Signal Transduction in Plant–Insect Interactions: From Membrane Potential Variations to Metabolomics

  • Simon Atsbaha Zebelo
  • Massimo E. Maffei


Upon herbivore attack plants react with a cascade of signals. Early events are represented by ion flux unbalances that eventually lead to plasma transmembrane potential (Vm) variations. These events are triggered by mechanical wounding implicated by chewing/piercing herbivores along with the injection of oral secretions (OS) containing plant response effectors and elicitors. Vm depolarization has been found to be a common event when plants interact with different biotrophs, and to vary depending on type and feeding habit of the biotroph. Here we show recent advances of internal and external signal transduction in plant-insect interactions by analyzing the differential impact of mechanical and herbivore damage on plants. Vm variations, calcium signaling, and ROS production precede the late events represented by gene expression, proteomics, and metabolomics. Transcriptomics allows to decipher genomic expression following Vm variations and signaling upon herbivory; proteomics helps to understand the biological function of expressed genes, whereas metabolomics gives feedbacks on the combined action of gene expression and protein synthesis, by showing the complexity of plant responses through synthesis of direct and indirect plant defense molecules. The practical application of modern methods starting from signal transduction to metabolic responses to insect herbivory are discussed and documented.


Jasmonic Acid Mechanical Wounding Insect Herbivory Colorado Potato Beetle Lima Bean 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Adie B, Chico JM, Rubio-Somoza I, Solano R (2007) Modulation of plant defenses by ethylene. J Plant Growth Regul 26:160–177Google Scholar
  2. Afzal AJ, Natarajan A, Saini N, Iqbal MJ, Geisler M, El Shemy HA, Mungur R et al (2009) The nematode resistance allele at the rhg1 locus alters the proteome and primary metabolism of soybean roots. Plant Physiol 151:1264–1280PubMedGoogle Scholar
  3. Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:873–879Google Scholar
  4. Arimura G, Maffei ME (2010) Calcium and secondary CPK signaling in plants in response to herbivore attack. Biochem Biophys Res Commun 400:455–460PubMedGoogle Scholar
  5. Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabyashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515PubMedGoogle Scholar
  6. Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta Mol Cell Biol Lipids 1734:91–111Google Scholar
  7. Arimura GI, Ozawa R, Maffei ME (2011) Recent advances in plant early signaling in response to herbivory. Int J Mol Sci 12:3723–3739PubMedGoogle Scholar
  8. Baldwin IT (2010) Plant volatiles. Curr Biol 20:R392–R397PubMedGoogle Scholar
  9. Baluska F, Mancuso S, Volkmann D, Barlow P (2004) Root apices as plant command centres: the unique ‘brain-like’ status of the root apex transition zone. Biologia 59:7–19Google Scholar
  10. Bede JC, Musser RO, Felton GW, Korth KL (2006) Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol Biol 60:519–531PubMedGoogle Scholar
  11. Berenbaum MR, Zangerl AR (1996) Phytochemical diversity: adaptation or random variation? In: Romeo JT, Saunders IA, Barbosa P (eds) Phytochemical diversity and redundancy in ecological interactions. Plenum Press, New YorkGoogle Scholar
  12. Bodenhausen N, Reymond P (2007) Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol Plant Microbe Interact 20:1406–1420PubMedGoogle Scholar
  13. Bonaventure G, VanDoorn A, Baldwin IT (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci 16:294–299PubMedGoogle Scholar
  14. Bos JIB, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet 6:e1001216PubMedGoogle Scholar
  15. Boter M, Amigues B, Peart J, Breuer C, Kadota Y, Casais C, Moore G et al (2007) Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity. Plant Cell 19:3791–3804PubMedGoogle Scholar
  16. Bricchi I, Leitner M, Foti M, Mithofer A, Boland W, Maffei ME (2010) Robotic mechanical wounding (mecworm) versus herbivore-induced responses: early signaling and volatile emission in lima bean (Phaseolus lunatus L.). Planta 232:719–729PubMedGoogle Scholar
  17. Bundy JG, Davey MP, Viant MR (2009) Environmental metabolomics: a critical review and future perspectives. Metabolomics 5:3–21Google Scholar
  18. Castells E, Berhow MA, Vaughn SF, Berenbaum MR (2005) Geographic variation in alkaloid production in Conium maculatum populations experiencing differential herbivory by Agonopterix alstroemeriana. J Chem Ecol 31:1693–1709PubMedGoogle Scholar
  19. Chen YZ, Pang QY, Dai SJ, Wang Y, Chen SX, Yan XF (2011) Proteomic identification of differentially expressed proteins in Arabidopsis in response to methyl jasmonate. J Plant Physiol 168:995–1008PubMedGoogle Scholar
  20. Collins RM, Afzal M, Ward DA, Prescott MC, Sait SM, Rees HH, Tomsett A (2010) Differential proteomic analysis of Arabidopsis thaliana genotypes exhibiting resistance or susceptibility to the insect herbivore, Plutella xylostella. PLoS ONE 5Google Scholar
  21. Cummins I, Dixon DP, Freitag-Pohl S, Skipsey M, Edwards R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43:266–280PubMedGoogle Scholar
  22. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedGoogle Scholar
  23. Diezel C, Kessler D, Baldwin IT (2011) Pithy protection: Nicotiana attenuata’s jasmonic acid-mediated defenses are required to resist stem-boring weevil larvae. Plant Physiol 155:1936–1946PubMedGoogle Scholar
  24. Dinkins CLP, Peterson RKD, Gibson JE, Hu Q, Weaver DK (2008) Glycoalkaloid responses of potato to Colorado potato beetle defoliation. Food Chem Toxicol 46:2832–2836Google Scholar
  25. Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338–350PubMedGoogle Scholar
  26. Duclohier H, Alder G, Kociolek K, Leplawy MT (2003) Channel properties of template assembled alamethicin tetramers. J Pept Sci 9:776–783PubMedGoogle Scholar
  27. Dudareva N, Pichersky E (2008) Metabolic engineering of plant volatiles. Curr Opin Biotechnol 19:181–189PubMedGoogle Scholar
  28. Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440Google Scholar
  29. Dugravot S, Thibout E, Abo-Ghalia A, Huignard J (2004) How a specialist and a non-specialist insect cope with dimethyl disulfide produced by Allium porrum. Entomol Exp Appl 113:173–179Google Scholar
  30. Ebel J, Mithöfer A (1998) Early events in the elicitation of plant defence. Planta 206:335–348Google Scholar
  31. Engelberth J, Seidl-Adams I, Schultz JC, Tumlinson JH (2007) Insect elicitors and exposure to green leafy volatiles differentially upregulate major octadecanoids and transcripts of 12-oxo phytodienoic acid reductases in Zea mays. Mol Plant Microbe Interact 20:707–716PubMedGoogle Scholar
  32. Felton GW, Korth KL (2000) Trade-offs between pathogen and herbivore resistance. Curr Opin Plant Biol 3:309–314PubMedGoogle Scholar
  33. Feng ZL, Liu RS, DeAngelis DL, Bryant JP, Kielland K, Stuart Chapin F, Swihart R (2009) Plant toxicity, adaptive herbivory, and plant community dynamics. Ecosystems 12:534–547Google Scholar
  34. Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D et al (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–715PubMedGoogle Scholar
  35. Ferry N, Stavroulakis S, Guan WZ, Davison GM, Bell HA, Weaver RJ, Down RE et al (2011) Molecular interactions between wheat and cereal aphid (Sitobion avenae): analysis of changes to the wheat proteome. Proteomics 11:1985–2002PubMedGoogle Scholar
  36. Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257PubMedGoogle Scholar
  37. Gao LL, Kamphuis LG, Kakar K, Edwards OR, Udvardi MK, Singh KB (2010) Identification of potential early regulators of aphid resistance in Medicago truncatula via transcription factor expression profiling. New Phytol 186:980–994PubMedGoogle Scholar
  38. Gilardoni PA, Schuck S, Jungling R, Rotter B, Baldwin IT, Bonaventure G (2010) SuperSAGE analysis of the Nicotiana attenuata transcriptome after fatty acid-amino acid elicitation (FAC): identification of early mediators of insect responses. BMC Pediatrics 10:66 Google Scholar
  39. Giordanengo P, Brunissen L, Rusterucci C, Vincent C, van Bel A, Dinant S, Girousse C et al (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. C R Biol 333:516–523PubMedGoogle Scholar
  40. Giri AP, Wunsche H, Mitra S, Zavala JA, Muck A, Svatos A, Baldwin IT (2006) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VII. Changes in the plant’s proteome. Plant Physiol 142:1621–1641PubMedGoogle Scholar
  41. Hagel JM, Facchini PJ (2008) Plant metabolomics: analytical platforms and integration with functional genomics. Phytochem Rev 7:479–497Google Scholar
  42. Heil M, Silva Bueno JC (2007) Within-plant signalling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci U S A 104:5467–5472PubMedGoogle Scholar
  43. Heil M, Lion U, Boland W (2008) Defense-inducing volatiles: in search of the active motif. J Chem Ecol 34:601–604PubMedGoogle Scholar
  44. Hilker M, Meiners T (2006) Early herbivore alert: insect eggs induce plant defense. J Chem Ecol 32:1379–1397PubMedGoogle Scholar
  45. Hilker M, Meiners T (2010) How do plants “notice” attack by herbivorous arthropods? Biol Rev 85:267–280PubMedGoogle Scholar
  46. Hilker M, Stein C, Schroder R, Varama M, Mumm R (2005) Insect egg deposition induces defence responses in Pinus sylvestris: characterisation of the elicitor. J Exp Biol 208:1849–1854PubMedGoogle Scholar
  47. Horiuchi J-I, Muroi A, Takabayashi J, Nishioka T (2007) Exposing Arabidopsis seedlings to borneol and bornyl acetate affects root growth: specificity due to the chemical and optical structures of the compounds. J Plant Interact 2:101–104Google Scholar
  48. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66PubMedGoogle Scholar
  49. Jansen JJ, Allwood JW, Marsden-Edwards E, van der Putten WH, Goodacre R, van Dam NM (2009) Metabolomic analysis of the interaction between plants and herbivores. Metabolomics 5:150–161Google Scholar
  50. Kanchiswamy CN, Muroi A, Maffei ME, Yoshioka H, Sawasaki T, Arimura G (2010) Ca2+-dependent protein kinases and their substrate HsfB2a are differently involved in the heat response signaling pathway in Arabidopsis. Plant Biotechnol 27:469–473Google Scholar
  51. Kant MR, Baldwin IT (2007) The ecogenetics and ecogenomics of plant-herbivore interactions: rapid progress on a slippery road. Curr Opin Genet Dev 17:519–524PubMedGoogle Scholar
  52. Klusener B, Weiler EW (1999) Pore-forming properties of elicitors of plant defense reactions and cellulolytic enzymes. FEBS Lett 459:263–266PubMedGoogle Scholar
  53. Koo AJK, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-l-isoleucine. Proc Natl Acad Sci U S A 108:9298–9303PubMedGoogle Scholar
  54. Kopke D, Beyaert I, Gershenzon J, Hilker M, Schmidt A (2010) Species-specific responses of pine sesquiterpene synthases to sawfly oviposition. Phytochemistry 71:909–917PubMedGoogle Scholar
  55. Kroymann J (2011) Natural diversity and adaptation in plant secondary metabolism. Curr Opin Plant Biol 14:246–251PubMedGoogle Scholar
  56. Kuzina V, Ekstrom CT, Andersen SB, Nielsen JK, Olsen CE, Bak S (2009) Identification of defense compounds in Barbarea vulgaris against the herbivore Phyllotreta nemorum by an ecometabolomic approach. Plant Physiol 151:1977–1990PubMedGoogle Scholar
  57. Lambdon PW, Hassall M (2005) How should toxic secondary metabolites be distributed between the leaves of a fast-growing plant to minimize the impact of herbivory? Funct Ecol 19:299–305Google Scholar
  58. Lawrence SD, Dervinis C, Novak N, Davis JM (2006) Wound and insect herbivory responsive genes in poplar. Biotechnol Lett 28:1493–1501PubMedGoogle Scholar
  59. Liu LL, Zhang J, Zhang YF, Li YC, Xi JH, Li SY (2010) Proteomic analysis of differentially expressed proteins of Arabidopsis thaliana response to specialist herbivore Plutella xylostella. Chem Res Chin Univ 26:958–963Google Scholar
  60. Lühring H, Nguyen VD, Schmidt L, Roese US (2007) Caterpillar regurgitant induces pore formation in plant membranes. FEBS Lett 581:5361–5370PubMedGoogle Scholar
  61. Macel M, van Dam NM, Keurentjes JJB (2010) Metabolomics: the chemistry between ecology and genetics. Mol Ecol Res 10:583–593Google Scholar
  62. Macias FA, Molinillo JMG, Varela RM, Galindo JCG (2007) Allelopathy—a natural alternative for weed control. Pest Manage Sci 63:327–348Google Scholar
  63. Maffei ME (2010) Sites of synthesis, biochemistry and functional role of plant volatiles. S Afr J Bot 76:612–631Google Scholar
  64. Maffei M, Bossi S (2006) Electrophysiology and plant responses to biotic stress. In: Volkov A (ed) Plant electrophysiology—theory and methods. Springer, BerlinGoogle Scholar
  65. Maffei M, Bossi S, Spiteller D, Mithöfer A, Boland W (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol 134:1752–1762PubMedGoogle Scholar
  66. Maffei ME, Mithofer A, Arimura GI, Uchtenhagen H, Bossi S, Bertea CM, Cucuzza LS et al (2006) Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol 140:1022–1035PubMedGoogle Scholar
  67. Maffei ME, Mithofer A, Boland W (2007a) Before gene expression: early events in plant-insect interaction. Trends Plant Sci 12:310–316PubMedGoogle Scholar
  68. Maffei ME, Mithofer A, Boland W (2007b) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68:2946–2959PubMedGoogle Scholar
  69. Maffei ME, Gertsch J, Appendino G (2011) Plant volatiles: production, function and pharmacology. Nat Prod Rep 28:1359–1380PubMedGoogle Scholar
  70. Maischak H, Grigoriev PA, Vogel H, Boland W, Mithofer A (2007) Oral secretions from herbivorous lepidopteran larvae exhibit ion channel-forming activities. FEBS Lett 581:898–904PubMedGoogle Scholar
  71. Maserti BE, Del Carratore R, la Croce CM, Podda A, Migheli Q, Froelicher Y, Luro F et al (2011) Comparative analysis of proteome changes induced by the two spotted spider mite Tetranychus urticae and methyl jasmonate in citrus leaves. J Plant Physiol 168:392–402PubMedGoogle Scholar
  72. Masi E, Ciszak M, Stefano G, Renna L, Azzarello E, Pandolfi C, Mugnai S et al (2009) Spatiotemporal dynamics of the electrical network activity in the root apex. Proc Natl Acad Sci U S A 106:4048–4053PubMedGoogle Scholar
  73. Matsumura H, Ito A, Saitoh H, Winter P, Kahl G, Reuter M, Kruger DH et al (2005) Supersage. Cell Microbiol 7:11–18PubMedGoogle Scholar
  74. Mcainsh MR, Gray JE, Hetherington AM, Leckie CP, Ng C (2000) Ca2+ signalling in stomatal guard cells. Biochem Soc Trans 28:476–481PubMedGoogle Scholar
  75. McLean S, Duncan AJ (2006) Pharmacological perspectives on the detoxification of plant secondary metabolites: implications for ingestive behavior of herbivores. J Chem Ecol 32:1213–1228PubMedGoogle Scholar
  76. Meldau S, Baldwin IT, Wu JQ (2011) SGT1 regulates wounding- and herbivory-induced jasmonic acid accumulation and Nicotiana attenuata’s resistance to the specialist lepidopteran herbivore Manduca sexta. New Phytol 189:1143–1156PubMedGoogle Scholar
  77. Memelink J (2009) Regulation of gene expression by jasmonate hormones. Phytochemistry 70:1560–1570PubMedGoogle Scholar
  78. Mithöfer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146:825–831PubMedGoogle Scholar
  79. 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 137:1160–1168PubMedGoogle Scholar
  80. Mithöfer A, Boland W, Maffei ME (2009a) Chemical ecology of plant-insect interactions. In: Parker J (ed) Molecular aspects of plant disease resistance. Wiley-Blackwell, ChirchesterGoogle Scholar
  81. Mithöfer A, Mazars C, Maffei M (2009b) Probing spatio-temporal intracellular calcium variations in plants. In: Pfannschmidt T (ed) Plant signal transduction. Humana Press Inc., TotowaGoogle Scholar
  82. Musser RO, Farmer E, Peiffer M, Williams SA, Felton GW (2006) Ablation of caterpillar labial salivary glands: technique for determining the role of saliva in insect-plant interactions. J Chem Ecol 32:981–992PubMedGoogle Scholar
  83. Olson DM, Davis RF, Wackers FL, Rains GC, Potter T (2008) Plant-herbivore-carnivore interactions in cotton, Gossypium hirsutum: linking belowground and aboveground. J Chem Ecol 34:1341–1348PubMedGoogle Scholar
  84. Onkokesung N, Galis I, von Dahl CC, Matsuoka K, Saluz HP, Baldwin IT (2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated herbivory in Nicotiana attenuata leaves. Plant Physiol 153:785–798PubMedGoogle Scholar
  85. Oyarce P, Gurovich L (2011) Evidence for the transmission of information through electric potentials in injured avocado trees. J Plant Physiol 168:103–108PubMedGoogle Scholar
  86. Preston CA, Laue G, Baldwin IT (2001) Methyl jasmonate is blowing in the wind, but can it act as a plant–plant airborne signal? Biochem Syst Ecol 29:1007–1023Google Scholar
  87. Pyatygin S, Opritov V, Vodeneev V (2008) Signaling role of action potential in higher plants. Russ J Plant Physiol 55:285–291Google Scholar
  88. Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483PubMedGoogle Scholar
  89. Rasmann S, Erwin AC, Halitschke R, Agrawal AA (2011) Direct and indirect root defences of milkweed (Asclepias syriaca): trophic cascades, trade-offs and novel methods for studying subterranean herbivory. J Ecol 99:16–25Google Scholar
  90. Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032PubMedGoogle Scholar
  91. Rehrig EM, Appel HM, Schultz JC (2011) Measuring ‘normalcy’ in plant gene expression after herbivore attack. Mol Ecol Res 11:294–304Google Scholar
  92. Schmelz EA, Carroll MJ, LeClere S, Phypps SM, Meredith J, Chourey PS, Alborn HT et al (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci U S A 103:8894–8899PubMedGoogle Scholar
  93. Schuler MA (2011) P450s in plant-insect interactions. Biochim Biophys Acta 1814:36–45PubMedGoogle Scholar
  94. Sergeant K, Renaut J (2010) Plant biotic stress and proteomics. Curr Proteomics 7:275–297Google Scholar
  95. Shao HB, Song WY, Chu LY (2008) Advances of calcium signals involved in plant anti-drought. C R Biol 331:587–596PubMedGoogle Scholar
  96. Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60:139–164PubMedGoogle Scholar
  97. Singh A, Singh IK, Verma PK (2008) Differential transcript accumulation in Cicer arietinum L. in response to a chewing insect Helicoverpa armigera and defence regulators correlate with reduced insect performance. J Exp Bot 59:2379–2392PubMedGoogle Scholar
  98. Snoeren TAL, De Jong PW, Dicke M (2007) Ecogenomic approach to the role of herbivore-induced plant volatiles in community ecology. J Chem Ecol 95:17–26Google Scholar
  99. Spiteller D, Pohnert G, Boland W (2001) Absolute configuration of volicitin, an elicitor of plant volatile biosynthesis from lepidopteran larvae. Tetrahedron Lett 42:1483–1485Google Scholar
  100. Stephens NR, Cleland RE, Van Volkenburgh E (2006) Shade-induced action potentials in Helianthus anuus L. originate primarily from the epicotyl. Plant Signaling Behav 1:15–22Google Scholar
  101. Stipanovic RD, Lopez JD, Dowd MK, Puckhaber LS, Duke SE (2006) Effect of racemic and (+)- and (-)-gossypol on the survival and development of Helicoverpa zea larvae. J Chem Ecol 32:959–968PubMedGoogle Scholar
  102. Thivierge K, Prado A, Driscoll BT, Bonneil E, Thibault P, Bede JC (2010) Caterpillar- and salivary-specific modification of plant proteins. J Proteome Res 9:5887–5895PubMedGoogle Scholar
  103. Torsten W, van Bel AJ (2008) Induction as well as suppression: how aphid saliva may exert opposite effects on plant defense. Plant Signaling Behav 3:427–430Google Scholar
  104. van Dam NM (2009) How plants cope with biotic interactions. Plant Biol 11:1–5PubMedGoogle Scholar
  105. VanDoorn A, Kallenbach M, Borquez AA, Baldwin IT, Bonaventure G (2010) Rapid modification of the insect elicitor N-linolenoyl-glutamate via a lipoxygenase-mediated mechanism on Nicotiana attenuata leaves. BMC Plant Biol 10:164PubMedGoogle Scholar
  106. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene-expression. Science 270:484–487PubMedGoogle Scholar
  107. Vlot AC, Klessig DF, Park SW (2008) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11:436–442PubMedGoogle Scholar
  108. Volkov AG, Haack RA (1995) Insect-induced bioelectrochemical signals in potato plants. Bioelectrochem Bioenerg 37:55–60Google Scholar
  109. Volkov AG, Mwesigwa J (2000) Interfacial electrical phenomena in green plants: action potentials. In: Volkov AG (ed) Liquid interfaces in chemical, biological, and pharmaceutical applications. Dekker, New YorkGoogle Scholar
  110. Volkov AG, Lang RD, Volkova-Gugeshashvili MI (2007) Electrical signaling in Aloe vera induced by localized thermal stress. Bioelectrochemistry 71:192–197PubMedGoogle Scholar
  111. Volkov AG, Adesina T, Markin VS, Jovanov E (2008) Kinetics and mechanism of Dionaea muscipula trap closing. Plant Physiol 146:694–702PubMedGoogle Scholar
  112. Volkov AG, Foster JC, Markin VS (2010) Signal transduction in Mimosa pudica: biologically closed electrical circuits. Plant, Cell Environ 33:816–827Google Scholar
  113. Wei Z, Hu W, Lin QS, Cheng XY, Tong MJ, Zhu LL, Chen RZ et al (2009) Understanding rice plant resistance to the brown planthopper (Nilaparvata lugens): a proteomic approach. Proteomics 9:2798–2808PubMedGoogle Scholar
  114. Whiteman NK, Groen SC, Chevasco D, Bear A, Beckwith N, Gregory TR, Denoux C et al (2011) Mining the plant-herbivore interface with a leafmining Drosophila of Arabidopsis. Mol Ecol 20:995–1014PubMedGoogle Scholar
  115. Winterhalter M (2000) Black lipid membranes. Curr Opin Colloid Interface Sci 5:250–255Google Scholar
  116. Woldemariam MG, Baldwin IT, Galis I (2011) Transcriptional regulation of plant inducible defenses against herbivores: a mini-review. J Plant Interact 6:113–119Google Scholar
  117. Wu JQ, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24PubMedGoogle Scholar
  118. Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–1122PubMedGoogle Scholar
  119. Yan XF, Wang ZY, Huang L, Wang C, Hou RF, Xu ZL, Qiao XJ (2009) Research progress on electrical signals in higher plants. Prog Nat Sci 19:531–541Google Scholar
  120. Yoshinaga N, Aboshi T, Abe H, Nishida R, Alborn HT, Tumlinson JH, Mori N (2008) Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae. Proc Natl Acad Sci U S A 105:18058–18063PubMedGoogle Scholar
  121. Zhang JH, Sun LW, Liu LL, Lian J, An SL, Wang X, Zhang J et al (2010) Proteomic analysis of interactions between the generalist herbivore Spodoptera exigua (Lepidoptera: Noctuidae) and Arabidopsis thaliana. Plant Mol Biol Rep 28:324–333Google Scholar
  122. Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146:852–858PubMedGoogle Scholar
  123. Zimmermann MR, Maischak H, Mithoefer A, Boland W, Felle HH (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol 149:1593–1600PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Plant Physiology Unit, Department of Life Sciences and Systems Biology, Innovation CentreUniversity of TurinTurinItaly
  2. 2.Department of Entomology and Plant PathologyAuburn UniversityAuburnUSA

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