Synergism in the effect of prior jasmonic acid application on herbivore-induced volatile emission by Lima bean plants: Transcription of a monoterpene synthase gene and volatile emission

Journal of Experimental Botany

Volumn 65, Issue 17, 2014, Pages 4821-4831

  Menzel, Tila R ^a   Weldegergis, Berhane T ^a   David, Anja ^b   Boland, Wilhelm ^b   Gols, Rieta ^a   Van Loon, Joop J A ^a   Dicke, Marcel ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Herbivore induced plant volatiles; Induced plant defence; Mite plant interactions; Phytohormones; Plant memory; Priming; Terpene synthase

Indexed keywords

PHASEOLUS LUNATUS;

ALKENE; BETA-OCIMENE; CYCLOPENTANE DERIVATIVE; ISOMERASE; JASMONIC ACID; OXYLIPIN; PHYTOHORMONE; PINENE CYCLASE I; TERPENE; VEGETABLE PROTEIN;

ANIMAL; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HERBIVORY; METABOLISM; PHASEOLUS; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TETRANYCHIDAE;

ALKENES; ANIMALS; CYCLOPENTANES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, PLANT; HERBIVORY; INTRAMOLECULAR LYASES; OXYLIPINS; PHASEOLUS; PLANT GROWTH REGULATORS; PLANT PROTEINS; POLYMERASE CHAIN REACTION; TERPENES; TETRANYCHIDAE;

EID: 84907416271     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru242     Document Type: Article

References (73)

1. 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 Physiology 135, 2025-2037.
2. Arimura GI, Köpke S, Kunert M, Volpe V, David A, Brand P, Dabrowska P, Maffei ME, Boland W. 2008. Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiology 146, 965-973.
3. Arimura GI, Ozawa R, Kugimiya S, Takabayashi J, Bohlmann J. 2004. Herbivore-induced defense response in a model legume. Twospotted spider mites induce emission of (E)-ocimene and transcript accumulation of (E)-ocimene synthase in Lotus japonicus. Plant Physiology 135, 1976-1983.
4. Arimura GI, Ozawa R, Nishioka T, Boland W, Koch T, Kühnemann F, Takabayashi J. 2002. Herbivore-induced volatiles induce the emission of ethylene in neighboring Lima bean plants. Plant Journal 29, 87-98.
5. Arimura GI, Ozawa R, Shimoda T, Nishloka T, Boland W, Takabayashi J. 2000. Herbivory-induced volatiles elicit defence genes in Lima bean leaves. Nature 406, 512-515.
6. Blechert S, Brodschelm W, Holder S, Kammerer L, Kutchan TM, Mueller MJ, Xia ZQ, Zenk MH. 1995. The octadecanoic pathway: Signal molecules for the regulation of secondary pathways. Proceedings of the National Academy of Sciences, USA 92, 4099-4105.
7. Boland W, Gäbler A. 1989. Biosynthesis of homoterpenes in higher plants. Helvetica Chimica Acta 72, 247-253.
8. Boter M, Ruíz-Rivero O, Abdeen A, Prat S. 2004. Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes and Development 18, 1577-1591.
9. Brader G, Tas É, Palva ET. 2001. Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiology 126, 849-860.
10. Bruinsma M, IJdema H, Van Loon JJA, Dicke M. 2008. Differential effects of jasmonic acid treatment of Brassica nigra on the attraction of pollinators, parasitoids, and butterflies. Entomologia Experimentalis et Applicata 128, 109-116.
11. Bruinsma M, Pang B, Mumm R, Van Loon JJA, Dicke M. 2009a. Comparing induction at an early and late step in signal transduction mediating indirect defence in Brassica oleracea. Journal of Experimental Botany 60, 2589-2599.
12. Bruinsma M, Posthumus MA, Mumm R, Mueller MJ, Van Loon JJA, Dicke M. 2009b. Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: Effects of time and dose, and comparison with induction by herbivores. Journal of Experimental Botany 60, 2575-2587.
13. Bruinsma M, van Broekhoven S, Poelman EH, Posthumus MA, Müller MJ, van Loon JJA, Dicke M. 2010. Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects. Oecologia 162, 393-404.
14. Chini A, Fonseca S, Fernández G et al. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666-671.
15. Conrath U. 2009. Priming of induced plant defense responses. Plant Innate Immunity 51, 361-395.
16. Cooper WR, Jia L, Goggin L. 2005. Effects of jasmonate-induced defenses on root-knot nematode infection of resistant and susceptible tomato cultivars. Journal of Chemical Ecology 31, 1953-1967.
17. De Boer JG, Dicke M. 2004. The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. Journal of Chemical Ecology 30, 255-271.
18. De Boer JG, Hordijk CA, Posthumus MA, Dicke M. 2008. Prey and non-prey arthropods sharing a host plant: Effects on induced volatile emission and predator attraction. Journal of Chemical Ecology 34, 281-290.
19. De Boer JG, Posthumus MA, Dicke M. 2004. Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. Journal of Chemical Ecology 30, 2215-2230.
20. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH. 1998. Hervibore-infested plants selectively attract parasitoids. Nature 393, 570-573.
21. De Vos M, Van Oosten VR, Van Poecke RMP et al. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions 18, 923-937.
22. Dicke M, Gols R, Ludeking D, Posthumus MA. 1999. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. Journal of Chemical Ecology 25, 1907-1922.
23. Dicke M, Van Beek TA, Posthumus MA, Ben Dom N, Van Bokhoven H, De Groot A. 1990. Isolation and identification of volatile kairomone that affects acarine predator-prey interactions Involvement of host plant in its production. Journal of Chemical Ecology 16, 381-396.
24. Dicke M, Van Loon JJA, Soler R. 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nature Chemical Biology 5, 317-324.
25. Dicke M, Vet LEM. 1999. Plant-carnivore interactions: Evolutionary and ecological consequences for plant, herbivore and carnivore. In: Olff H, Brown VK, Drent RH, eds. Herbivores: Between Plants and Predators. Oxford: Blackwell Science, 483-520.
26. Frost CJ, Mescher MC, Carlson JE, De Moraes CM. 2008. Plant defense priming against herbivores: Getting ready for a different battle. Plant Physiology 146, 818-824.
27. Gols R, Posthumus MA, Dicke M. 1999. Jasmonic acid induces the production of gerbera volatiles that attract the biological control agent Phytoseiulus persimilis. Entomologia Experimentalis et Applicata 93, 77-86.
28. Gols R, Roosjen M, Dijkman H, Dicke M. 2003. Induction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation. Journal of Chemical Ecology 29, 2651-2666.
29. Hare JD. 2010. Ontogeny and season constrain the production of herbivore-inducible plant volatiles in the field. Journal of Chemical Ecology 36, 1363-1374.
30. Heil M, Baldwin IT. 2002. Fitness costs of induced resistance: Emerging experimental support for a slippery concept. Trends in Plant Science 7, 61-67.
31. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT. 2009. Priming in systemic plant immunity. Science 324, 89-91.
32. Kegge W, Weldegergis BT, Soler R, Eijk MVV, Dicke M, Voesenek LACJ, Pierik R. 2013. Canopy light cues affect emission of constitutive and methyl jasmonate-induced volatile organic compounds in Arabidopsis thaliana. New Phytologist 200, 861-874.
33. Kempema LA, Cui X, Holzer FM, Walling LL. 2007. Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiology 143, 849-865.
34. Kessler A, Baldwin IT. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141-2144.
35. Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: The emerging molecular analysis. Annual Review of Plant Biology , 53, 299-328.
36. Koch T, Krumm T, Jung V, Engelberth J, Boland W. 1999. Differential induction of plant volatile biosynthesis in the lima bean by early and late intermediates of the octadecanoid-signaling pathway. Plant Physiology 121, 153-162.
37. Kohler A, Schwindling S, Conrath U. 2002. Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiology 128, 1046-1056.
38. Koo AJK, Gao X, Daniel Jones A, Howe GA. 2009. A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant Journal 59, 974-986.
39. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CMJ. 2008. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiology 147, 1358-1368.
40. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-δδCT method. Methods 25, 402-408.
41. Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R. 2004. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16, 1938-1950.
42. McConn M, Creelman RA, Bell E, Mullet JE, Browse J. 1997. Jasmonate is essential for insect defense in Arabidopsis. Proceedings of the National Academy of Sciences, USA 94, 5473-5477.
43. Mithöfer A, Boland W. 2008. Recognition of herbivory-associated molecular patterns. Plant Physiology 146, 825-831.
44. Moayeri HRS, Ashouri A, Poll L, Enkegaard A. 2007. Olfactory response of a predatory mirid to herbivore induced plant volatiles: Multiple herbivory vs. single herbivory. Journal of Applied Entomology 131, 326-332.
45. Mumm R, Dicke M. 2010. Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Canadian Journal of Zoology 88, 628-667.
46. Muroi A, Ramadan A, Nishihara M, Yamamoto M, Ozawa R, Takabayashi J, Arimura GI. 2011. The composite effect of transgenic plant volatiles for acquired immunity to herbivory caused by inter-plant communications. PLoS ONE 6, e24594.
47. Omer AD, Thaler JS, Granett J, Karban R. 2000. Jasmonic acid induced resistance in grapevines to a root and leaf feeder. Journal of Economic Entomology 93, 840-845.
48. Ozawa R, Arimura GI, Takabayashi J, Shimoda T, Nishioka T. 2000. Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant and Cell Physiology 41, 391-398.
49. Ozawa R, Shiojiri K, Sabelis MW, Arimura GI, Nishioka T, Takabayashi J. 2004. Corn plants treated with jasmonic acid attract more specialist parasitoids, thereby increasing parasitization of the common armyworm. Journal of Chemical Ecology 30, 1797-1808.
50. Paré PW, Tumlinson JH. 1999. Plant volatiles as a defense against insect herbivores. Plant Physiology 121, 325-331.
51. Perazzolli M, Roatti B, Bozza E, Pertot I. 2011. Trichoderma harzianum T39 induces resistance against downy mildew by priming for defense without costs for grapevine. Biological Control 58, 74-82.
52. Pieterse CMJ, Dicke M. 2007. Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends in Plant Science 12, 564-569.
53. Ponzio C, Gols R, Pieterse CMJ, Dicke M. 2013. Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Functional Ecology 27, 587-598.
54. Ryan CA. 2000. The systemin signaling pathway: Differential activation of plant defensive genes. Biochimica et Biophysica Acta - Protein Structure and Molecular Enzymology 1477, 112-121.
55. Schmelz EA, Alborn HT, Banchio E, Tumlinson JH. 2003. Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory. Planta 216, 665-673.
56. Schulze B, Lauchli R, Sonwa MM, Schmidt A, Boland W. 2006. Profiling of structurally labile oxylipins in plants by in situ derivatization with pentafluorobenzyl hydroxylamine. Analytical Biochemistry 348, 269-283.
57. Snoeren TAL, van Poecke RMP, Dicke M. 2009. Multidisciplinary approach to unravelling the relative contribution of different oxylipins in indirect defense of Arabidopsis thaliana. Journal of Chemical Ecology 35, 1021-1031.
58. Stout MJ, Workman KV, Bostock RM, Duffey SS. 1998. Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113, 74-81.
59. Takabayashi J, Takahashi S, Dicke M, Posthumus MA. 1995. Developmental stage of herbivore Pseudaletia separata affects production of herbivore-induced synomone by corn plants. Journal of Chemical Ecology 21, 273-287.
60. Thaler JS, Humphrey PT, Whiteman NK. 2012. Evolution of jasmonate and salicylate signal crosstalk. Trends in Plant Science 17, 260-270.
61. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J. 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661-665.
62. Thulke O, Conrath U. 1998. Salicylic acid has a dual role in the activation of defence-related genes in parsley. Plant Journal 14, 35-42.
63. Tierranegra-García N, Salinas-Soto P, Torres-Pacheco I et al. 2011. Effect of foliar salicylic acid and methyl jasmonate applications on protection against pill-bugs in lettuce plants (Lactuca sativa). Phytoparasitica 39, 137-144.
64. Van Hulten M, Pelser M, Van Loon LC, Pieterse CMJ, Ton J. 2006. Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences, USA 103, 5602-5607.
65. Van Poecke RMP, Dicke M. 2002. Induced parasitoid attraction by Arabidopsis thaliana: Involvement of the octadecanoid and the salicylic acid pathway. Journal of Experimental Botany 53, 1793-1799.
66. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome biology 3.
67. Walters DR, Paterson L, Walsh DJ, Havis ND. 2008. Priming for plant defense in barley provides benefits only under high disease pressure. Physiological and Molecular Plant Pathology 73, 95-100.
68. Wentzell AM, Kliebenstein DJ. 2008. Genotype, age, tissue, and environment regulate the structural outcome of glucosinolate activation. Plant Physiology 147, 415-429.
69. Worrall D, Holroyd GH, Moore JP, Glowacz M, Croft P, Taylor JE, Paul ND, Roberts MR. 2012. Treating seeds with activators of plant defence generates long-lasting priming of resistance to pests and pathogens. New Phytologist 193, 770-778.
70. Yamada S, Kano A, Tamaoki D, Miyamoto A, Shishido H, Miyoshi S, Taniguchi S, Akimitsu K, Gomi K. 2012. Involvement of OsJAZ8 in jasmonate-induced resistance to bacterial blight in rice. Plant and Cell Physiology 53, 2060-2072.
71. Zhang PJ, Zheng SJ, Van Loon JJA, Boland W, David A, Mumm R, Dicke M. 2009a. Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proceedings of the National Academy of Sciences, USA 106, 21202-21207.
72. Zhang S, Yang X, Sun M, Sun F, Deng S, Dong H. 2009b. Riboflavininduced priming for pathogen defense in Arabidopsis thaliana. Journal of Integrative Plant Biology 51, 167-174.
73. Zheng SJ, Van Dijk JP, Bruinsma M, Dicke M. 2007. Sensitivity and speed of induced defense of cabbage (Brassica oleracea L.): Dynamics of BoLOX expression patterns during insect and pathogen attack. Molecular Plant-Microbe Interactions 20, 1332-1345.