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Salicylic acid is required for Mi-1-mediated resistance of tomato to whitefly Bemisia tabaci, but not for basal defense to this insect pest

Published online by Cambridge University Press:  02 June 2015

C.I. Rodríguez-Álvarez ,
M.F. López-Climent ,
A. Gómez-Cadenas ,
I. Kaloshian  and
G. Nombela
C.I. Rodríguez-Álvarez
Affiliation:
Department of Plant Protection, Institute for Agricultural Sciences, Spanish National Research Council (CSIC), Serrano 115 Dpdo., Madrid 28006, Spain
M.F. López-Climent
Affiliation:
Department of Experimental Sciences, University Jaume I (UJI), Castellón de la Plana 12071, Spain
A. Gómez-Cadenas
Affiliation:
Department of Experimental Sciences, University Jaume I (UJI), Castellón de la Plana 12071, Spain
I. Kaloshian
Affiliation:
Department of Nematology, University of California, Riverside, CA 92521, USA
G. Nombela*
Affiliation:
Department of Plant Protection, Institute for Agricultural Sciences, Spanish National Research Council (CSIC), Serrano 115 Dpdo., Madrid 28006, Spain
*
*Author for correspondence Phone: +1(34) 917452500 Fax: +1(34) 915640800 E-mail: [email protected]
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Abstract

Plant defense to pests or pathogens involves global changes in gene expression mediated by multiple signaling pathways. A role for the salicylic acid (SA) signaling pathway in Mi-1-mediated resistance of tomato (Solanum lycopersicum) to aphids was previously identified and its implication in the resistance to root-knot nematodes is controversial, but the importance of SA in basal and Mi-1-mediated resistance of tomato to whitefly Bemisia tabaci had not been determined. SA levels were measured before and after B. tabaci infestation in susceptible and resistant Mi-1-containing tomatoes, and in plants with the NahG bacterial transgene. Tomato plants of the same genotypes were also screened with B. tabaci (MEAM1 and MED species, before known as B and Q biotypes, respectively). The SA content in all tomato genotypes transiently increased after infestation with B. tabaci albeit at variable levels. Whitefly fecundity or infestation rates on susceptible Moneymaker were not significantly affected by the expression of NahG gene, but the Mi-1-mediated resistance to B. tabaci was lost in VFN NahG plants. Results indicated that whiteflies induce both SA and jasmonic acid accumulation in tomato. However, SA has no role in basal defense of tomato against B. tabaci. In contrast, SA is an important component of the Mi-1-mediated resistance to B. tabaci in tomato.

Keywords

salicylic acid (SA)jasmonic acid (JA)Mi-1Bemisia tabaciSolanum lycopersicum
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 5 , October 2015 , pp. 574 - 582
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Copyright
Copyright © Cambridge University Press 2015 

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References

Achuo, E.A., Audenaert, K., Meziane, H. & Höfte, M. (2004) The salicylic acid-dependent defense pathway is effective against different pathogens in tomato and tobacco. Plant Physiology 53, 65–72.Google Scholar
Alba, J., Glas, J., Schimmel, B. & Kant, M. (2011) Avoidance and suppression of plant defenses by herbivores and pathogens. Journal of Plant Interactions 6, 221–227.CrossRefGoogle Scholar
Ament, K., Kant, M.R., Sabelis, M.W., Haring, M.A. & Schuurink, R.C. (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiology 135, 2025–2037.Google Scholar
Anderson, J.P., Gleason, C.A., Foley, R.C., Thrall, P.H., Burdon, J.B. & Singh, K.B. (2010) Plants versus pathogens: an evolutionary arms race. Functional Plant Biology 37, 499–512.Google Scholar
Audenaert, K., De Meyer, G.B. & Höfte, M.M. (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiology 128, 491–501.Google Scholar
Beynon, J.L. (1997) Molecular genetics of disease resistance: an end to the ‘gene-for-gene’ concept? pp. 359–377 in Crute, I.R., Holub, E.B. and Burdon, J.J. (Eds) The Gene-for-gene Relationship in Plant-Parasite Interactions. New York, CAB International.Google Scholar
Bhattarai, K.K., Xie, Q.-G., Pourshalimi, D., Younglove, T. & Kaloshian, I. (2007) Coi1-dependent signaling pathway is not required for Mi-1-mediated potato aphid resistance. Molecular Plant-Microbe Interactions 20, 276–282.Google Scholar
Bhattarai, K.K., Xie, Q.-G., Mantelin, S., Bishnoi, U., Girke, T., Navarre, D.A. & Kaloshian, I. (2008) Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Molecular Plant-Microbe Interactions 21, 1205–1214.Google Scholar
Bonato, O., Lurette, A., Vidal, C. & Fargues, J. (2007) Modelling temperature-dependent bionomics of Bemisia tabaci (Q-biotype). Physiological Entomology 32, 50–55.Google Scholar
Bostock, R.M. (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annual Review of Phytpathology 43, 545–580.Google Scholar
Brading, P.A., Hammond-Kosack, K.E., Parr, A. & Jones, J.D. (2000) Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum . Plant Journal 23, 305–318.Google Scholar
Branch, C., Hwang, C.-F., Navarre, D.A. & Williamson, V.M. (2004) Salicylic acid is part of the Mi-1-mediated defense response to root-knot nematode in tomato. Molecular Plant-Microbe Interactions 17, 351–356.Google Scholar
Chaman, M.E., Copaja, S.V. & Arg&oña, V.H. (2003) Relationships between salicylic acid content, phenylalanine ammonia-lyase (PAL) activity, and resistance of barley to aphid infestation. Journal of Agricultural and Food Chemistry 51, 2227–2231.CrossRefGoogle ScholarPubMed
Cooper, W.C., Jia, L., & Goggin, F.L. (2004) Acquired and R-gene-mediated resistance against the potato aphid in tomato. Journal of Chemical Ecology 30, 2527–2542.CrossRefGoogle ScholarPubMed
De Barro, P.J., Liu, S.S., Boykin, L.M. & Dinsdale, A.B. (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 1–19.Google Scholar
Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E. & Ryals, J. (1994) A central role of salicylic acid in plant disease resistance. Science 266, 1247–1250.Google Scholar
Dinsdale, A., Cook, L., Riginos, C., Buckley, Y.M. & De Barro, P. (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America 103, 196–208.Google Scholar
Durgbanshi, A., Arbona, V., Pozo, O., Miersch, O., Sancho, J. V. & Gómez-Cadenas, A. (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography-electrospray tandem mass spectrometry. Journal of Agricultural and Food Chemistry 53, 8437–8442.Google Scholar
El Oirdi, M., El Rahman, T.A., Rigano, L., El Hadrami, A., Rodriguez, M.C., Daayf, F., Vojnov, A. & Bouarab, K. (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23, 2405–2421.CrossRefGoogle ScholarPubMed
Elzinga, D.A. & Jander, G. (2013) The role of protein effectors in plant-aphid interactions. Current Opinion in Plant Biology 16, 451–456.Google Scholar
Flor, H.H. (1971) Current status of the gene-for-gene concept. Annual Review of Phytpathology 9, 275–296.CrossRefGoogle Scholar
Friedrich, L., Lawton, K., Ruess, W., Masner, P., Specker, N., Rella, M.G., Meier, B., Dincher, S., Staub, T., Uknes, S., Métraux, J.-P., Kessmann, H. & Ryals, J. (1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant Journal 10, 61–70.Google Scholar
Fu, Z.Q. & Dong, X. (2013) Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology 64, 839–863.Google Scholar
Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. & Ryals, J. (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754–756.CrossRefGoogle ScholarPubMed
Guirao, P., Beitia, F. & Cenis, J.L. (1997) Biotype determination of Spanish populations of Bemisia tabaci (Hemiptera: Aleyrodidae). Bulletin of Entomological Research 87, 587–593.Google Scholar
Havlickova, H., Cvikrova, M., Eder, J. & Hrubcova, M. (1998) Alterations in the levels of phenolics and peroxidase activities induced by Rhopalosiphum padi (L.) in two winter wheat cultivars. Journal Plant Disease and Protection 105, 140–148.Google Scholar
Hogenhout, S.A. & Bos, J.I.B. (2011) Effector proteins that modulate plant–insect interactions. Current Opinion in Plant Biology 14, 1–7.Google Scholar
Kempema, L.A., Cui, X.P., Holzer, F.M. & Walling, L.L. (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiology 143, 849–865.Google Scholar
Kunkel, B.N. & Brooks, D.M. (2002) Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5, 325–331.CrossRefGoogle ScholarPubMed
Li, C., Schilmiller, A.L., Liu, G., Lee, G.I., Jayanty, S., Sageman, C., Vrebalov, J., Giovannoni, J.J., Yagi, K., Kobayashi, Y. & Howe, G.A. (2005) Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17, 971–986.CrossRefGoogle ScholarPubMed
Li, L., Lee, G.I. & Howe, G.A. (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proceedings of the National Academy of Sciences 99, 6416–6421.Google Scholar
Li, Q., Xie, Q.G., Smith Becker, J., Navarre, D.A. & Kaloshian, I. (2006) Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Molecular Plant-Microbe Interactions 19, 655–664.Google Scholar
Louis, J. & Shah, J. (2013) Arabidopsis thaliana-Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids. Frontiers in Plant Science, 4, article 213, 1–18. doi: 10.3389/fpls.2013.00213.Google Scholar
Martínez de Ilarduya, O., Xie, Q. & Kaloshian, I. (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Molecular Plant-Microbe Interactions 16, 699–708.Google Scholar
Muñiz, M. & Nombela, G. (2001) Bemisia tabaci: a new clip-cage for biological studies. European Whitefly Studies Network A2, 1–2.Google Scholar
Mur, L.A.J., 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 Physiology 140, 249–262.Google Scholar
Nombela, G., Beitia, F.J. & Muñiz, M. (2001) A differential interaction study of Bemisia tabaci Q-biotype on commercial tomato varieties with or without the Mi resistance gene, and comparative host responses with the B-biotype. Entomologia Experimentalis et Applicata 98, 339–344.CrossRefGoogle Scholar
Nombela, G., Williamson, V.M. & Muñiz, M. (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci . Molecular Plant-Microbe Interactions 16, 645–649.CrossRefGoogle ScholarPubMed
Nombela, G., Pascual, S., Aviles, M., Guillard, E. & Muñiz, M. (2005) Benzothiadiazole induces local resistance to Bemisia tabaci (Hemiptera: Aleyrodidae) in tomato plants. Journal of Economic Entomology 98, 2266–2271.Google Scholar
Nombela, G., Garzo, E., Duque, M. & Muñiz, M. (2009) Preinfestations of tomato plants by whiteflies (Bemisia tabaci) or aphids (Macrosiphum euphorbiae) induce variable resistance or susceptibility responses. Bulletin of Entomological Research 99, 183–191.Google Scholar
O'Donnell, P.J., Schmelz, E., Block, A., Miersch, O., Wasternack, C., Jones, J.B. & Klee, H.J. (2003) Multiple hormones act sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiology 133, 1181–1189.Google Scholar
Pautot, V., Holzer, F.M., Reisch, B. & Walling, L.L. (1993) Leucine aminopeptidase: an inducible component of the defense response in Lycopersicon esculentum (tomato). Proceedings of the National Academy of Sciences 90, 9906–9910.Google Scholar
Pieterse, C.M., Van der Does, D., Zamioudis, C., Leon-Reyes, A. & Van Wees, S.C. (2012) Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28, 489–521.Google Scholar
Puthoff, D.P., Holzer, F.M., Perring, T.M. & Walling, L.L. (2010) Tomato pathogenesis-related protein genes are expressed in response to Trialeurodes vaporariorum and Bemisia tabaci Biotype B Feeding. Journal of Chemical Ecology 36, 1271–1285.Google Scholar
Robert-Seilaniantz, A., Grant, M. & Jones, J.D. (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytpathology 49, 317–343.Google Scholar
Roberts, P.A. & Thomason, I.J. (1986) Variability in reproduction of isolates of Meloidogyne incognita and M. javanica on resistant tomato genotypes. Plant Disease Journal 70, 547–551.Google Scholar
Rojo, E., Solano, R. & Sánchez-Serrano, J.J. (2003) Interactions between signaling compounds involved in plant defense. Journal of Plant Growth Regulation 22, 82–98.Google Scholar
Rossi, M., Goggin, F.L., Milligan, S.B., Kaloshian, I., Ullman, D.E. & Williamson, V.M. (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences 95, 9750–9754.Google Scholar
Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C. & Manners, J.M. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences 97, 11655–11660.Google Scholar
Spoel, S.H., Koornneef, A., Claessens, S.M.C., Korzelius, J.P., Van Pelt, J.A., Mueller, M.J., Buchala, A.J., Métraux, J.-P., Brown, R., Kazan, K., Van Loon, L.C., Dong, X. & Pieterse, C.M.J. (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15, 760–770.Google Scholar
StatSoft (1994) Statistica version 4.5 for the Windows operating system. Reference for statistical procedures. StatSoft, Tulsa, OK, U.S.A.Google Scholar
Thaler, J.S., Agrawal, A.A. & Halitschke, R. (2010) Salicylate-mediated interactions between pathogens and herbivores. Ecology 91, 1075–1082.Google Scholar
Thompson, G.A. & Goggin, F.L. (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. Journal of Experimental Botany 57, 755–766.CrossRefGoogle ScholarPubMed
van Loon, L.C., Rep, M. & Pieterse, C.M.J. (2006) Significance of inducible defense-related proteins in infected plants. Annual Review of Phytpathology 44, 135–162.Google Scholar
Vlot, A.C., Dempsey, D.A. & Klessig, D.F. (2009) Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology 47, 177–206.Google Scholar
Walling, L. (2000) The Myriad plant responses to herbivores. Journal of Plant Growth Regulation 19, 195–216.Google Scholar
Walling, L.L. (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiology 146, 859–866.CrossRefGoogle ScholarPubMed
Zarate, S.I., Kempema, L.A. & Walling, L.L. (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiology 143, 866–875.Google Scholar
Zhang, P.-J., Zheng, S.-J., Loon, J.J.A., van Boland, W., David, A., Mumm, R. & Dicke, M. (2009) Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proceedings of the National Academy of Sciences 106, 21202–21207.CrossRefGoogle ScholarPubMed