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Roles of ethylene and jasmonic acid in systemic induced defense in tomato (Solanum lycopersicum) against Helicoverpa zea


Inducible defenses that provide enhanced resistance to insect attack are nearly universal in plants. The defense-signaling cascade is mediated by the synthesis, movement, and perception of jasmonate (JA) and the interaction of this signaling molecule with other plant hormones and messengers. To explore how the interaction of JA and ethylene influences induced defenses, we employed the never-ripe (Nr) tomato mutant, which exhibits a partial block in ethylene perception, and the defenseless (def1) mutant, which is deficient in JA biosynthesis. The defense gene proteinase inhibitor (PIN2) was used as marker to compare plant responses. The Nr mutant showed a normal wounding response with PIN2 induction, but the def1 mutant did not. As expected, methyl JA (MeJA) treatment restored the normal wound response in the def1 mutant. Exogenous application of MeJA increased resistance to Helicoverpa zea, induced defense gene expression, and increased glandular trichome density on systemic leaves. Exogenous application of ethephon, which penetrates tissues and decomposes to ethylene, resulted in increased H. zea growth and interfered with the wounding response. Ethephon treatment also increased salicylic acid in systemic leaves. These results indicate that while JA plays the main role in systemic induced defense, ethylene acts antagonistically in this system to regulate systemic defense.

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Nr :

Never ripe mutant

def1 :

Defenseless 1 mutant


Rutgers wild-type plants of Nr mutant


Castlemart, wild-type plants of def1 mutant


Methyl jasmonate

PIN2 :

Protease inhibitor 2

ERF1 :

Ethylene response factor

PR1 :

Pathogenesis related gene


Polyphenol oxidase




Salicylic acid


  1. Abe H, Tomitaka Y, Shimoda T, Seo S, Sakurai T, Kugimiya S, Tsuda S, Kobayashi M (2011) Antagonistic plant defense system regulated by phytohormones assists interactions among vector insect, thrips, and a tospovirus. Plant Cell Physiol 10:1093

  2. Adie B, Chico JM, Rubio-Somoza I, Solano R (2007a) Modulation of plant defenses by ethylene. J Plant Growth Regul 26:160–177

  3. Adie B, Pérez-Pérez J, Pérez-Pérez MM, Godoy M, Sánchez-Serrano J-J, Schmelz EA, Solano R (2007b) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–1681

  4. Agrawal AA (1999) Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness. Ecology 80:1713–1723

  5. Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135:2025–2037

  6. An LZ, Xu XF, Tang HG, Zhang MX, Hou ZD, Liu YH, Zhao ZG, Feng HY, Xu SJ, Wang XL (2006) Ethylene production and 1-aminocyclopropane-1-carboxylate (ACC) synthase gene expression in tomato (Lycopersicon esculentum Mill.) leaves under enhanced UV-B radiation. J Integr Plant Biol 48:1190–1196

  7. Ankala A, Luthe DS, Williams WP, Wilkinson JR (2009) Integration of ethylene and jasmonic acid signaling pathways in the expression of maize defense protein Mir 1-CP. Mol Plant Microbe Interact 22:1555–1564

  8. Baldwin IT, Halitschke R, Kessler A, Schittko U (2001) Merging molecular and ecological approaches in plant-insect interactions. Curr Opin Plant Biol 4:351–358

  9. Beckers GJM, Spoel SH (2006) Fine-tuning plant defence signalling: Salicylate versus jasmonate. Plant Biol 8:1–10

  10. Bergey DR, Orozco-Cardenas M, de Moura DS, Ryan CA (1999) A wound- and systemin-inducible polygalacturonase in tomato leaves. Proc Natl Acad Sci USA 96:1756–1760

  11. Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29:23–32

  12. Bi JL, Murphy JB, Felton GW (1997) Antinutritive and oxidative components as mechanisms of induced resistance in cotton to Helicoverpa zea. J Chem Ecol 23:97–117

  13. Bodenhausen N, Reymond P (2007) Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol Plant Microbe Interact 20:1406–1420

  14. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580

  15. Boughton AJ, Hoover K, Felton GW (2005) Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J Chem Ecol 31:2211–2216

  16. Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205

  17. Campos ML, de Almeida M, Rossi ML, Martinelli AP, Litholdo 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 60:4346–4360

  18. Chandok MR, Ekengren SK, Martin GB, Klessig DF (2004) Suppression of pathogen-inducible NO synthase (iNOS) activity in tomato increases susceptibility to Pseudomonas syringae. Proc Natl Acad Sci USA 101:8239–8244

  19. Chen H, McCaig BC, Melotto M, He SY, Howe GA (2004) Regulation of plant arginase by wounding, jasmonate, and the phytotoxin coronatine. J Biol Chem 279:45998–46007

  20. Chippendale GM (1970) Metamorphic changes in fat body proteins of the southwestern corn borer, Diatraea grandiosella. J Insect Physiol 16:1057–1068

  21. Cole AB, Kiraly L, Lane LC, Wiggins BE, Ross K, Schoelz JE (2004) Temporal expression of PR-1 and enhanced mature plant resistance to virus infection is controlled by a single dominant gene in a new Nicotiana hybrid. Mol Plant Microbe Interact 17:976–985

  22. Cooper WR, Goggin FL (2005) Effects of jasmonate-induced defenses in tomato on the potato aphid, Macrosiphum euphorbiae. Entomologia Experimentalis et Applicata 115:107–115

  23. Diaz J, ten Have A, van Kan JAL (2002) The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiol 129:1341–1351

  24. Duffey SS (1986) Plant glandular trichomes: their partial role in defence against insects. In: Juniper BE, Southwood TE (eds) Insects and the plant surface. Arnold, London, pp 151–172

  25. Fan J, Hill L, Crooks C, Doerner P, Lamb C (2009) Abscisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiol 150:1750–1761

  26. Felton GW, Broadway RM, Duffey SS (1989) Inactivation of protease inhibitor activity by plant-derived quinones complications for host-plant resistance against noctuid herbivores. J Insect Physiol 35:981–990

  27. Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, Mathews MC, Murphy JB, Lamb C, Dixon RA (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr Biol 9:317–320

  28. Gfeller A, Liechti R, Farmer EE (2010) Arabidopsis jasmonate signaling pathway. Sci Signal 3: cm3

  29. Gibson S (2003) Ethylene inhibits trichome formation on stems and brancing on leaves. Int Conf 14:501707200

  30. Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT (2008) Shared signals—alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol Lett 11:24–34

  31. Harfouche AL, Shivaji R, Stocker R, Williams PW, Luthe DS (2006) Ethylene signaling mediates a maize defense response to insect herbivory. Mol Plant Microbe Interact 19:189–199

  32. Heinrich M, Baldwin IT, Wu J (2011) Two mitogen-activated protein kinase kinases, MKK1 and MEK2, are involved in wounding- and specialist lepidopteran herbivore Manduca sexta-induced responses in Nicotiana attenuata. J Exp Bot 62:4355–4365

  33. Horgan FG, Quiring DT, Lagnaoui A, Pelletier Y (2009) Effects of altitude of origin on trichome-mediated anti-herbivore resistance in wild Andean potatoes. Flora 204:49–62

  34. Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23:223–237

  35. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

  36. Huang Z, Yeakley JM, Garcia EW, Holdridge JD, Fan JB, Whitham SA (2005) Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiol 137:1147–1159

  37. Kahl J, Siemens DH, Aerts RJ, Gabler R, Kühnemann F, Preston CA, Baldwin IT (2000) Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–342

  38. Kang JH, Shi F, Jones AD, Marks MD, Howe GA (2010) Distortion of trichome morphology by the hairless mutation of tomato affects leaf surface chemistry. J Exp Bot 61:1053–1064

  39. Kazama H, Dan H, Imaseki H, Wasteneys GO (2004) Transient exposure to ethylene stimulates cell division and alters the fate and polarity of hypocotyl epidermal cells. Plant Physiol 134:1614–1623

  40. Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92:1769–1780

  41. Kniskern JM, Traw MB, Bergelson J (2007) Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Mol Plant Microbe Interact 20:1512–1522

  42. Koiwa H, Shade RE, Zhu-Salzman K, Subramanian L, Murdock LL, Nielsen SS, Bressan RA, Hasegawa PM (1998) Phage display selection can differentiate insecticidal activity of soybean cystatins. Plant J 14:371–379

  43. Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RAM, Ritsema T, Pieterse CMJ (2009) Ethylene modulates the role of NPR1 in cross-talk between salicylate and jasmonate signaling. Plant Physiol 108:133926

  44. Li L, Zhao YF, McCaig BC, Wingerd BA, Wang JH, Whalon ME, Pichersky E, Howe GA (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16:126–143

  45. Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178

  46. Mantelin S, Kishor KB, Isgouhi K (2009) Ethylene contributes to potato aphid susceptibility in a compatible tomato host. New Phytol 183:444–456

  47. Martinez de Ilarduya O, Xie Q, Kaloshian I (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol Plant Microbe Interact 16:699–708

  48. McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defense Arabidopsis. Proc Natl Acad Sci USA 94:5473–5477

  49. Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng WQ, Thines B, Staswick P, Browse J, Howe GA, He SY (2008) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1F-box protein. Plant J 55:979–988

  50. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

  51. Navarro L (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

  52. O’Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917

  53. Onate-Sanchez L, Anderson JP, Young J, Singh KB (2007) AtERF14, a member of the ERF family of transcription factors plays a nonredundant role in plant defense. Plant Physiol 143:400–409

  54. Onkokesung N, Galis I, von Dahl CC, Matsuoka K, Saluz H-P, Baldwin IT (2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated herbivory in Nicotiana attenuata leaves. Plant Physiol 153:785–798

  55. Peiffer M, Felton GW (2005) The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in larval Helicoverpa zea. Arch Insect Biochem Physiol 58:106–113

  56. Peiffer M, Tooker JF, Luthe DS, Felton GW (2009) Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184:644–656

  57. Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569

  58. Pieterse CM, van Wees SC, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

  59. Plett JM, Mathur J, Regan S (2009) Ethylene receptor ETR2 controls trichome branching by regulating microtubule assembly in Arabidopsis thaliana. J Exp Bot 60:3923–3933

  60. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G (2011) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158(2):854–863

  61. Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–720

  62. Rojo E, León J, Sánchez-Serrano JJ (1999) Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20:135–142

  63. Rotenberg D, Thompson TS, German TL, Willis DK (2006) Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. J Virological Meth 138:49–59

  64. Schmelz EA, Engelberth J, Alborn HT, O’Donnell P, Sammons M, Toshima H, Tumlinson JH 3rd (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Natl Acad Sci USA 100:10552–10557

  65. Shoji T, Nakajima K, Hashimoto T (2000) Ethylene suppresses jasmonate-induced gene expression in nicotine biosynthesis. Plant Cell Physiol 41:1072–1076

  66. Stotz HU, Pittendrigh BR, Kroymann J, Weniger K, Fritsche J, Bauke A, Mitchell-Olds T (2000) Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol 124:1007–1017

  67. Thaler JS, Agrawal AA, Halitschke R (2010) Salicylate-mediated interactions between pathogens and herbivores. Ecology 91:1075–1082

  68. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal cross-talk. Trends Plant Sci 17:260–270

  69. Thipyapong P, Steffens JC (1996) Defensive role of polyphenol oxidases against Pseudomonas syringae pv tomato. Plant Physiol 111:791

  70. Tian D, Peiffer M, Shoemaker E, Tooker J, Haubruge E, Francis F, Luthe DS, Felton GW (2012a) Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS ONE 7:e36168

  71. Tian D, Tooker J, Peiffer M, Chung S, Felton G (2012b) Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta 236:1053–1066

  72. Tooker JF, De Moraes CM (2005) Jasmonate in lepidopteran eggs and neonates. J Chem Ecol 31:2753–2759

  73. Tornero P, Gadea J, Conejero V, Vera P (1997) Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis-related gene during the hypersensitive response and development. Mol Plant Microbe Interact 10:624–634

  74. Traw MB, Bergelson J (2003) Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiol 133:1367–1375

  75. van Poecke RMP, Dicke M (2002) Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. J Exp Bot 53:1793–1799

  76. van Schie CCN, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol 64:251–263

  77. Vankan JAL, Cozijnsen T, Danhash N, Dewit P (1995) Induction of tomato stress protein mRNAs by ethephon, 2,6-dichloroisonicotinic acid and salicylate. Plant Mol Biol 27:1205–1213

  78. Vera P, Conejero V (1990) Effect of ethephon on protein degradation and the accumulation of ‘pathogenesis-related’ (PR) proteins in tomato leaf discs. Plant Physiol 92:227–233

  79. Verhage A, van Wees SCM, Pieterse CMJ (2010) Plant immunity: it’s the hormones talking, but what do they say? Plant Physiol 154:536–540

  80. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

  81. Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I, Miersch O (2006) The wound response in tomato—role of jasmonic acid. J Plant Physiol 163:297–306

  82. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189

  83. Yasuda M, Nakashita H, Hasegawa S, Nishioka M, Arai Y, Uramoto M, Yamaguchi I, Yoshida S (2003) N-cyanomethyl-2-chloroisonicotinamide induces systemic acquired resistance in Arabidopsis without salicylic acid accumulation. Biosci Biotechnol Biochem 67:322–328

  84. Zhang Y, Xu S, Ding P, Wang D, Cheng YT, He J, Gao M, Xu F, Li Y, Zhu Z, Li X, Zhang Y (2010) Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci USA 107:18220–18225

  85. Zhang L, Jia C, Liu L, Zhang Z, Li C, Wang Q (2011) The involvement of jasmonates and ethylene in Alternaria alternata f. sp. lycopersici toxin-induced tomato cell death. J Exp Bot 62:5405–5418

  86. Zhao Y (2003) Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485–499

  87. Zhu-Salzman K, Salzman RA, Koiwa H, Murdock LL, Bressan RA, Hasegawa PM (1998) Ethylene negatively regulates local expression of plant defense lectin genes. Physiologia Plantarum 104:365–372

  88. Zsogon A, Lambais MR, Benedito VA, Figueira AVD, Peres LEP (2008) Reduced arbuscular mycorrhizal colonization in tomato ethylene mutants. Scientia Agricola 65:259–267

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Dawn S. Luthe reviewed an earlier draft of the manuscript and provided helpful criticism. The work was supported in part by the United States Department of Agriculture–Agricultural and Food Research Initiative grant 2011-67013-30352.

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Correspondence to Gary W. Felton.

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Tian, D., Peiffer, M., De Moraes, C.M. et al. Roles of ethylene and jasmonic acid in systemic induced defense in tomato (Solanum lycopersicum) against Helicoverpa zea . Planta 239, 577–589 (2014).

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  • Methyl jasmonate
  • Ethephon
  • Induced systemic defense
  • Insect herbivore
  • Trichomes
  • Proteinase inhibitor
  • Hormones
  • Jasmonic acid
  • Salicylic acid