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The Participation of salicylic and jasmonic acids in genetic and induced resistance of tomato to Meloidogyne incognita (Kofoid and White, 1919)

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Abstract

Salicylic (SA) and jasmonic (JA) acids are the best known mediators of signal systems in plants. In this investigation the participation and character of interactions between SA- and JA-signals under the induced and genetic resistance of plants to nematodes was investigated on the model system tomato (Lycopersicon esculentum) and the root-knot nematode Meloidogyne incognita. This study demonstrates that application of JA and SA to tomato foliage induces systemic effects that suppress root-knot nematode infestation, inhibition of nematode reproduction, and also increased activity of LOX and PAL, the enzymes of biosynthesis of JA and SA. JA treatment did not inhibit Mz-mediated resistance, which suggests a lack of signaling conflicts between these two forms of defense.

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References

  • Bhattarai, K.K., **e, Qi-G., Mantelin, S., et al., Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway, MPMI, 2008, vol. 21, no. 9, pp. 1205–1214.

    Article  PubMed  CAS  Google Scholar 

  • Bradford, M.M., Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, no. 1, pp. 248–254.

    Article  PubMed  CAS  Google Scholar 

  • Branch, C., Hwang, C.-F., Navarre, D.A., and Willamson, V.M., Salicylic acid is part of the Mi-1-mediated defense response to root-knot nematode in tomato, Mol. Plant-Microbe Interact., 2004, vol. 17, no. 4, pp. 351–356.

    Article  PubMed  CAS  Google Scholar 

  • Chizhov, V.N., Pridannikov, M.V., and Subbotin, S.A., Root-knot nematodes of the family Meloidogynidae, Skarbilovich, 1959, in Fitoparaziticheskie nematody Rossii (Phytoparasitic Nematodes in Russia), Moscow: KMK, 2012, pp. 89–118.

    Google Scholar 

  • Cooper, W.R., Jia, L., and Goggin, L., Effects of jasmonate-induced defenses on root-knot nematode infection of resistant and susceptible tomato cultivars, J. Chem. Ecol., 2005, vol. 31, pp. 1953–1967.

    Article  PubMed  CAS  Google Scholar 

  • Dropkin, V.H., The necrotic reaction of tomatoes and other hosts resistant to meloidogyne: reversal by temperature, Phytopathology, 1969, vol. 59, pp. 1632–1637.

    Google Scholar 

  • Durrant, W.E. and Dong, X., Systemic acquired resistance, Annu. Rev. Phytopathol., 2004, vol. 42, no. 3, pp. 185–209.

    Article  PubMed  CAS  Google Scholar 

  • Farmer, E.E., Almeras, E., and Krisnamurthy, V., Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory, Curr. Op. Plant Biol., 2003, vol. 6, pp. 372–378.

    Article  CAS  Google Scholar 

  • Feussner, I. and Wasternack, C., The lipoxygenase pathway, Annu. Rev. Plant Biol., 2002, vol. 53, pp. 275–279.

    Article  PubMed  CAS  Google Scholar 

  • Fujimoto, T., Tomitaka, Y., Abe, H., et al., Jasmonic acid signaling pathway of Arabidopsis thaliana is import for root-knot nematode invasion, Nematol. Res., 2011a, vol. 41, no. 1, pp. 9–17.

    Article  Google Scholar 

  • Fujimoto, T., Tomitaka, Y., Abe, H., et al., Expression profile of jasmonic acid-induced genes and induced resistance against the import for root-knot nematode (Meloidogyne incognita) in tomato plants (Solanum lycopersicum) after foliar treatment with methyl jasmonate, J. Plant Physiol., 2011b, vol. 168, no. 8, pp. 1084–1097.

    Article  PubMed  CAS  Google Scholar 

  • Gerasimova, N.G., Pridvorova, S.M., and Ozeretskovskaya, O.L., Role of L-phenylalanine ammonia lyase in the induced resistance and susceptibility of potato plants, Appl. Biochem. Microbiol., 2005, vol. 41, no. 1, pp. 103–105.

    CAS  Google Scholar 

  • Glazebrook, J., Contrasting mechanisms of defense aganst biotrophic and necrotrophic pathogens, Annu. Rev. Phytopathol., 2005, vol. 43, pp. 205–227.

    Article  PubMed  CAS  Google Scholar 

  • Gutjahr, C. and Paszkowski, U., Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions, Mol. Plant-Microbe Interact., 2009, vol. 22, no. 7, pp. 763–772.

    Article  PubMed  CAS  Google Scholar 

  • Holtzman, O., Effects of soil temperature on resistance of tomato to root-knot nematode (Meloidogyne incognita), Phytopathology, 1965, vol. 55, pp. 990–992.

    Google Scholar 

  • Howe, G.A., Lightner, J., Browse, J., and Ryan, C.A., An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack, Plant Cell, 1996, vol. 8, pp. 2067–2077.

    PubMed  CAS  Google Scholar 

  • Il’inskaya, L.I., Gerasimova, N.A., Perekhod, E.A., et al., Lipoxygenase activity in plants with induced resistance to diseases, Russ. J. Plant Physiol., 2000, vol. 47, no. 4, pp. 449–455.

    Google Scholar 

  • Kessier, A. and Baldwin, I.T., Plant responses to insect herbivory: the emerging molecular analysis, Annu. Rev. Plant Biol., 2002, vol. 53, pp. 299–328.

    Article  Google Scholar 

  • Kuc, J., Development and future direction of induced systemic resistance in plans, Crop Protection, 2000, vol. 18, pp. 859–861.

    Article  Google Scholar 

  • Kunkel, B.N. and Brooks, D.M., Cross-talk between signaling pathways in pathogen defense, Curr. Opin. Plant Biology, 2002, vol. 5, pp. 325–331.

    Article  CAS  Google Scholar 

  • Li, C., Willams, M.M., Loh, Y.-T., et al., Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway, Plant Physiol., 2002, vol. 130, pp. 494–503.

    Article  PubMed  CAS  Google Scholar 

  • McConn, M., Creelman, R.A., Bell, E., et al., Jasmonate is essential for insect defense in Arabidopsis, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 5473–5477.

    Article  PubMed  CAS  Google Scholar 

  • McDowell, J.M. and Dangl, J.L., Signal transduction in the plant immune response, Trends Biochem. Sci., 2000, vol. 25, pp. 79–82.

    Article  PubMed  CAS  Google Scholar 

  • Melillo, M.T., Leonetti, P., Bongiovanni, M., et al., Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato-root knot nematode interactions, New Phytol., 2006, vol. 170, pp. 501–512.

    Article  PubMed  CAS  Google Scholar 

  • Milligan, S.B., Bodeau, J., Yaghoobi, J., et al., The root knot nematode resistance gene mi from tomato is a member of the leucine zipper, nucleotide binding, leucine rich repeat family of plant genes, Plant Cell, 1998, vol. 10, pp. 1307–1319.

    PubMed  CAS  Google Scholar 

  • Molinari, S., Inhibition of H2O2-degrading enzymes in the response of Mi-bearing tomato to root-knot nematodes and salicylic acid treatment, Nematol. Mediterr., 2001, vol. 29, pp. 235–239.

    Google Scholar 

  • Molinari, S., New developments in understanding the role of salicylic acid in plant defense, CAB Rev., 2007, vol. 67, pp. 1–10.

    Google Scholar 

  • Molinari, S., Salicylic acid as an elicitor of resistance to root-knot nematodes in tomato, Acta Hort. (ISHS), 2008, vol. 789, pp. 119–126.

    CAS  Google Scholar 

  • Molinari, S., Natural genetic and induced plant resistance, as a control strategy to plant-parasitic nematodes alternative to pesticides, Plant Cell Rep., 2011, vol. 30, pp. 311–323.

    Article  PubMed  CAS  Google Scholar 

  • Molinari, S. and Loffredo, E., The role of salicylic acid in defense response of tomato to root-knot nematodes, Physiol. Mol. Plant Pathol., 2006, vol. 68, pp. 69–78.

    Article  CAS  Google Scholar 

  • Molinari, S., Zacheo, G., and Bleve-Zacheo, T., Effects of nematode infestation on mitochondria isolated from susceptible and resistant tomato roots, Physiol. Mol. Plant Pathol., 1990, vol. 37, pp. 27–37.

    Article  CAS  Google Scholar 

  • Nandi, B., Sukual, N.C., Banerjee, N., et al., Salicylic acid enhances resistance in cowpea against Meloidogyne incognita, Phytopathol. Medit., 2002, vol. 41, pp. 39–44.

    CAS  Google Scholar 

  • Nombela, G., Williamson, V.M., and Muniz, M., The root-knot nematode resistance gene Mi-1.2 of Tomato is responsible for resistance against the whitefly Bemisia tabaci, Mol. Plant-Microbe Interact., 2003, vol. 16, pp. 645–649.

    Article  PubMed  CAS  Google Scholar 

  • Reymond, P. and Farmer, E.E., Jasmonate and salicylate as global signals for defense gene expression, Curr. Opin. Plant Biol., 1998, vol. 1, no. 5, pp. 404–411.

    Article  PubMed  CAS  Google Scholar 

  • Rossi, M., Goggin, F.L., Milligan, S.B., et al., The nematode resistance gene Mi of tomato confers resistance against the potato aphid, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 9750–9754.

    Article  PubMed  CAS  Google Scholar 

  • Ryan, C.A. and Moura, D.S., Systemic wound signaling in plants: a new perception, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 6519–6520.

    Article  PubMed  CAS  Google Scholar 

  • Semblat, J.P., Rosso, M.N., and Hussey, R.S., Molecular cloning of a cDNA encoding an amphid secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita, Mol. Plant-Microbe Interact., 2001, vol. 14, pp. 72–79.

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui, I.A. and Shaukat, S.S., Systemic resistance in tomato induced by biocontrol bacteria against the root-knot nematode, Meloidogyne javanica is independent of salicylic acid production, J. Phytopathol., 2002, vol. 152, no. 1, pp. 48–54.

    Article  Google Scholar 

  • Tarchevskii, I.A., Signal’nye sistemy kletok rastenii (Signaling Systems of Plant Cells), Moscow: Nauka, 2002.

    Google Scholar 

  • Tzortzakakis, E.A. and Gowen, S.R., Occurrence of a resistance breaking pathotype of Meloidogyne javanica on tomatoes in Crete, Greece, Fundam. Appl. Nematol., 1996, vol. 19, pp. 283–288.

    Google Scholar 

  • Udalova, Zh., Vasyukova, N., Zinovieva, S., and Baicheva, O., Immunomodulation activity of chitin-chitosan oligomer with fragments of salicylic acid in tomato-root-knot nematode system, J. Balkan Ecol., 2011a, vol. 14, no. 4, pp. 397–403.

    Google Scholar 

  • Udalova, Zh.V., Baicheva, O., Pridannikov, M.V., and Zinovieva, S.V., Promising methods of plant protection against root-knot nematodes, Ross. Parazitol. Zh., 2011b, no. 2, pp. 109–115.

    Google Scholar 

  • Vasyukova, N.I. and Ozeretskovskaya, O.L., Induced plant resistance and salicylic acid: a review, Appl. Biochem. Microbiol., 2007, vol. 43, no. 4, pp. 367–373.

    Article  CAS  Google Scholar 

  • Vasyukova, N.I. and Ozeretskovskaya, O.L., Jasmonate-dependent defense signaling in plant tissues, Russ. J. Plant Physiol., 2009, vol. 56, no. 5, pp. 581–590.

    Article  CAS  Google Scholar 

  • Vasyukova, N.I., Panina, Ya.S., Zinovieva, S.V., et al., The role of salicylic acid in systemic resistance of tomato to nematodes, Dokl. Biol. Sci., 2003, vol. 391, pp. 343–345.

    Article  PubMed  CAS  Google Scholar 

  • Vasyukova, N.I., Pridvorova, S.M., Gerasimova, N.G., et al., The involvement of phenylalanine ammonia-lyase and salicylic acid in the induction of resistance of tomato plants infested with gall nematode Meloidogyne incognita, Dokl. Biol. Sci., 2007, vol. 416, pp. 382–385.

    Article  PubMed  CAS  Google Scholar 

  • Vasyukova, N.I., Zinovieva, S.V., Udalova, Zh.V., et al., Jasmonic acid and tomato plant resistance to root-knot nematode Meloidogyne incognitas, Dokl. Biol. Sci., 2009, vol. 428, pp. 430–433.

    Article  Google Scholar 

  • Williamson, V.M. and Hussey, R.S., Nematode pathogenesis and resistance in plants, Plant Cell, 1996, vol. 8, pp. 1735–1745.

    PubMed  CAS  Google Scholar 

  • Wubben, M.J.E., **, J., and Baum, T.J., Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots, Mol. Plant-Microbe Interact., 2008, vol. 21, no. 4, pp. 424–432.

    Article  PubMed  CAS  Google Scholar 

  • Zinovieva, S.V., Vasyukova, N.I., Udalova, Zh.V., et al., The role of salicylic acid in systemic resistance of tomato to nematodes, Dokl. Biol. Sci., 2003, vol. 391, pp. 343–345.

    Article  Google Scholar 

  • Zinovieva, S.V., Udalova, Zh.V., Vasyukova, N.I., and Ozeretskovskaya, O.L., Effect of biogenic elicitors on the infection of potato with Globodera rostochiensis Beherens, 1975, Tr. Vseros. Inst. Gel’mintologii im. K.I. Skryabina, 2007, vol. 43, pp. 104–114.

    Google Scholar 

  • Zinovieva, S.V., Vasyukova, N.I., Udalova, Zh.V., and Gerasimova, N.G., Study of immunological mechanisms of interaction of parasitic nematodes and plants: the role of elicitors and signaling molecules, in Teoreticheskie i prakticheskie problemy parazitologii (Theoretical and Practical Problems of Parasitology), Moscow: Nauka, 2010, pp. 135–139.

    Google Scholar 

  • Zinovieva, S.V., Vasyukova, N.I., Udalova, Zh.V., et al., Involvement of salicylic acid in induction of nematode resistance in plants, Biol. Bull., 2011, vol. 38, no. 5, pp. 453–458.

    Article  CAS  Google Scholar 

  • Zinovieva, S.V., Ozeretskovskaya, O.L., Iliinskaya, L.I., and Yasyukiva, N.I., Biogenic elicitor (arachidonic acid) induced resistance in tomato to Meloidogyne incognita, Russ. J. Nematol., 1995, vol. 3, no. 1, pp. 65–67.

    Google Scholar 

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Authors and Affiliations

  1. Centre of Parasitology, Severtsov Institute of Problems of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr. 33, Moscow, 119071, Russia

    S. V. Zinovieva & Zh. V. Udalova

  2. Bach Institute of Biochemistry, Russian Academy of Sciences, Leninskii pr. 33, Moscow, 119071, Russia

    N. I. Vasyukova & N. G. Gerasimova

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  1. S. V. Zinovieva
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  2. N. I. Vasyukova
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  3. Zh. V. Udalova
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  4. N. G. Gerasimova
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Correspondence to S. V. Zinovieva.

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Original Russian Text © S.V. Zinovieva, N.I. Vasyukova, Zh.V. Udalova, N.G. Gerasimova, 2013, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2013, No. 3, pp. 332–340.

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Zinovieva, S.V., Vasyukova, N.I., Udalova, Z.V. et al. The Participation of salicylic and jasmonic acids in genetic and induced resistance of tomato to Meloidogyne incognita (Kofoid and White, 1919). Biol Bull Russ Acad Sci 40, 297–303 (2013). https://doi.org/10.1134/S1062359013030126

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