipins from flax-linolipins A and B. FEBS J 276: 4463-4472.
Chehab EW, Kaspi R, Savchenko T, Rowe H, Negre-Zakharov F, Kliebenstein D, Dehesh K (2008) Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS ONE 3: 1-10.
Choudhary DK, Prakash A, Johri BN (2007) Induced systemic resistance (ISR) in plants: mechanism of action. Indian J Microbiol 47: 289-297.
Croft KPC, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol 101: 13-24.
De Vleesschauwer D, Höfte M (2009) Rhizobacteria induced systemic resistance. Adv Bot Res 51: 223-281.
Dixon DP, Lapthorn A, Edwards R (2002) Plant gluthatione transferases. Genome Biol 3: reviews 3004. 1-3004. 10.
Fauconnier ML, Rojas-Beltran J, Dupuis B, Delaplace P, Frettinger P, Gosset V, du Jardin P (2008) Changes in oxylipin synthesis after Phytophtora infestans infection of potato leaves do not correlate with resistance. Plant Physiol Biochem 46: 823-831.
Göbel C, Feussner I, Schmidt A, Scheel D, Sanchez-Serrano J, Hamberg M, Rosahl S (2001) Oxylipin profiling reveals the preferential stimulation of the 9-lipoxygenase pathway in elicitor-treated potato cells. J Biol Chem 276: 6267-6273.
Göbel C, Feussner I, Hamberg M, Rosahl S (2002) Oxylipin profiling in pathogen infected potato leaves. Biochim Biophys Acta 1584: 55-64.
Gosset V, Harmel N, Göbe C, Francis F, Haubruge E, Wathelet JP, du Jardin P, Feussner I, Fauconnier ML (2009) Attacks by a piercing-sucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa decemlineata Say) on potato plants (Solanum tuberosum L.) induce differential changes in volatile compound release and oxylipin synthesis. J Exp Bot 60: 1231-1240.
Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Annals microbiol 60: 579-598.
Heitz T, Bergey DR, Ryan CA (1997) A gene encoding a chloroplast-targeted lipoxygenase in tomato leaves is transiently induced by wounding, systemin, and methyl jasmonate. Plant Physiol 114: 1085-1093.
Howe GA, Schilmiller AL (2002) Oxylipin metabolism in response to stress. Curr Opin Plant Biol 5: 230-236.
Kim DK, Lee HJ, Lee Y (1994) Detection of two phospholipase A2 (PLA2) activities in leaves of higher plant Vicia faba and comparision with mamalian PLA2's. FEBS Lett 343: 213-218.
Kühn H, Borchert A (2002) Regulation of enzymatic lipid peroxidation: the interplay of peroxidizing and peroxide reducing enzymes. Free Radic Biol Med 33: 154-172.
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 Biol 11: 29.
Mercado-Blanco J, Bakker PA (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie van Leeuwenhoek 92: 367-389.
Mosblech A, Feussner I, Heilmann I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Phsiol Biochem 47: 511-517.
Nakashima A, Iijima Y, Aoki K, Shibata D, Sugimoto K, Takabayashi J, Matsui K (2011) Monogalactosyl diacylglycerol is a substrate for lipoxygenase: its implications for oxylipin formation from lipids. J Plant Interact 6: 93-97.
Ongena M, Giger A, Jacques P, Dommes J, Thonart P (2002) Study of bacterial determinants involved in the induction of systemic resistance in bean by Pseudomonas putida BTP1. Eur J Plant Pathol 108: 187-196.
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 Inter 17: 1009-1018.
Ongena M, Jourdan E, Schafer M, Kech C, Budzikiewicz H, Luxen A, Thonart P (2005) Isolation of an N-alkylated benzylamine derivative from Pseudomonas putida BTP1 as elicitor of induced systemic resistance in bean. Mol Plant Microbe Interact 18: 562-569.
Pieterse CMJ, van Pelt JA, Ton J. Parchmann S, Mueller MJ, Buchala AJ, Métraux JP, van Loon LC (2000) Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiol Mol Plant Pathol 57: 123-134.
Pieterse CMJ, van Der Ent S, van Pelt JA, van Loon LC (2007) The role of ethylene in rhizobacteria-induced systemic resistance (ISR). Adv Plant Ethylene Res. 325-331.
Pieterse CMJ, Leon-Reyes A, van der Ent S, van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5: 308-316.
Porta H, Rosa Sosa M (2002) Plant lipoxygenase. Physiological and molecular features. Plant Physiol 130: 15-21.
Pozo MJ, van Der Ent S, van Loon LC, Pieterse CMJ (2008) Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol 180: 511-523.
Prost I, Dhondt S, Rothe G, Vicente J, Rodriguez MJ, Kift N, Carbone F, Griffiths G, Esquerré-Tugayé 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.
Sailaja PR, Podile AR, Reddanna P (1998) Biocontrol strain of Bacillus subtilis AF1 rapidly induces lipoxygenase in groundnut (Arachis hypogaea L.) compared to crown rot pathogen Asperigllus niger. Eur J Plant Pathol 104: 125-132.
Schaller F (2001) Enzymes of the biosynthesis of octadecanoid-derived signalling molecules. J of Exp Bot 52: 11-23.
Schaller F, Stintzi A (2009) Enzymes in jasmonate biosynthesis- structure, function, regulation. Phytochem 70: 1532-1538.
van der Ent S, Verhagen BW, van Doorn R, Bakker D, Verlaan MG, Pel MJ, Joosten RG, Proveniers MC, van Loon LC, Ton J, Pieterse CMJ (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146: 1293-1304.
van der Ent S, van Wees SC, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70: 1581-1588.
van Peer R, Nieman GJ, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81: 728-734.
Vick BA (1991) A spectrophotometric assay for hydroperoxyde lyase. Lipids 26: 315-320.