Skip to main content
SpringerLink
Log in

A novel patatin-like protein from cotton plant, GhPat1, is co-expressed with GhLox1 during Xanthomonas campestris-mediated hypersensitive cell death

  • Biotic and Abiotic Stress
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

In cotton plant, Xanthomonas-induced hypersensitive response (HR) is accompanied by a lipid peroxidation process involving a 9-lipoxygenase (LOX), GhLox1. Initiation of this oxidative metabolism implies the release of the LOX substrates, or polyunsaturated fatty acids. Since patatin-like proteins (PLPs) are likely candidates for mediating the latter step, we searched for genes encoding such enzymes, identified and cloned one of them that we named GhPat1. Biochemical and molecular studies showed that GhPat1 expression was up-regulated during the incompatible interaction, prior to the onset of the corresponding galactolipase activity and cell death symptoms in tissues. Protein sequence analysis and modelling also revealed that GhPat1 catalytic amino acids and fold were conserved across plant PLPs. Based on these results and our previous work (Jalloul et al. in Plant J 32:1–12, 2002), a role for GhPat1, in synergy with GhLox1, during HR-specific lipid peroxidation is discussed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

CE:

Cotton patatin-like EST

DAD1:

Defective in anther dehiscence 1

DGL:

DONGLE

FAH:

Fatty acid hydroperoxide

HR:

Hypersensitive response

LAH:

Lipid acyl-hydrolase

LOX:

Lipoxygenase

PCD:

Programmed cell death

PLA2 :

Phospholipase A2

PLP:

Patatin-like protein

PUFA:

Polyunsaturated fatty acid

TMV:

Tobacco mosaic virus

Xcm :

Xanthomonas campestris pv. malvacearum

References

  • Alméras E, Stolz S, Vollenweider S, Reymond P, Mène-Saffrané L, Farmer EE (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. Plant J 34:205–216

    Article  PubMed  Google Scholar 

  • Ameisen JC (2002) On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ 9:367–393

    Article  PubMed  CAS  Google Scholar 

  • Andersson MX, Hamberg M, Kourtchenko O, Brunnström A, McPhail KL, Gerwick WH, Göbel C, Feussner I, Ellerström M (2006) Oxylipin profiling of the hypersensitive response in Arabidopsis thaliana. Formation of a novel oxo-phytodienoic acid-containing galactolipid, arabidopside E. J Biol Chem 281:31528–31537

    Article  PubMed  CAS  Google Scholar 

  • Andrews DL, Beames B, Summers MD, Park WD (1988) Characterization of the lipid acyl hydrolase activity of the major potato (Solanum tuberosum) tuber protein, patatin, by cloning and abundant expression in a baculovirus vector. Biochem J 252:199–206

    PubMed  CAS  Google Scholar 

  • Banerji S, Flieger A (2004) Patatin-like proteins: a new family of lipolytic enzymes present in bacteria? Microbiology 150:522–525

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Cacas JL, Vailleau F, Davoine C, Ennar N, Agnel JP, Tronchet M, Ponchet M, Blein JP, Roby D, Triantaphylidès 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

    Article  CAS  Google Scholar 

  • Corre F, Henry Y, Rode A, Hartmann C (1996) Em gene expression during somatic embryogenesis in the monocot Triticum aestivum L. Plant Sci 117:139–149

    Article  CAS  Google Scholar 

  • Davoine C, Douki T, Iacazio G, Montillet JL, Triantaphylidès C (2005) Conjugation of keto fatty acids to glutathione in plant tissues. Characterization and quantification by HPLC-tandem mass spectrometry. Anal Chem 77:7366–7372

    Article  PubMed  CAS  Google Scholar 

  • Delannoy E, Jalloul A, Assigbetsé K, Marmey P, Geiger JP, Lherminier J, Daniel JF, Martinez C, Nicole M (2003) Activity of class III peroxidases in the defense of cotton to bacterial blight. Mol Plant Microbe Interact 16:1030–1038

    Article  PubMed  CAS  Google Scholar 

  • Dessen A, Tang J, Schmidt H, Stahl M, Clark JD, Seehra J, Somers WS (1999) Crystal structure of human cytosolic phospholipase A2 reveals a novel topology and catalytic mechanism. Cell 97:349–360

    Article  PubMed  CAS  Google Scholar 

  • Dhondt S, Geoffroy P, Stelmach BA, Legrand M, Heitz T (2000) Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes. Plant J 23:431–440

    Article  PubMed  CAS  Google Scholar 

  • Diamond M, McCabe PF (2007) The role of mitochondria in plant programmed cell death. In: Logan DC (ed) Plant mitochondria (annual plant reviews series), vol 31. Blackwell Publishing, Oxford, pp 308–335

    Google Scholar 

  • Drews GN, Beals TP, Bui AQ, Goldberg RB (1992) Regional and cell-specific gene expression patterns during petal development. Plant Cell 4:1383–1404

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984

    Article  PubMed  CAS  Google Scholar 

  • Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Hamberg M, Sanz A, Rodriguez MJ, Calvo AP, Castresana C (2003) Activation of the fatty acid α-dioxygenases pathway during bacterial infection of tobacco leaves. Formation of oxylipins protecting against cell death. J Biol Chem 278:51796–51805

    Article  PubMed  CAS  Google Scholar 

  • Heitz T, La Camera S, Gouzerh G, Dhondt S, Geoffroy P, Legrand M (2004) Pathogen-induced lipid acyl hydrolases and oxylipin metabolism. In: The international joint workshop on PR-proteins and induced resistance, Hotel Marienlyst, Elsinore, Denmark, 5–9 May 2004

  • Hillocks RJ (1992) Cotton diseases. CAB International, Wallingford, pp 39–85

    Google Scholar 

  • Hirschberg HJ, Simons JFA, Dekker N, Egmond MR (2001) Cloning, expression, purification and characterization of patatin, a novel phospholipase A. Eur J Biochem 268:5037–5044

    Article  PubMed  CAS  Google Scholar 

  • Holk A, Rietz S, Zahn M, Quader H, Scherer GF (2002) Molecular identification of cytosolic, patatin-related phospholipases A from Arabidopsis thaliana with potential functions in plant signal transduction. Plant Physiol 130:90–101

    Article  PubMed  CAS  Google Scholar 

  • Hyun Y, Choi S, Hwang HJ, Yu J, Nam SJ, Ko J, Park JY, Seo YS, Kim EY, Ryu SB, Kim WT, Lee YH, Kang H, Lee I (2008) Cooperation and functional diversification of two closely related galactolipase genes for jasmonate biosynthesis. Dev Cell 14:183–192

    Article  PubMed  CAS  Google Scholar 

  • Innes N (1983) Bacterial blight of cotton. Biol Rev 58:157–176

    Article  Google Scholar 

  • Ishiguro S, Kawai-Oda A, Uedo J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalysing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2200

    Article  PubMed  CAS  Google Scholar 

  • Jalloul A, Montillet JL, Assigbetsé K, Agnel JP, Delannoy E, Triantaphylidès C, Daniel JF, Marmey P, Geiger J-P, Nicole M (2002) Lipid peroxidation in cotton: Xanthomonas interactions and the role of lipoxygenases during the hypersensitive reaction. Plant J 32:1–12

    Article  PubMed  CAS  Google Scholar 

  • Knight VI, Wang H, Lincoln JE, Lulai EC, Gilchrist DG, Bostock RM (2001) Hydroperoxides of fatty acids induce programmed cell death in tomato protoplasts. Physiol Mol Plant Pathol 59:277–286

    Article  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 124:1121–1130

    Article  PubMed  CAS  Google Scholar 

  • La Camera S, Geoffroy P, Samaha H, Ndiaye A, Rahim G, Legrand M, Heitz T (2005) A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis. Plant J 44:810–825

    Article  PubMed  CAS  Google Scholar 

  • Lewis K (2000) Programmed death in bacteria. Microbiol Mol Biol 64:503–514

    Article  CAS  Google Scholar 

  • Marmey P, Jalloul A, Alhamdia M, Assigbetse K, Cacas JL, Voloudakis AE, Champion A, Clerivet A, Montillet JL, Nicole M (2007) The 9-lipoxygenase GhLOX1 gene is associated with the hypersensitive reaction of cotton Gossypium hirsutum to Xanthomonas campestris pv malvacearum. Plant Physiol Biochem 45:596–606

    Article  PubMed  CAS  Google Scholar 

  • Matos AR, D’Arcy-Lameta A, Franca M, Petres S, Edelman L, Kader J-C, Zuily-Fodil Y, Pham Thi AT (2001) A novel patatin-like gene stimulated by drought stress encodes a galactolipid acyl hydrolase. FEBS Lett 491:188–192

    Article  PubMed  CAS  Google Scholar 

  • Matos AR, Gigon A, Laffray D, Pêtres S, Zuily-Fodil Y, Pham-Thi AT (2008) Effects of progressive drought stress on the expression of patatin-like lipid acyl hydrolase genes in Arabidopsis leaves. Physiol Plant 134:110–120

    Article  PubMed  CAS  Google Scholar 

  • Melan MA, Dong X, Endara ME, Davis KR, Ausubel FM, Peterman TK (1993) An Arabidopsis thaliana lipoxygenase gene can be induced by pathogens, abscisic acid, and methyl jasmonate. Plant Physiol 101:441–450

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Montillet JL, Cacas JL, Garnier L, Montané MH, Douki T, Bessoule JJ, Polkowska-Kowalczyk L, Maciejewska U, Agnel JP, Vial A, Triantaphylidès C (2004) The upstream oxylipin profile of Arabidopsis thaliana: a tool to scan for oxidative stresses. Plant J 40:439–451

    Article  PubMed  CAS  Google Scholar 

  • Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59:501–520

    Article  PubMed  CAS  Google Scholar 

  • Nakai K, Kanehisa M (1992) A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14:897–911

    Article  PubMed  CAS  Google Scholar 

  • Narusaka Y, Narusaka M, Seki M, Fujita M, Ishida J, Nakashima M, Enju A, Sakurai T, Satou M, Kamiya A, Park P, Kobayashi M, Shinozaki K (2003) Expression profiles of Arabidopsis thaliana phospholipase A IIA gene in response to biotic and abiotic stresses. Plant Cell Physiol 44:1246–1252

    Article  PubMed  CAS  Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computer. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Prost I, Dhondt S, Rothe G, Vicente J, Rodriguez MJ, Kift N, Carbonne 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

    Article  PubMed  CAS  Google Scholar 

  • Rietz S, Holk A, Scherer GFE (2004) Expression of the patatin-related phospholipase A gene AtPLA IIA in Arabidopsis thaliana is up-regulated by salicylic acid, wounding, ethylene, and iron and phosphate deficiency. Planta 219:743–753

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rydel TJ, Williams JM, Krieger E, Moshiri F, Stallings WC, Brown SM, Pershing JC, Purcell JP, Alibhai MF (2003) The crystal structure, mutagenesis, and activity studies reveal that patatin is a lipid acyl hydrolase with a Ser-Asp catalytic dyad. Biochemistry 42:6696–6708

    Article  PubMed  CAS  Google Scholar 

  • Santos MA (1991) An improved method for the small scale preparation of bacteriophage DNA based on phage precipitation by zinc chloride. Nucleic Acids Res 19:5442

    Article  PubMed  CAS  Google Scholar 

  • Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modelling server. Nucleic Acids Res 31:3381–3385

    Article  PubMed  CAS  Google Scholar 

  • Strickland J, Gregory LO, Walsh TA (1995) Inhibition of Diabrotica larval growth by patatin, the lipid acyl hydrolase from potato tubers. Plant Physiol 109:667–674

    PubMed  CAS  Google Scholar 

  • Véronesi C, Rickauer M, Fournier J, Pouénat ML, Esquerré-Tugayé MT (1996) Lipoxygenase gene expression in the tobacco-Phytophthora parasitica pv nicotianae interaction. Plant Physiol 112:997–1004

    Article  PubMed  Google Scholar 

  • Vollenweider S, Weber H, Stolz S, Chételat A, Farmer EE (2000) Fatty acid ketodienes and fatty acid ketotrienes: Michael addition acceptors that accumulate in wounded and diseased Arabidopsis leaves. Plant J 24:467–476

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We wish to warmly thank E. Delannoy for his help and stimulating discussions. We also thank J. Aribi for technical assistance in the greenhouse work.

Author information

Authors and Affiliations

  1. UMR RPB (Résistance des Plantes aux Bioagresseurs), IRD, B.P. 64501, 34394, Montpellier Cedex 5, France

    Jean-Luc Cacas, Philippe Marmey, Majd Sayegh-Alhamdia & Michel Nicole

  2. DSV-DEVM, Laboratoire des Echanges Membranaires & Signalisation, Cadarache, CEA, 13108, Saint-Paul-Lez Durance Cedex, France

    Jean-Luc Montillet

  3. Department of Plant Protection, Faculty of Agronomy, University of Damascus, Damascus, Syria

    Aida Jalloul

  4. Structural Bioinformatics Group, Centro Nacional de Investigaciones Oncologicas, C/Melchor Fernandez Almagro, 3, 28029, Madrid, Spain

    Ana Rojas-Mendoza

  5. UMR RBP, Université Montpellier II, 34095, Montpellier Cedex 5, France

    Alain Clérivet

Authors
  1. Jean-Luc Cacas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philippe Marmey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean-Luc Montillet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Majd Sayegh-Alhamdia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aida Jalloul
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ana Rojas-Mendoza
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alain Clérivet
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michel Nicole
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean-Luc Cacas.

Additional information

Communicated by Leandro Peña.

Jean-Luc Cacas and Philippe Marmey have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cacas, JL., Marmey, P., Montillet, JL. et al. A novel patatin-like protein from cotton plant, GhPat1, is co-expressed with GhLox1 during Xanthomonas campestris-mediated hypersensitive cell death. Plant Cell Rep 28, 155–164 (2009). https://doi.org/10.1007/s00299-008-0622-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-008-0622-x

Keywords

Search

Navigation