Skip to main content
Log in

Differential induction of oxylipin pathway in potato and tobacco cells by bacterial and oomycete elicitors

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Potato and tobacco cells are differentially suited to study oxylipin pathway and elicitor-induced responses.

Abstract

Synthesis of oxylipins via the lipoxygenase (LOX) pathway provides plant cells with an important class of signaling molecules, related to plant stress responses and innate immunity. The aim of this study was to evaluate the induction of LOX pathway in tobacco and potato cells induced by a concentrated culture filtrate (CCF) from Phytophthora infestans and lipopolysaccharide (LPS) from Pectobacterium atrosepticum. Oxylipin activation was evaluated by the measurement of LOX activity and metabolite quantification. The basal levels of oxylipins and fatty acids showed that potato cells contained higher amounts of linoleic (LA), linolenic (LnA) and stearic acids than tobacco cells. The major oxylipin in potato cells, 9(S),10(S),11(R)-trihydroxy-12(Z),15(Z)-octadecadienoic acid (9,10,11-THOD), was not detected in tobacco cells. CCF induced a sharp increase of LA and LnA at 8 h in tobacco cells. In contrast they decreased in potato cells. In CCF-treated tobacco cells, colneleic acid increased up to 24 h, colnelenic acid and 9(S)-hydroxyoctadecatrienoic acid (9(S)-HOT) increased up to 16 h. In potato cells, only colneleic acid increased slightly until 16 h. A differential induction of LOX activity was measured in both cells treated by CCF. With LPS treatment, only 9,10,11-THOD accumulation was significantly induced at 16 h in potato cells. Fatty acids were constant in tobacco but decreased in potato cells over the studied time period. These results showed that the two elicitors were differently perceived by the two Solanaceae and that oxylipin pathway is strongly induced in tobacco with the CCF. They also revealed that elicitor-induced responses depended on both cell culture and elicitor.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

CCF:

Concentrated culture filtrate

Cv:

Cultivar

HOD:

Hydroxy octadecadienoic acid

HOE:

Hydroxy octadecenoic acid

HOT:

Hydroxy octadecatrienoic acid

HPO:

Hydroperoxide

HPOD:

Hydroperoxy octadecadienoic acid

HPOT:

Hydroperoxy octadecatrienoic acid

HR:

Hypersensitive response

LAH:

Lipid acyl hydrolase

LOX:

Lipoxygenase

LPS:

Lipopolysaccharide

PAL:

Phenylalanine ammonia-lyase

PLA:

Phospholipase

Pv:

Pathovar

PUFA:

Polyunsaturated fatty acid

ROS:

Reactive oxygen species

References

  • Andreou A, Feussner I (2009) Lipoxygenases—structure and reaction mechanism. Phytochemistry 70(13–14):1504–1510. doi:10.1016/j.phytochem.2009.05.008

    Article  PubMed  CAS  Google Scholar 

  • Attard A, Gourgues M, Galiana E, Panabières F, Ponchet M, Keller H (2008) Strategies of attack and defense in plant-oomycete interactions, accentuated for Phytophthora parasitica Dastur (syn. P. Nicotianae Breda de Haan). J Plant Physiol 165(1):83–94. doi:10.1016/j.jplph.2007.06.011

    Article  PubMed  CAS  Google Scholar 

  • Blée E (2002) Impact of phyto-oxylipins in plant defense. Trends Plant Sci 7(7):315–322

    Article  PubMed  Google Scholar 

  • Blein J-P, Coutos-Thévenot P, Marion D, Ponchet M (2002) From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci 7(7):293–296

    Article  PubMed  CAS  Google Scholar 

  • Bourque S, Binet MN, Ponchet M, Pugin A, Lebrun-Garcia A (1999) Characterization of the cryptogein binding sites on plant plasma membranes. J Biol Chem 274(49):34699–34705. doi:10.1074/jbc.274.49.34699

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  PubMed  CAS  Google Scholar 

  • Cacas J-L, Vailleau F, Davoine C, Ennar N, Agnel J-P, Tronchet M, Ponchet M, Blein J-P, Roby D, Triantaphylides C, Montillet J-L (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(11):1367–1378

    Article  CAS  Google Scholar 

  • Christie WW (1993) Preparation of ester derivatives of fatty acids for chromatographic analysis. Adv Lipid Methodol 2:69–111

    Google Scholar 

  • Conconi A, Miquel M, Browse JA, Ryan CA (1996) Intracellular levels of free linolenic and linoleic acids increase in tomato leaves in response to wounding. Plant Physiol 111(3):797–803. doi:10.1104/pp.111.3.797

    PubMed  CAS  Google Scholar 

  • Desender S, Klarzynski O, Potin P, Barzic M-R, Andrivon D, Val F (2006) Lipopolysaccharides of Pectobacterium atrosepticum and Pseudomonas corrugata induce different defence response patterns in tobacco, tomato, and potato. Plant Biol 8(5):636–645

    Article  PubMed  CAS  Google Scholar 

  • Desender S, Andrivon D, Val F (2007) Activation of defence reactions in Solanaceae: where is the specificity? Cell Micro 9(1):21–30

    Article  CAS  Google Scholar 

  • Dhondt S, Gouzerh G, Müller A, Legrand M, Heitz T (2002) Spatio-temporal expression of patatin-like lipid acyl hydrolases and accumulation of jasmonates in elicitor-treated tobacco leaves are not affected by endogenous levels of salicylic acid. Plant J 32(5):749–762. doi:10.1046/j.1365-313X.2002.01465.x

    Article  PubMed  CAS  Google Scholar 

  • Erbs G, Newman M-A (2012) The role of lipopolysaccharide and peptidoglycan, two glycosylated bacterial microbe-associated molecular patterns (MAMPs), in plant innate immunity. Mol Plant Pathol 13(1):95–104. doi:10.1111/j.1364-3703.2011.00730.x

    Article  PubMed  CAS  Google Scholar 

  • Fammartino A, Cardinale F, Gobel C, Mene-Saffrane L, Fournier J, Feussner I, Esquerre-Tugaye M-T (2007) Characterization of a divinyl ether biosynthetic pathway specifically associated with pathogenesis in tobacco. Plant Physiol 143(1):378–388. doi:10.1104/pp.106.087304

    Article  PubMed  CAS  Google Scholar 

  • Fammartino A, Verdaguer B, Fournier J, Tamietti G, Carbonne F, Esquerré-Tugayé M-T, Cardinale F (2010) Coordinated transcriptional regulation of the divinyl ether biosynthetic genes in tobacco by signal molecules related to defense. Plant Physiol Biochem 48(4):225–231

    Article  PubMed  CAS  Google Scholar 

  • Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53(1):275–297. doi:doi:10.1146/annurev.arplant.53.100301.135248

    Article  PubMed  CAS  Google Scholar 

  • Fournier J, Pouénat M-L, Rickauer M, Rabinovltch-Chable H, Rigaud M, Esquerré-Tugayé M-T (1993) Purification and characterization of elicitor-induced lipoxygenase in tobacco cells. Plant J 3(1):63–70. doi:10.1111/j.1365-313X.1993.tb00011.x

    Article  CAS  Google Scholar 

  • Galliard T (1971) The enzymic deacylation of phospholipids and galactolipids in plants. Purification and properties of a lipolytic acyl-hydrolase from potato tubers. Biochem J 121:379–390

    PubMed  CAS  Google Scholar 

  • Gaquerel E, Hervé C, Labrière C, Boyen C, Potin P, Salaün J-P (2007) Evidence for oxylipin synthesis and induction of a new polyunsaturated fatty acid hydroxylase activity in Chondrus crispus in response to methyl jasmonate. Biochim Biophys Acta 1771(5):565–575

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Interact 19(7):711–724. doi:10.1094/mpmi-19-0711

    Article  PubMed  CAS  Google Scholar 

  • 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(9):6267–6273. doi:10.1074/jbc.M008606200

    Article  PubMed  Google Scholar 

  • Göbel C, Feussner I, Hamberg M, Rosahl S (2002) Oxylipin profiling in pathogen-infected potato leaves. Biochim Biophys Acta 1584(1):55–64

    Article  PubMed  Google Scholar 

  • Göbel C, Feussner I, Rosahl S (2003) Lipid peroxidation during the hypersensitive response in potato in the absence of 9-lipoxygenases. J Biol Chem 278(52):52834–52840. doi:10.1074/jbc.M310833200

    Article  PubMed  Google Scholar 

  • Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J (2000) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23(4):441–450. doi:10.1046/j.1365-313x.2000.00804.x

    Article  PubMed  CAS  Google Scholar 

  • Griffiths G, Leverentz M, Silkowski H, Gill N, Sánchez-Serrano JJ (2000) Lipid hydroperoxide levels in plant tissues. J Exp Bot 51(349):1363–1370. doi:10.1093/jexbot/51.349.1363

    Article  PubMed  CAS  Google Scholar 

  • Gross A, Kapp D, Nielsen T, Niehaus K (2005) Endocytosis of Xanthomonas campestris pathovar campestris lipopolysaccharides in non-host plant cells of Nicotiana tabacum. New Phytol 165(1):215–226. doi:10.1111/j.1469-8137.2004.01245.x

    Article  PubMed  CAS  Google Scholar 

  • Hamberg M (2011) Stereochemistry of hydrogen removal during oxygenation of linoleic acid by singlet oxygen and synthesis of 11(< i > s </i >)-deuterium-labeled linoleic acid. Lipids 46(2):201–206. doi:10.1007/s11745-010-3510-4

    Article  PubMed  CAS  Google Scholar 

  • Hamberg M, Sanz A, Rodriguez MJ, Calvo AP, Castresana C (2003) Activation of the fatty acid α-dioxygenase pathway during bacterial infection of tobacco leaves. J Biol Chem 278(51):51796–51805. doi:10.1074/jbc.M310514200

    Article  PubMed  CAS  Google Scholar 

  • Ingle RA, Carstens M, Denby KJ (2006) PAMP recognition and the plant-pathogen arms race. BioEssays 28(9):880–889. doi:10.1002/bies.20457

    Article  PubMed  CAS  Google Scholar 

  • Kallenbach M, Alagna F, Baldwin IT, Bonaventure G (2010) Nicotiana attenuata SIPK, WIPK, NPR1, and fatty acid-amino acid conjugates participate in the induction of jasmonic acid biosynthesis by affecting early enzymatic steps in the pathway. Plant Physiol 152(1):96–106. doi:10.1104/pp.109.149013

    Article  PubMed  CAS  Google Scholar 

  • Kanzaki H, Saitoh H, Takahashi Y, Berberich T, Ito A, Kamoun S, Terauchi R (2008) NbLRK1, a lectin-like receptor kinase protein of Nicotiana benthamiana, interacts with Phytophthora infestans INF1 elicitin and mediates INF1-induced cell death. Planta 228(6):977–987. doi:10.1007/s00425-008-0797-y

    Article  PubMed  CAS  Google Scholar 

  • Kato T, Yamaguchi Y, Abe N, Uyehara T, Namai T, Kodama M, Shiobara Y (1985) Structure and synthesis of unsaturated trihydroxy C-18 fatty-acids in rice plant suffering from rice blast disease. Tetrahedron Let. 26:2357–2360

    Article  CAS  Google Scholar 

  • Kenton P, Mur LAJ, Atzorn R, Wasternack C, Draper J (1999) (−)-Jasmonic acid accumulation in tobacco hypersensitive response lesions. Mol Plant Microbe Interact 12(1):74–78. doi:10.1094/mpmi.1999.12.1.74

    Article  CAS  Google Scholar 

  • Kim Y-T, Oh J, Kim K-H, Uhm J-Y, Lee B-M (2010) Isolation and characterization of NgRLK1, a receptor-like kinase of Nicotiana glutinosa that interacts with the elicitin of Phytophthora capsici. Mol Biol Rep 37(2):717–727. doi:10.1007/s11033-009-9570-y

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2008) Direct fungicidal activities of C6-aldehydes are important constituents for defense responses in Arabidopsis against Botrytis cinerea. Phytochemistry 69(11):2127–2132

    Article  PubMed  CAS  Google Scholar 

  • Kolomiets MV, Chen H, Gladon RJ, Braun EJ, Hannapel DJ (2000) A leaf lipoxygenase of potato induced specifically by pathogen Infection. Plant Physiol 124(3):1121–1130. doi:10.1104/pp.124.3.1121

    Article  PubMed  CAS  Google Scholar 

  • Kröner A, Hamelin G, Andrivon D, Val F (2011) Quantitative resistance of potato to Pectobacterium atrosepticum and Phytophthora infestans: integrating PAMP-triggered response and pathogen growth. PLoS ONE 6(8):e23331

    Article  PubMed  Google Scholar 

  • Le Quéré V, Plée-Gautier E, Potin P, Madec S, Salaün J-P (2004) Human CYP4F3s are the main catalysts in the oxidation of fatty acid epoxides. J Lipid Res 45(8):1446–1458. doi:10.1194/jlr.M300463-JLR200

    Article  PubMed  Google Scholar 

  • Liavonchanka A, Feussner I (2006) Lipoxygenases: occurrence, functions and catalysis. J Plant Physiol 163(3):348–357. doi:DOI:10.1016/j.jplph.2005.11.006

    Article  PubMed  CAS  Google Scholar 

  • López MA, Vicente J, Kulasekaran S, Vellosillo T, Martínez M, Irigoyen ML, Cascón T, Bannenberg G, Hamberg M, Castresana C (2011) Antagonistic role of 9-lipoxygenase-derived oxylipins and ethylene in the control of oxidative stress, lipid peroxidation and plant defence. Plant J 67(3):447–458. doi:10.1111/j.1365-313X.2011.04608.x

    Article  PubMed  Google Scholar 

  • Mène-Saffrané L, Esquerre-Tugaye M-T, Fournier J (2003) Constitutive expression of an inducible lipoxygenase in transgenic tobacco decreases susceptibility to Phytophthora parasitica var. nicotianae. Mol Breed 12:271–282. doi:10.1023/B:MOLB.0000006754.19398.d4

    Article  Google Scholar 

  • Montillet J-L, Agnel J-P, Ponchet M, Vailleau F, Roby D, Triantaphylidès C (2002) Lipoxygenase-mediated production of fatty acid hydroperoxides is a specific signature of the hypersensitive reaction in plants. Plant Physiol Biochem 40(6–8):633–639

    Article  CAS  Google Scholar 

  • Mosblech A, Feussner I, Heilmann I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Physiol Biochem 47(6):511–517. doi:DOI:10.1016/j.plaphy.2008.12.011

    Article  PubMed  CAS  Google Scholar 

  • Pinot F, Salaün J-P, Bosch H, Lesot A, Mioskowski C, Durst F (1992) ω-Hydroxylation of Z9-octadecenoic, Z9,10-epoxystearic and 9,10-dihydroxystearic acids by microsomal cytochrome P450 systems from Vicia sativa. Biochem Biophys Res Commun 184(1):183–193

    Article  PubMed  CAS  Google Scholar 

  • Plešková V, Kašparovský T, Obořil M, Ptáčková N, Chaloupková R, Ladislav D, Damborský J, Lochman J (2011) Elicitin-membrane interaction is driven by a positive charge on the protein surface: role of Lys13 residue in lipids loading and resistance induction. Plant Physiol Biochem 49(3):321–328

    Article  PubMed  Google Scholar 

  • Poltorak A, He XL, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282(5396):2085–2088. doi:10.1126/science.282.5396.2085

    Article  PubMed  CAS  Google Scholar 

  • Ponchet M, Panabières F, Milat ML, Mikes V, Montillet JL, Suty L, Triantaphylides C, Tirilly Y, Blein JP (1999) Are elicitins cryptograms in plant-oomycete communications? Cell Mol Life Sci 56(11):1020–1047. doi:10.1007/s000180050491

    Article  PubMed  CAS  Google Scholar 

  • Prost I, Dhondt S, Rothe G, Vicente J, Rodriguez MJ, Kift N, Carbonne F, Griffiths G, Esquerre-Tugaye M-T, 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(4):1902–1913. doi:10.1104/pp.105.066274

    Article  PubMed  CAS  Google Scholar 

  • Rickauer M, Brodschelm W, Bottin A, Véronési C, Grimal H, Esquerré-Tugayé MT (1997) The jasmonate pathway is involved differentially in the regulation of different defence responses in tobacco cells. Planta 202(2):155–162. doi:10.1007/s004250050114

    Article  CAS  Google Scholar 

  • Roy S, Pouénat M-L, Caumont C, Cariven C, Prévost M-C, Esquerré-Tugayé M-T (1995) Phospholipase activity and phospholipid patterns in tobacco cells treated with fungal elicitor. Plant Sci 107(1):17–25

    Article  CAS  Google Scholar 

  • Rustérucci C, Montillet J-L, Agnel J-P, Battesti C, Alonso B, Knoll A, Bessoule J–J, Etienne P, Suty L, Blein J-P, Triantaphylidès C (1999) Involvement of lipoxygenase-dependent production of fatty acid hydroperoxides in the development of the hypersensitive cell death induced by cryptogein on tobacco leaves. J Biol Chem 274(51):36446–36455. doi:10.1074/jbc.274.51.36446

    Article  PubMed  Google Scholar 

  • Ryu SB, Wang X (1998) Increase in free linolenic and linoleic acids associated with phospholipase D-mediated hydrolysis of phospholipids in wounded castor bean leaves. Biochim Biophys Acta 1393(1):193–202

    Article  PubMed  CAS  Google Scholar 

  • Schaller F (2001) Enzymes of the biosynthesis of octadecanoid-derived signalling molecules. J Exp Bot 52(354):11–23. doi:10.1093/jexbot/52.354.11

    Article  PubMed  CAS  Google Scholar 

  • Schaloske RH, Dennis EA (2006) The phospholipase A2 superfamily and its group numbering system. Biochim Biophys Acta 1761(11):1246–1259

    Article  PubMed  CAS  Google Scholar 

  • Stumpe M, Kandzia R, Göbel C, Rosahl S, Feussner I (2001) A pathogen-inducible divinyl ether synthase (CYP74D) from elicitor-treated potato suspension cells. FEBS Lett 507(3):371–376. doi:Doi:10.1016/s0014-5793(01)03019-8

    Article  PubMed  CAS  Google Scholar 

  • Val F, Desender S, Bernard K, Potin P, Hamelin G, Andrivon D (2008) A culture filtrate of Phytophthora infestans primes defense reaction in potato cell suspensions. Phytopathology 98(6):653–658. doi:10.1094/PHYTO-98-6-0653

    Article  PubMed  CAS  Google Scholar 

  • Vellosillo T, Martínez M, López MA, Vicente J, Cascón T, Dolan L, Hamberg M, Castresana C (2007) Oxylipins produced by the 9-lipoxygenase pathway in arabidopsis regulate lateral root development and defense responses through a specific signaling cascade. Plant Cell Online 19(3):831–846. doi:10.1105/tpc.106.046052

    Article  CAS  Google Scholar 

  • Weber H (2002) Fatty acid-derived signals in plants. Trends Plant Sci 7(5):217–224

    Article  PubMed  CAS  Google Scholar 

  • Weber H, Chetelat A, Caldelari D, Farmer EE (1999) Divinyl ether fatty acid synthesis in late blight—diseased potato leaves. Plant Cell 11(3):485–494. doi:10.1105/tpc.11.3.485

    PubMed  CAS  Google Scholar 

  • Westphal O, Jann K (1965) Bacterial lipopolysaccharides: extraction with phenol-water and further application of the procedure. Methods Carbohydr Chem 5:83–91

    CAS  Google Scholar 

  • Yaeno T, Matsuda O, Iba K (2004) Role of chloroplast trienoic fatty acids in plant disease defense responses. Plant J 40(6):931–941. doi:10.1111/j.1365-313X.2004.02260.x

    Article  PubMed  CAS  Google Scholar 

  • Zien CA, Wang C, Wang X, Welti R (2001) In vivo substrates and the contribution of the common phospholipase D, PLDα, to wound-induced metabolism of lipids in Arabidopsis. Biochim Biophys Acta 1530(2–3):236–248

    PubMed  CAS  Google Scholar 

  • Zucker M (1968) Sequential induction of phenylalanine ammonia-lyase and a lyase-inactivating system in potato tuber disks. Plant Physiol 43(3):365–374. doi:10.1104/pp.43.3.365

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded through funds from the “Région Bretagne” PRIR Program, France.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Florence Val.

Additional information

Communicated by M. Petersen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saubeau, G., Goulitquer, S., Barloy, D. et al. Differential induction of oxylipin pathway in potato and tobacco cells by bacterial and oomycete elicitors. Plant Cell Rep 32, 579–589 (2013). https://doi.org/10.1007/s00299-012-1377-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-012-1377-y

Keywords

Navigation