Arthropod-Plant Interactions

, Volume 6, Issue 2, pp 221–230 | Cite as

Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes

  • Kei Kawazu
  • Atsushi Mochizuki
  • Yukie Sato
  • Wataru Sugeno
  • Mika Murata
  • Shigemi Seo
  • Ichiro Mitsuhara
Original Paper


We compared the expression profiles of jasmonic acid (JA)-inducible genes (Pin2 and LapA1) and salicylic acid (SA)-inducible genes (PRb-1b and GluB) in the tomato (Solanum lycopersicum cv. Micro-Tom) against herbivores using differing feeding modes: the leaf-chewing larvae of the insects Spodoptera litura and S. exigua; the western flower thrips (Frankliniella occidentalis) and the two-spotted spider mite (Tetranychus urticae) as cell-content feeders; and the leaf miner fly (Liriomyza sativae). Feeding by larvae of both S. litura and S. exigua chiefly activated JA-inducible genes, similar to the response to wound stimuli. Feeding by the thrips F. occidentalis also activated JA-inducible genes, as previously reported in Arabidopsis. Feeding by the spider mite T. urticae activated a JA-inducible LapA1 gene but did not activate a JA-inducible Pin2 gene and additionally activated SA-inducible genes, which were accompanied by the accumulation of SA. This may be a strain that represses induction of the JA signaling pathway. One day after oviposition by the leaf miner fly, L. sativae, JA-inducible genes were activated. However, after the L. sativae larvae hatched and began eating within the leaf tissues, JA-inducible gene expression decreased and SA-inducible gene expression increased. Activation of SA-inducible genes (PRb-1b and GluB) by L. sativae larval feeding seems to suppress JA-mediated plant defense but appears to be unrelated to SA accumulation.


Lepidopteran insect Thrips Spider mite Leaf miner fly Solanum lycopersicum cv. Micro-Tom 



We thank Ms. Yoko Gotoh and Ms. Masumi Teruse for their technical assistance and Ms. Kayoko Furukawa and Ms. Chiaki Kimoto for their assistance in insect rearing and plant growing. This study was supported in part by the Program for Promotion of Basic Research Activities for Innovative Biosciences, Bio-oriented Technology Research Advancement Institution.

Supplementary material

11829_2011_9174_MOESM1_ESM.jpg (87 kb)
Online Resources 1 Feeding scars on tomato leaves at different time points after inoculation of chewing caterpillars, Spodoptera litura and S. exigua, and of cell-content feeders, Frankliniella occidentalis and Tetranychus urticae, and after oviposition of leafminer fly, Liriomyza sativae. (JPEG 86 kb)
11829_2011_9174_MOESM2_ESM.jpg (141 kb)
Online Resources 2 Expression profiles of JA- and SA-inducible genes in tomato leaves treated with methyl jasmonate (MeJA), salicylic acid (SA), and distilled water (DW). The data were normalized by the expression level of an Actin gene, and fold-change in the expression levels in the tomato plant at the 4-leaf stage was calculated as a ratio with respect to those of healthy leaves at 0 days. (JPEG 141 kb)


  1. Abe H, Ohnishi J, Narusaka M, Seo S, Narusaka Y, Tsuda S, Kobayashi M (2008) Function of jasmonate in response and tolerance of Arabidopsis to thrips feeding. Plant Cell Physiol 49:68–80PubMedCrossRefGoogle Scholar
  2. Arimura G, Tashiro K, Kuhara S, Nishioka T, Ozawa R, Takabayashi J (2000) Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochem Biophys Res Commun 277:305–310PubMedCrossRefGoogle Scholar
  3. Avdiushko SA, Brown GC, Dahlman DL, Hildebrand DF (1997) Methyl jasmonate exposure induces insect resistance in cabbage and tobacco. Environ Entomol 26:642–654Google Scholar
  4. Boughton AJ, Hoover K, Felton GW (2005) Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J Chem Ecol 31:2211–2216PubMedCrossRefGoogle Scholar
  5. Campos ML, de Almeida M, Rossi ML, Martinelli AP, Litholdo Junior CG, Figueira A, Rampelotti-Ferreira FT, Vendramim JD, Benedito VA, Peres LEP (2009) Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. J Exp Bot 60:4347–4361PubMedCrossRefGoogle Scholar
  6. Chao WS, Gu YQ, Pautot V, Bray EA, Walling L (1999) Leucine aminopeptidase RNAs, proteins, and activities increase in response to water deficit, salinity, and the wound signals systemin, methyl jasmonate, and abscisic acis. Plant Physiol 120:979–992PubMedCrossRefGoogle Scholar
  7. Cipollini DF, Redman AM (1999) Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato. J Chem Ecol 25:271–281CrossRefGoogle Scholar
  8. Cipollini DF, Sipe M (2001) Jasmonic acid treatment and mammalian herbivory differentially affect chemical defense expression and growth of Brassica kaber. Chemoecology 11:137–143CrossRefGoogle Scholar
  9. Cipollini D, Enright S, Traw MB, Bergelson J (2004) Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol Ecol 13:1643–1653PubMedCrossRefGoogle Scholar
  10. Constabel CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–296PubMedCrossRefGoogle Scholar
  11. De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux JP, Van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant-Microbe Int 18:923–937CrossRefGoogle Scholar
  12. De Vos M, Van Zaanen W, Koorneef A, Korzelius JP, Dicke M, Van Loon LC, Pieterse CMJ (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol 142:352–363PubMedCrossRefGoogle Scholar
  13. Diezel C, von Dahl C, Gaquerel E, Baldwin IT (2009) Different lepidopteran elicitors account for crosstalk in herbivory-induced phytohormone signaling. Plant Physiol 150:1576–1586PubMedCrossRefGoogle Scholar
  14. Doares SH, Narváez-Vásquez J, Conconi A, Ryan CA (1995) Salicylic-acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746PubMedGoogle Scholar
  15. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedCrossRefGoogle Scholar
  16. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  17. Eichenseer H, Mathews MC, Bi JL, Murphy JB, Felton GW (1999) Salivary glucose oxidase: multifunctional roles for Helicoverpa zea. Arch Insect Biochem Physiol 42:99–109PubMedCrossRefGoogle Scholar
  18. Ellis C, Karafyllidis I, Turner JG (2002) Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol Plant-Microbe Int 15:1025–1030CrossRefGoogle Scholar
  19. Glawe GA, Zavala A, Kessler A, Van Dam NM, Baldwin IT (2003) Ecological costs and benefits correlated with trypsin protease inhibitor production in Nicotiana attenuata. Ecology 84:79–90CrossRefGoogle Scholar
  20. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann Rev Phytopathol 43:205–227CrossRefGoogle Scholar
  21. Gotoh T (1996) Rearing of the spider mite. In: Ehara S, Shinkaji N (eds) Principles of plant acarology. The Association of Natural Farm Education, Tokyo, pp 314–319 (in Japanese)Google Scholar
  22. Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777PubMedCrossRefGoogle Scholar
  23. Gu Y-Q, Pautot V, Holzer FM, Walling LL (1996) A complex array of proteins related to the multimeric leucine aminopeptidase of tomato. Plant Physiol 110:1257–1266PubMedGoogle Scholar
  24. Halitschke R, Ziegler J, Keinänen M, Baldwin IT (2004) Silencing of hydroperoxide lyase and allene oxide synthase reveals substrate and defense signaling crosstalk in Nicotiana attenuata. Plant J 40:35–46PubMedCrossRefGoogle Scholar
  25. Heidel AJ, Baldwin IT (2004) Microarray analysis of salicylic acid- and jasmonic acid- signaling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ 27:1362–1373CrossRefGoogle Scholar
  26. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66PubMedCrossRefGoogle Scholar
  27. Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8:2067–2077PubMedCrossRefGoogle Scholar
  28. Ilarduya OM, Xie Q, Kaloshian I (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol Plant-Microbe Int 16:699–708CrossRefGoogle Scholar
  29. Johnson R, Narvaez J, An GH, Ryan CA (1989) Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc Natl Acad Sci USA 86:9871–9875PubMedCrossRefGoogle Scholar
  30. Kandoth PK, Ranf S, Pancholi SS, Jayanty S, Walla MD, Miller W, Howe GA, Lincoln DE, Stratmann JW (2007) Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects. Proc Natl Acad Sci USA 104:12205–12210PubMedCrossRefGoogle Scholar
  31. Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135:483–495PubMedCrossRefGoogle Scholar
  32. Kant MR, Sabelis MW, Haring MA, Schuurink RC (2008) Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defenses. Proc R Soc B 275:443–452PubMedCrossRefGoogle Scholar
  33. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Ann Rev Plant Biol 53:299–328CrossRefGoogle Scholar
  34. Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844PubMedCrossRefGoogle Scholar
  35. Lawrence SD, Novak NG, Ju CJT, Cooke JEK (2008) Potato, Solanum tuberosum, defense against Colorado potato beetle, Leptinotarsa decemlineata (Say): microarray gene expression profiling of potato by Colorado potato beetle regurgitant treatment of wounded leaves. J Chem Ecol 34:1013–1025PubMedCrossRefGoogle Scholar
  36. Li C, Williams MM, Loh Y-T, Lee GI, Howe GA (2002) Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiol 130:494–503PubMedCrossRefGoogle Scholar
  37. Li Q, Xie Q-G, Smith-Becker J, Navarre DA, Kaloshian I (2006) Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol Plant-Microbe Int 19:655–664CrossRefGoogle Scholar
  38. Merkx-Jacques M, Bede JC (2004) Caterpillar salivary enzymes: “eliciting” a response. Phytoprotection 85:33–37Google Scholar
  39. Mithöfer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1161–1168CrossRefGoogle Scholar
  40. Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085PubMedCrossRefGoogle Scholar
  41. Moran PJ, Cheng Y, Cassell JL, Thompson GA (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Arch Insect Biochem Physiol 51:182–203PubMedCrossRefGoogle Scholar
  42. Mueller LA, Solow TH, Taylor N, Skwarecki B, Buels R, Binns J, Lin C, Wright MH, Ahrens R, Wang Y et al (2005) The SOL genomics network. A comparative resource for Solanaceae biology and beyond. Plant Physiol 138:1310–1317PubMedCrossRefGoogle Scholar
  43. Mueller LA, Lankhorst KR, Tanksley SD, Giovannoni JJ, White R, Vrebalov J, Fei Z, van Eck J, Buels R, Mills AA et al (2009) A snapshot of the emerging tomato genome sequence. Plant Genome 2:78–92CrossRefGoogle Scholar
  44. Mur LAJ, 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
  45. Musser RO, Cipollini DF, Hum-Musser SM, Williams SA, Brown JK, Felton GW (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Arch Insect Biochem Physiol 58:128–137PubMedCrossRefGoogle Scholar
  46. Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol 39:500–507CrossRefGoogle Scholar
  47. Omer AD, Granett J, Karban R, Villa EM (2001) Chemically induced resistance against multiple pests in cotton. Int J Pest Manag 47:49–54CrossRefGoogle Scholar
  48. Pautot V, Holzer FM, Reisch B, Walling LL (1993) Leucine aminopeptidase: an inducible component of the defense response in Lycopersicon esculentum (tomato). Proc Natl Acad Sci USA 90:9906–9910PubMedCrossRefGoogle Scholar
  49. Pegadaraju V, Knepper C, Reese J, Shah J (2005) Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid. Plant Physiol 139:1927–1934PubMedCrossRefGoogle Scholar
  50. Peña-Cortés H, Albrecht T, Prat S, Weiler EW, Willmitzer L (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128CrossRefGoogle Scholar
  51. Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569PubMedCrossRefGoogle Scholar
  52. Puthoff DP, Holzer FM, Perring TM, Walling LL (2010) Tomato pathogenesis-related protein genes are expressed in response to Trialeurodes vaporariorum and Bemisia tabaci biotype B feeding. J Chem Ecol 36:1271–1285PubMedCrossRefGoogle Scholar
  53. Rayapuram C, Baldwin IT (2007) Increased SA in NPR1-silenced plants antagonizes JA and JA-dependent direct and indirect defenses in herbivore-attacked Nicotiana attenuata in nature. Plant J 52:700–715PubMedCrossRefGoogle Scholar
  54. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner H-Y, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819PubMedCrossRefGoogle Scholar
  55. Ryan CA (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477:112–121PubMedCrossRefGoogle Scholar
  56. Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A, Oliveira MGA, Lima ER, Kant M, Sabelis MW, Janssen A (2011) A herbivore that manipulates plant defence. Ecol Lett 14:229–236PubMedCrossRefGoogle Scholar
  57. Seo S, Okamoto M, Seto H, Ishizuka K, Sano H, Ohashi Y (1995) Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270:1988–1992PubMedCrossRefGoogle Scholar
  58. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman WH and Company, New YorkGoogle Scholar
  59. Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux JP, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770PubMedCrossRefGoogle Scholar
  60. Stotz HU, Koch T, Biedermann A, Weniger K, Boland W, Mitchell-Olds T (2002) Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways. Planta 214:648–652PubMedCrossRefGoogle Scholar
  61. Stout NJ, Workman J, Duffey SS (1994) Differential induction of tomato foliar proteins by arthropod herbivores. J Chem Ecol 20:2575–2594CrossRefGoogle Scholar
  62. Stout MJ, Workman KV, Bostock RM, Duffey SS (1998) Stimulation and attenuation of induced resistance by elicitors and inhibitors of chemical induction in tomato (Lycopersicon esculentum) foliage. Entomol Exp Appl 86:267–279CrossRefGoogle Scholar
  63. Thaler JS, Farag MA, Paré PW, Dicke M (2002) Jasmonate-deficient plants have reduced direct and indirect defences against herbivores. Ecol Let 5:764–774CrossRefGoogle Scholar
  64. Thomma BP, Penninckx IA, Cammue BP, Broekaert WF (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immuno 13:63–68CrossRefGoogle Scholar
  65. Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755–766PubMedCrossRefGoogle Scholar
  66. Van Kan JAL, Cozijnsen T, Danhash N, de Wit PJGM (1995) Induction of tomato stress protein mRNAs by ethephon, 2, 6-dichloroisonicotinic acid and salicylate. Plant Mol Biol 27:1205–1213PubMedCrossRefGoogle Scholar
  67. von Dahl CC, Winz RA, Halitschke R, Kühnemann F, Gase K, Baldwin IT (2007) Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. Plant J 51:293–307CrossRefGoogle Scholar
  68. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216PubMedGoogle Scholar
  69. Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866PubMedCrossRefGoogle Scholar
  70. Wang L, Allmann S, Wu JS, Baldwin IT (2008) Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiol 146:904–915PubMedCrossRefGoogle Scholar
  71. Wu J, Baldwin IT (2009) Herbivory-induced signalling in plants: perception and action. Plant Cell Environ 32:1161–1174PubMedCrossRefGoogle Scholar
  72. Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875PubMedCrossRefGoogle Scholar
  73. Zheng SJ, Dicke M (2008) Ecological genomics of plant-insect interactions: from gene to community. Plant Physiol 146:812–817PubMedCrossRefGoogle Scholar
  74. Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B, Lou Y (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60:638–648PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Kei Kawazu
    • 1
  • Atsushi Mochizuki
    • 1
  • Yukie Sato
    • 1
  • Wataru Sugeno
    • 1
  • Mika Murata
    • 1
  • Shigemi Seo
    • 2
  • Ichiro Mitsuhara
    • 2
  1. 1.National Institute for Agro-Environmental SciencesTsukuba, IbarakiJapan
  2. 2.National Institute of Agrobiological SciencesTsukuba, IbarakiJapan

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