Advertisement

Planta

, Volume 227, Issue 2, pp 363–373 | Cite as

Wounding and pathogen infection induce a chloroplast-targeted lipoxygenase in the common bean (Phaseolus vulgaris L.)

  • Helena Porta
  • Rosa Elia Figueroa-Balderas
  • Mario Rocha-Sosa
Original Article

Abstract

Chloroplastic LOXs are implicated in the biosynthesis of oxylipins like jasmonic acid and C6 volatiles among others. In this study, we isolated the cDNA of a novel chloroplast-targeted Phaseolus vulgaris LOX, (PvLOX6). This gene is highly induced after wounding, non-host pathogen infection, and by signaling molecules as H2O2, SA, ethylene and MeJA. The phylogenetic analysis of PvLOX6 showed that it is closely related to chloroplast-targeted LOX from potato (H1) and tomato (TomLOXC); both of them are implicated in the biosynthesis of C6 volatiles. Induction of PvLOX6 mRNA by wounding ethylene and jasmonic acid on the one side, and non-host pathogen, salicylic acid on the other indicates that common bean uses the same LOX to synthesize oxylipins in response to different stresses.

Keywords

Lipoxygenase Phaseolus Ethylene H2O2 Pathogen Wounding 

Abbreviations

AOS

Allene oxide synthase

HPL

Hydroperoxide lyase

JA

Jasmonic acid

LOX

Lipoxygenase

MeJA

Methyl jasmonate

PvLOX6

Phaseolus vulgaris lipoxygenase 6

OPDA

12-oxo-phytodienoic acid

SA

Salicylic acid

Notes

Acknowledgments

We thank Patricia Rueda for the technical support, Eugenio López-Bustos and Paul Gaytán for the oligonucleotide synthesis, Jorge Yanez for the sequencing, Andrés Saralegui for the confocal images, and José J. Sánchez Serrano from CNB, Madrid, Spain, for providing us with the potato H1 antibodies. We also thank Gladys Cassab and Miguel Angel Cevallos for their helpful comments on the manuscript. The Dirección General de Asuntos Para el Personal Académico-UNAM (IN212103) funded for this work.

References

  1. 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 383:1645–1657PubMedCrossRefGoogle Scholar
  2. Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc Natl Acad Sci USA 92:8675–8679PubMedCrossRefGoogle Scholar
  3. Bergey DR, Howe GA, Ryan CA (1996) Polypeptide signalling for plant defensive genes exhibits analogies to defence signalling in animals. Proc Natl Acad Sci USA 93:12053–12058PubMedCrossRefGoogle Scholar
  4. 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: 679–685PubMedGoogle Scholar
  5. Bouquin T, Lasserre E, Pradier J, Pech JC, Balague C (1997) Wound and ethylene induction of the ACC oxidase melon gene CM-ACO1 occurs via two direct and independent transduction pathways. Plant Mol Biol 35:1029–1035PubMedCrossRefGoogle Scholar
  6. Cavallo V, Raggi V (2002) Jasmonic acid accumulation in bean hypersensitively resistant to Uromices phaseoli. J Plant Plathol 84:77–82Google Scholar
  7. Chen G, Hackett R, Walker D, Taylor A, Lin Z, Grierson D (2004) Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant Physiol 136:2641–2651PubMedCrossRefGoogle Scholar
  8. Croft K, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol 101:13–24PubMedGoogle Scholar
  9. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  10. Eiben HG, Slusarenko AJ (1994) Complex spatial and temporal expression of lipoxygenase genes during Phaseolus vulgaris (L.) development. Plant J 5:123–135PubMedCrossRefGoogle Scholar
  11. Farmaki T, Sanmartin M, Jimenez P, Paneque M, Sanz C, Vancanneyt G, Leon J, Sanchez-Serrano JJ (2007) Differential distribution of the lipoxygenase pathway enzymes within potato chloroplasts. J Exp Bot 58:555–568PubMedCrossRefGoogle Scholar
  12. Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297PubMedCrossRefGoogle Scholar
  13. Garcia-Ponce B, Rocha-Sosa M (2000) The octadecanoid pathway is required for pathogen-induced multi-functional acetyl-CoA carboxylase accumulation in common bean (Phaseolus vulgaris L.). Plant Sci 157:181–190PubMedCrossRefGoogle Scholar
  14. Griffiths A, Barry C, Alpuche-Solis A, Grierson D (1999) Ethylene and developmental signals regulate expression of lipoxygenase genes during tomato fruit ripening. J Exp Bot 50:793–798CrossRefGoogle Scholar
  15. Halitschke R, Baldwin IT (2003) Antisense LOX expression increases herbivore performance by decreasing defense response and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J 36:794–807PubMedCrossRefGoogle Scholar
  16. 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 114:1085–1093PubMedCrossRefGoogle Scholar
  17. Iuchi S, Yamaguchi-Shinozaki K, Urao T, Terao T, Shinozaki K (1996) Novel drought-inducible genes in the highly drought-tolerant cowpea: cloning of cDNAs and analysis of the expression of the corresponding genes. Plant Cell Physiol 37:1073–1082PubMedGoogle Scholar
  18. Keegstra K (1989) Transport and routing of proteins into chloroplasts. Cell 56:247–253PubMedCrossRefGoogle Scholar
  19. Leon J, Royo J, Sanchez-Serrano JJ (2001) Wound signaling in plants. J Exp Bot 52:1–9PubMedCrossRefGoogle Scholar
  20. Leon J, Royo J, Vancanneyt G, Sanz C, Silkowski H, Griffiths G, Sanchez-Serrano JJ (2002) Lipoxygenase H1 gene silencing reveals a specific role in supplying fatty acid hydroperoxides for aliphatic aldehyde production. J Biol Chem 277:416–423PubMedCrossRefGoogle Scholar
  21. Liu D, A Li N, A Dube S, A Kalinski A, A Herman E, A Mattoo AK (1993) Molecular characterization of a rapidly and transiently wound-induced soybean (Glycine max L.) gene encoding 1-aminocyclopropane-1-carboxylate synthase. Plant Cell Physiol 4:1151–1157Google Scholar
  22. Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163:16–20PubMedCrossRefGoogle Scholar
  23. Meier BM, Shaw N, Slusarenko AJ (1993) Spatial and temporal accumulation of defense gene transcripts in bean (Phaseolus vulgaris) leaves in relation to bacteria-induced hypersensitive cell death. Mol Plant Microbe Interact 6:453–466PubMedGoogle Scholar
  24. 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 140:249–262PubMedCrossRefGoogle Scholar
  25. 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 57:3767–3779PubMedCrossRefGoogle Scholar
  26. 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 non-pathogenic Pseudomonas strain. Mol Plant Microbe Interact 17:1009–1018PubMedCrossRefGoogle Scholar
  27. Orozco-Cardenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96:6553–6557PubMedCrossRefGoogle Scholar
  28. Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  29. Peña-Cortes H, Albrecht T, Prat S, Weiler E, Willmitzer L (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128CrossRefGoogle Scholar
  30. Peng YL, Shirano Y, Ohta H, Hibino T, Tanaka K, Shibata D (1994) A novel lipoxygenase from rice. Primary structure and specific expression upon incompatible infection with rice blast fungus. J Biol Chem 269:3755–3761PubMedGoogle Scholar
  31. Porta H, Rocha-Sosa M (2000) A Phaseolus vulgaris lipoxygenase gene expressed in nodules and in Rhizobium tropici inoculated roots. Biochim Biophys Acta 1517:139–142PubMedGoogle Scholar
  32. Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiol 130:15–21PubMedCrossRefGoogle Scholar
  33. Porta H, Rueda-Benitez P, Campos F, Colmenero-Flores JM, Colorado JM, Carmona MJ, Covarrubias AA, Rocha-Sosa M (1999) Analysis of lipoxygenase mRNA accumulation in the common bean (Phaseolus vulgaris L.) during development and under stress conditions. Plant Cell Physiol 40:850–858PubMedGoogle Scholar
  34. Ramirez M, Graham MA, Blanco-Lopez L, Silvente S, Medrano-Soto A, Blair MW, Hernandez G, Vance CP, Lara M (2005) Sequencing and analysis of common bean ESTs. Building a foundation for functional genomics. Plant Physiol 137:1211–1227PubMedCrossRefGoogle Scholar
  35. Royo J, Vancanneyt G, Perez AG, Sanz C, Stormann K, Rosahl S, Sanchez-Serrano JJ (1996) Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. J Biol Chem 271:21012–21019PubMedCrossRefGoogle Scholar
  36. Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018PubMedCrossRefGoogle Scholar
  37. Salzman RA, Brady JA, Finlayson SA, Buchanan CD, Summer EJ, Sun F, Klein PE, Klein RR, Pratt LH, Cordonnier-Pratt MM, Mullet JE (2005) Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiol 138:352–368PubMedCrossRefGoogle Scholar
  38. Schaffrath U, Zabbai F, Dudler R (2000) Characterization of RCI-1, a chloroplastic rice lipoxygenase whose synthesis is induced by chemical plant resistance activators. Eur J Biochem 267:5935–5942PubMedCrossRefGoogle Scholar
  39. Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365PubMedCrossRefGoogle Scholar
  40. Tadeusz W, Tomczak A, Michelmore R (2005) Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnol J 3:259–273CrossRefGoogle Scholar
  41. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  42. Voros 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 251:36–44PubMedCrossRefGoogle Scholar
  43. Yang Y, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes Dev 11:1621–1639PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Helena Porta
    • 1
  • Rosa Elia Figueroa-Balderas
    • 1
  • Mario Rocha-Sosa
    • 1
  1. 1.Departmento de Biología Molecular de PlantasInstituto de Biotecnología, Universidad Nacional Autónoma de MéxicoCuernavacaMexico

Personalised recommendations