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Journal of Chemical Ecology

, Volume 31, Issue 9, pp 1953–1967 | Cite as

Effects of Jasmonate-Induced Defenses on Root-Knot Nematode Infection of Resistant and Susceptible Tomato Cultivars

  • W. R. Cooper
  • L. Jia
  • L. Goggin
Article

Abstract

Jasmonates, such as jasmonic acid (JA), are plant-signaling compounds that trigger induced resistance against certain pathogens and a broad range of arthropod herbivores. One goal of this study was to determine the effects of JA-dependent defenses in tomato on root-knot nematodes. Another was to determine if the artificial induction of these defenses could enhance nematode control on plants that carry Mi-1.2, a nematode resistance gene that is present in many tomato cultivars. At moderate soil temperatures, Mi-1.2 can effectively suppress reproduction of most isolates of the common root-knot nematode species Meloidogyne javanica, M. incognita, and M. arenaria. Mi-mediated resistance has its limitations, however. Mi-1.2 is reported to lose its effectiveness at soil temperatures above 28°C, and certain virulent nematode isolates can overcome resistance even at moderate soil temperatures. This study used a foliar application of JA to activate induced resistance in two near-isogenic lines of tomato (Lycopersicon esculentum) with and without Mi-1.2, and evaluated the effects of induced resistance at moderate soil temperatures on one avirulent nematode isolate (M. javanica isolate VW4) and two virulent isolates (M. javanica isolate VW5 and M. incognita isolate 557R). In addition, the effects of induced resistance on avirulent nematode performance were examined at a high temperature (32°C). The results indicate that JA application induces a systemic defense response that reduces avirulent nematode reproduction on susceptible tomato plants. Furthermore, JA-dependent defenses proved to be heat-stable, whereas the effects of Mi-mediated resistance were reduced but not eliminated at 32°C. JA treatment enhanced Mi-mediated resistance at high temperature, but did not suppress either of the virulent nematode isolates tested.

Key Words

Induced resistance octadecanoid pathway jasmonic acid Mi temperature-sensitive resistance nematode resistance Meloidogyne virulence avirulence 

Notes

Acknowledgments

We are grateful to Dr. Valerie Williamson, Waclawa Pudlo, and Dr. Cynthia Gleason for providing nematode isolates for this project. We thank Fangyan Chen and John Geurber for their assistance with greenhouse maintenance, and Dr. Ron McNew and Dr. Andronikos Mauromoustakos for assistance with statistical analysis. We also appreciate the feedback of Dr. Robert Riggs and two anonymous reviewers on this manuscript. This research was funded by the Arkansas Agricultural Experiment Station and the California Tomato Commission, as well as by USDA Southern Agricultural Research and Education program (SARE) grant no. GS03-027.

References

  1. Araujo, M. T., Bassett, M. J., Augustine, J. J., Dickson, D. W. 1982Effect of diurnal changes in soil temperatures on resistance to Meloidogyne incognita in tomatoJ. Nematol.14414416Google Scholar
  2. Atkinson, H. J., Urwin, P. E., Clarke, M. C., McPherson, M. J. 1996Image analysis of the growth of Globodera pallida and Meloidogyne incognita on transgenic tomato roots expression cystatinsJ. Nematol.28209215Google Scholar
  3. Atkinson, H. J., Urwin, P. E., McPherson, M. J. 2003Engineering plants for nematode resistanceAnnu. Rev. Phytopathol.41615639CrossRefPubMedGoogle Scholar
  4. Bajaj, K. L., Singh, P., Mahajan, R. 1985Changes induced by Meloidogyne incognita in superoxide dismutase, peroxidase and polyphenol oxidase activity in tomato rootsBiochem. Physiol. Pflanzen180543546Google Scholar
  5. Baldwin, I. T., Schmelz, E. A., Ohnmeiss, T. E. 1994Wound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana-sylvestris Spegazzini and ComesJ. Chem. Ecol.2021392157CrossRefGoogle Scholar
  6. Botella, M. A., Xu, Y., Prabha, T. N., Zhao, Y., Narasimhan, M. L., Wilson, K. A., Nielsen, S. S., Bressan, R. A., Hasegawa, P. M. 1996Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonatePlant Physiol11212011210CrossRefPubMedGoogle Scholar
  7. Branch, C., Hwang, C. F., Navarre, D. A., Williamson, V. M. 2004Salicylic acid is part of the Mi-1-mediated defense response to root-knot nematode in tomatoMol. Plant Microb. Interact.17351356Google Scholar
  8. Brown, C. R., Mojtahedi, H., Santo, G. S., Williamson, V. M. 1997Effect of the Mi gene in tomato on reproductive factors of Meloidogyne chitwoodi and M. haplaJ. Nematol.29416419Google Scholar
  9. Bruce, T. J., Martin, J. L., Picket, J. A., Pye, B. J., Smart, L. E., Wadhams, L. J. 2003Cis-Jasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius) (Homoptera: Aphididae)Pest Manag. Sci.5910311036CrossRefPubMedGoogle Scholar
  10. Brueske, C. M. 1980Phenylalanine ammonia lyase activity in tomato roots infected and resistant to the root-knot nematode Meloidogyne incognitaPhysiol. Plant Pathol.16409414Google Scholar
  11. Castagnone-Sereno, P. 2002Genetic variability in parthenogenetic root-knot nematodes, Meloidogyne spp., and their ability to overcome plant resistance genesNematology4605608CrossRefGoogle Scholar
  12. Castagnone-Sereno, P., Bongiovanni, M., Djian-Caporalino, C. 2001New data on the specificity of the root-knot nematode resistance genes Me1 and Me3 in pepperPlant Breed.120429433CrossRefGoogle Scholar
  13. Cooper, W. R. and Goggin, F. L. 2005. Effects of jasmonate-induced defenses in tomato on the potato aphid, Macrosiphum euphorbiae. Entomol. Exp. Appl. 115:107–115.Google Scholar
  14. Cooper, W. R., Jia, L., Goggin, F. L. 2004Acquired and R-gene mediated aphid resistance in tomatoJ. Chem. Ecol.3025272542CrossRefPubMedGoogle Scholar
  15. Dammann, C., Rojo, E., Sanchez serrano, J. J. 1997Abscisic acid and jasmonic acid activate wound-inducible genes in potato through separate, organ-specific signal transduction pathwaysPlant J.11773782CrossRefPubMedGoogle Scholar
  16. Davis, E. L., Rich, J. R. 1987Nicotine content of tobacco roots and toxicity to Meloidogyne incognitaJ. Nematol.192329Google Scholar
  17. Doares, S. H., Narvaez-Vasquez, J., Conconi, A., and Ryan, C. A. 1995. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108:1741–1746.Google Scholar
  18. Dropkin, V. H. 1969The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperaturePhytopathology5916321637Google Scholar
  19. Ellis, C., Karafyllidis, L., Turner, J. G. 2002Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicaeMol. Plant Microb. Interact.1510251030Google Scholar
  20. Farmer, E., Johnson, E., Ryan, C. A. 1992Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acidPlant Physiol.989951002Google Scholar
  21. Flor, H. H. 1955Host parasite interactions in flax rust—its genetic and other implicationsPhytopathology45680685Google Scholar
  22. Gomez, K. A., Gomez, A. A. 1984Statistical Procedures for Agricultural ResearchWiley-InterscienceNew York, NYGoogle Scholar
  23. Haroon, S. A., Baki, A. A., Huettel, R. N. 1993An in vitro test for temperature sensitivity and resistance to Meloidogyne incognita in tomatoJ. Nematol.258388Google Scholar
  24. Holtzman, O. 1965Effects of soil temperature on resistance of tomato to root-knot nematode (Meloidogyne incognita)Phytopathology55990992Google Scholar
  25. Howe, G. A., Lightner, J., Browse, J., Ryan, C. A. 1996An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attackPlant Cell820672077CrossRefPubMedGoogle Scholar
  26. Hussey, R. S., Barker, K. H. 1973A comparison of methods of collecting inocula of Meloidogyne spp., including a new techniquePlant Dis. Rep.5710251028Google Scholar
  27. Karban, R., Baldwin, I. T. 1997Induced Responses to HerbivoryUniversity of Chicago PressChicago, ILGoogle Scholar
  28. Lambert, K. N., Tedford, E. C., Caswell, E. P., Williamson, V. M. 1992A system for continuous production of root-knot nematode juveniles in hydroponic culturePhytopathology82512515Google Scholar
  29. Lambert, K. N., Ferrie, B. J., Nombela, G., Brenner, E. D., Williamson, V. M. 1999Identification of genes whose transcripts accumulate rapidly in tomato after root-knot nematode infectionPhysiol. Plant Pathol.55341348CrossRefGoogle Scholar
  30. Li, C., Williams, M. M., Loh, Y.-T., Lee, G. I., Howe, G. A. 2002Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathwayPlant Physiol.130494503CrossRefPubMedGoogle Scholar
  31. Mader, J. C. 1999Effects of jasmonic acid, silver nitrate and L-AOPP on the distribution of free and conjugated polyamines in roots and shoots of Solanum tuberosum in vitroJ. Plant Physiol.1547988Google Scholar
  32. McConn, M., Creelman, R. A., Bell, E., Mullet, J. E., Browse, J. 1997Jasmonate is essential for insect defense in ArabidopsisProc. Natl. Acad. Sci. USA9454735477CrossRefPubMedGoogle Scholar
  33. Medina-Filho, H., Tanksley, S. D. 1983Breeding for nematode resistanceSharp, W. R.Evans, D. A.Ammirato, P. V.Yamada, Y. eds. Handbook of Plant Cell Culture, Vol. 1MacMillan PublishersNew York, NY904923Google Scholar
  34. Melakeberhan, H. 1998Effects of temperature and nitrogen source on tomato genotypes response to Meloidogyne incognita infectionFundam. Appl. Nematol.212532Google Scholar
  35. Milligan, S. B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P., Williamson, V. M. 1998The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine rich repeat family of plant genesPlant Cell1013071319CrossRefPubMedGoogle Scholar
  36. Noling, J. W. 2002Nematode management in commercial vegetable crops. Institute of Food and Agricultural Sciences document ENY-14, Florida Cooperative Extension ServiceUniversity of FloridaGainesville, FLGoogle Scholar
  37. Nombela, G., Williamson, V. M., Muniz, M. 2003The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaciMol. Plant–Microb. Interact.16645649Google Scholar
  38. Oka, Y., Cohen, Y. 2001Induced resistance to cyst and root-knot nematodes in cereals by DL-B-amino-n-butyric acidEur. J. Plant Pathol.107219227CrossRefGoogle Scholar
  39. Omer, A. D., Granett, J., Karban, R., Villa, E. M. 2001Chemically-induced resistance against multiple pests in cottonInt. J. Pest Manag.474954CrossRefGoogle Scholar
  40. Omer, A. D., Thaler, J. S., Granett, J., Karban, R. 2000Jasmonic acid induced resistance in grapevines to a root and leaf feederJ. Econ. Entomol.93840845PubMedGoogle Scholar
  41. Paulson, R. E., Webster, J. M. 1972Ultra structure of the hypersensitive reaction in roots of tomato, Lycopersicon esculentum L., to infection by the root-knot nematode, Meloidogyne incognitaPhysiol. Plant Pathol.2227234Google Scholar
  42. Pena-Cortes, H., Albrecht, T., Weiler, E. W., and Willlmitzer, L. 1993. Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128.Google Scholar
  43. Riggs, R. D., Winstead, N. N. 1959Studies on resistance in tomato to root-knot nematodes and on occurrence of pathogenic biotypesPhytopathology49716724Google Scholar
  44. Rossi, M., Goggin, F. L., Milligan, S. B., Kaloshian, I., Ullman, D. E., Williamson, V. M. 1998The nematode resistance gene Mi of tomato confers resistance against the potato aphidProc. Natl. Acad. Sci. USA9597509754CrossRefPubMedGoogle Scholar
  45. Ryan, C. A. 2000The systemin signaling pathway: Differential activation of plant defense genesBiochim. Biophys. Acta1477112121PubMedGoogle Scholar
  46. Soriano, I. R., Riley, I. T., Potter, M. J., Bowers, W. S. 2004aPhytoecdysteroids: A novel defense against plant-parasitic nematodesJ. Chem. Ecol.3018851899CrossRefGoogle Scholar
  47. Soriano, I. R., Asenstorfer, R. E., Schmidt, O., Riley, I. T. 2004Inducible flavone in oats(Avena sativa) is a novel defense against plant-parasitic nematodesPhytopathology9412071214Google Scholar
  48. Staswick, P. E., Yuen, G. Y., Lehman, C. C. 1998Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregularePlant J.15747754CrossRefPubMedGoogle Scholar
  49. Takken, F. L. W., Joosten, M. H. A. J. 2000Plant resistance genes: their structure, function, and evolutionEur. J. Plant Pathol.106699713CrossRefGoogle Scholar
  50. Thaler, J. S. 1999Induced resistance in agricultural crops: Effects of jasmonic acid on herbivory and yield in tomato plantsEnviron. Entomol.993037Google Scholar
  51. Thaler, J. S., Stout, M. J., Karban, R., Duffey, S. S. 1996Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and fieldJ. Chem. Ecol.2217671781CrossRefGoogle Scholar
  52. Thaler, J. S., Fidantsef, A. L., Duffey, S. S., Bostock, R. M. 1999Trade-offs in plant defense against pathogens and herbivores: A field demonstration of chemical elicitors of induced resistanceJ. Chem. Ecol.2515971609CrossRefGoogle Scholar
  53. Thaler, J. S., Owen, B., Higgins, V. J. 2004The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestylesPlant Physiol.135530538CrossRefPubMedGoogle Scholar
  54. Tung, P., Hooker, T. S., Tampe, P. A., Reid, D. M., Thorpe, T. A. 1996Effects on growth and development of isolated tomato roots cultured in vitroInt. J. Plant Sci.157713721CrossRefGoogle Scholar
  55. Tzortzakakis, E. A., Gowen, S. R. 1996Occurrence of a resistance breaking pathotype of Meloidogyne javanica on tomatoes in Crete, GreeceFundam. Appl. Nematol.19283288Google Scholar
  56. Urwin, P. E., McPherson, M. J., Atkinson, H. J. 1998Enhanced transgenic plant resistance to nematodes by dual proteinase inhibitor constructsPlanta204472479CrossRefPubMedGoogle Scholar
  57. Urwin, P. E., Green, J., Atkinson, H. J. 2003Expression of a plant cystatin confers partial resistance to Globodera, full resistance is achieved by pyramiding a cystatin with natural resistanceMol. Breed.12263269CrossRefGoogle Scholar
  58. Dam, N. M., Horn, M., Mares, M., Baldwin, I. T. 2001Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuataJ. Chem. Ecol.27547568CrossRefPubMedGoogle Scholar
  59. Dam, N. M., Harvey, J. A., Wackers, F. L., Bezemer, T. M., Putten, W. H., Vet, L. E. M. 2003Interactions between aboveground and belowground induced responses against phytophagesBasic Appl. Ecol.46377CrossRefGoogle Scholar
  60. Poecke, R. M. P., Dicke, M. 2004Indirect defense of plants against herbivores: Using Arabidopsis thaliana as a model plantPlant Biol.6387401CrossRefPubMedGoogle Scholar
  61. Vijayan, P., Shockey, J., Levesque, C. A., Cook, R. J., Browse, J. 1998A role for jasmonate in pathogen defense of ArabidopsisProc. Natl Acad. Sci. USA9572097214CrossRefPubMedGoogle Scholar
  62. Wang, S. C., Ichii, M., Taketa, S., Xu, L. L., Xia, K., Zhou, X. 2002Lateral root formation in rice (Oryza sativa): Promotion effect of jasmonic acidJ. Plant Physiol.159827832CrossRefGoogle Scholar
  63. Williamson, V. M. 1998Root-knot nematode resistance genes in tomato and their potential for future useAnnu. Rev. Phytopathol.36277293CrossRefPubMedGoogle Scholar
  64. Williamson, V. M., Hussey, R. S. 1996Nematode pathogenesis and resistance in plantsPlant Cell817351745CrossRefPubMedGoogle Scholar
  65. Williamson, V. M., Gleason, C. 2003Plant–nematode interactionsCurr. Opin. Plant Biol.6327333CrossRefPubMedGoogle Scholar
  66. Yaghoobi, J., Kaloshian, I., Wen, Y., Williamson, V. M. 1995Mapping a new nematode resistance locus in Lycoperiscon peruvianumTheor. Appl. Genet.91457464CrossRefGoogle Scholar
  67. Zacheo, G., Orlando, C., Bleve-Zacheo, T. 1993Characterization of anionic peroxidases in tomato isolines infected by Meloidogyne incognitaJ. Nematol.25249256Google Scholar
  68. Zhang, Z. P., Baldwin, I. T. 1997Transport of [2-C-14] jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestrisPlanta203436441CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  1. 1.Department of EntomologyUniversity of ArkansasFayettevilleUSA
  2. 2.Department of EntomologyUniversity of KentuckyLexingtonUSA

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