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Systemic Wound Signaling in Plants

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Long-Distance Systemic Signaling and Communication in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 19))

Abstract

Ever since the seminal discovery of systemic wound signaling in tomato and potato plants by Green and Ryan (Science 1972), a number of candidate systemic wound signals have been proposed. These can be classified into three groups: (1) Chemical signals, including the alarm hormone systemin and other peptide hormones, jasmonic acid is a phytohormone, as well as reactive oxygen species (ROS); (2) physical signals, including electrical and hydraulic signals; and (3) herbivore-induced volatile compounds, including green leafy volatiles and terpenes. These signals are generated at or close to the site of herbivore-inflicted injury and systemically move to target tissues where they induce defense responses. Chemical and physical signals depend on the connectivity of the plant body, whereas volatile compounds are released into the airspace. Different plants with different morphologies and ecological niches employ different modes of systemic signaling.

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References

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

    Article  CAS  Google Scholar 

  • Alarcon JJ, Malone M (1994) Substantial hydraulic signals are triggered by leaf-biting insects in tomato. J Exp Bot 45:953–957

    Article  Google Scholar 

  • Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949

    Article  CAS  Google Scholar 

  • Aloni B, Wyse RE, Griffith S (1986) Sucrose transport and phloem unloading in stem of Vicia faba: possible involvement of a sucrose carrier and osmotic regulation. Plant Physiol 81:482–486

    Article  PubMed  CAS  Google Scholar 

  • Ament K, Krasikov V, Allmann S, Rep M, Takken FL, Schuurink RC (2006) Methyl salicylate production in tomato affects biotic interactions. Plant J 62:124–134

    Article  CAS  Google Scholar 

  • Amon P, Haas E, Sumper M (1998) The sex-inducing pheromone and wounding trigger the same set of genes in the multicellular green alga Volvox. Plant Cell 10:781–789

    PubMed  CAS  Google Scholar 

  • Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406(6795):512–515

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta 1734:91–111

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Shiojiri K, Karban R (2010) Acquired immunity to herbivory and allelopathy caused by airborne plant emissions. Phytochemistry 71:1642–1649

    Article  PubMed  CAS  Google Scholar 

  • Avila CA, Arévalo-Soliz LM, Jia L, Navarre DA, Chen Z, Howe GA, Meng QW, Smith JE, Goggin FL (2012) Loss of function of FATTY ACID DESATURASE7 in tomato enhances basal aphid resistance in a salicylate-dependent manner. Plant Physiol 158:2028–2041

    Article  PubMed  CAS  Google Scholar 

  • Baldwin IT, Kessler A, Halitschke R (2002) Volatile signaling in plant–plant–herbivore interactions: what is real? Curr Opin Plant Biol 5:351–354

    Article  PubMed  CAS  Google Scholar 

  • Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant–plant interactions: “talking trees” in the genomics era. Science 311:812–815

    Article  PubMed  CAS  Google Scholar 

  • Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  PubMed  CAS  Google Scholar 

  • Barroso JB, Corpas FJ, Carreras A et al (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793

    Article  PubMed  CAS  Google Scholar 

  • Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493

    Article  PubMed  Google Scholar 

  • Baydoun EAH, Fry SC (1985) The immobility of pectic substances in injured tomato leaves and its bearing on the identity of the wound hormone. Planta 165:269–276

    Article  CAS  Google Scholar 

  • Beckers GJ, Spoel SH (2006) Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biol (Stuttg) 8:1–10

    Article  CAS  Google Scholar 

  • Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–953

    Article  PubMed  CAS  Google Scholar 

  • Berger B, Baldwin IT (2007) The hydroxyproline-rich glycopeptide systemin precursor NapreproHypSys does not play a central role in Nicotiana attenuata’s anti-herbivore defense responses. Plant Cell Environ 30:1450–1464

    Article  PubMed  CAS  Google Scholar 

  • Berger B, Baldwin IT (2009) Silencing the hydroxyproline-rich glycopeptide systemin precursor in two accessions of Nicotiana attenuata alters flower morphology and rates of self-pollination. Plant Physiol 149:1690–1700

    Article  PubMed  CAS  Google Scholar 

  • Bergey D, Howe G, Ryan CA (1996) Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci USA 93:12053–12058

    Article  PubMed  CAS  Google Scholar 

  • Berner JM, van der Westhuizen AJ (2010) Inhibition of xanthine oxidase activity results in the inhibition of Russian wheat aphid-induced defense enzymes. J Chem Ecol 36:1375–1380

    Article  PubMed  CAS  Google Scholar 

  • Birkenmeier GF, Ryan CA (1998) Wound signaling in tomato plants. Evidence that ABA is not a primary signal for defense gene activation. Plant Physiol 117:687–693

    Article  PubMed  CAS  Google Scholar 

  • Bishop P, Makus DJ, Pearce G, Ryan CA (1981) Proteinase inhibitor inducing factor activity in tomato leaves resides in oligosaccharides enzymically released from cell walls. Proc Natl Acad Sci USA 78:3536–3640

    Article  PubMed  CAS  Google Scholar 

  • Bishop P, Pearce G, Bryant JE, Ryan CA (1984) Isolation and characterization of the proteinase inhibitor inducing factor from tomato leaves: identity and activity of poly- and oligogalacturonide fragments. J Biol Chem 259:13172–13177

    PubMed  CAS  Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448

    Article  PubMed  Google Scholar 

  • Breithaupt C, Kurzbauer R, Lilie H, Schaller A, Strassner J, Huber R, Macheroux P, Clausen T (2006) Crystal structure of 12-oxophytodienoate reductase 3 from tomato: self-inhibition by dimerization. Proc Natl Acad Sci USA 103:14337–14342

    Article  PubMed  CAS  Google Scholar 

  • Broekgaarden C, Poelman EH, Steenhuis G, Voorrips RE, Dicke M, Vosman B (2008) Responses of Brassica oleracea cultivars to infestation by the aphid Brevicoryne brassicae: an ecological and molecular approach. Plant Cell Environ 31:1592–1605

    Article  PubMed  CAS  Google Scholar 

  • Browse J (2009) The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochemistry 70:1539–1546

    Article  PubMed  CAS  Google Scholar 

  • Browse J, Howe GA (2008) New weapons and a rapid response against insect attack. Plant Physiol 146:832–838

    Article  PubMed  CAS  Google Scholar 

  • Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011) Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J Exp Bot 62:1803–1813

    Article  PubMed  CAS  Google Scholar 

  • Chen F, D’Auria JC, Tholl D, Ross JR, Gershenzon J, Noel JP, Pichersky E (2003) An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J 36:577–588

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102:19237–19242

    Article  PubMed  CAS  Google Scholar 

  • Chung HS, Niu Y, Browse J, Howe GA (2009) Top hits in contemporary JAZ: An update on jasmonate signaling. Phytochemistry 70:1547–1559

    Article  PubMed  CAS  Google Scholar 

  • Constabel CP, Yip L, Ryan CA (1998) Prosystemin from potato, black nightshade, and bell pepper: primary structure and biological activity of predicted systemin polypeptides. Plant Mol Biol 36:55–62

    Article  PubMed  CAS  Google Scholar 

  • Corrado G, Sasso R, Pasquariello M, Iodice L, Carretta A, Cascone P, Ariati L, Digilio MC, Guerrieri E, Rao R (2007) Systemin regulates both systemic and volatile signaling in tomato plants. J Chem Ecol 33:669–681

    Article  PubMed  CAS  Google Scholar 

  • Couldridge C, Newbury HJ, Ford-Lloyd B, Bale J, Pritchard J (2007) Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. Bull Entomol Res 97:523–532

    Article  PubMed  CAS  Google Scholar 

  • de la Noval BM, Pérez E, Olalde V, Délano JP, Martínez N (2004) Inducción de β-1,3-glucanasa y quitinasas en plántulas de tomate por hongos micorrizógenos y sistemina. Cult Trop 2:5–12

    Google Scholar 

  • de la Noval B, Pérez E, Martínez B, León O, Martínez-Gallardo N, Délano-Frier J (2007) Exogenous systemin has a contrasting effect on disease resistance in mycorrhizal tomato (Solanum lycopersicum) plants infected with necrotrophic or hemibiotrophic pathogens. Mycorrhiza 17:449–460

    Article  PubMed  CAS  Google Scholar 

  • De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580

    Article  PubMed  CAS  Google Scholar 

  • de Vos M, Kim JH, Jander G (2007) Biochemistry and molecular biology of Arabidopsis–aphid interactions. Bioessays 29:871–883

    Article  PubMed  CAS  Google Scholar 

  • Degenhardt DC, Refi-Hind S, Stratmann JW, Lincoln DE (2010) Systemin and jasmonic acid regulate constitutive and herbivore-induced systemic volatile emissions in tomato, Solanum lycopersicum. Phytochemistry 71:2024–2037

    Article  PubMed  CAS  Google Scholar 

  • Díaz M, Achkor H, Titarenko E, Martínez MC (2003) The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Lett 543:136–139

    Article  PubMed  CAS  Google Scholar 

  • Dicke M, Agrawal AA, Bruin J (2003) Plants talk, but are they deaf? Trends Plant Sci 8:403–405

    Article  PubMed  CAS  Google Scholar 

  • 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 155:1936–1946

    Article  PubMed  CAS  Google Scholar 

  • Doares SH, Narvaez-Vasquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746

    PubMed  CAS  Google Scholar 

  • Doherty HM, Selvendran RR, Bowles DJ (1988) The wound response of tomato plants can be inhibited by aspirin and related hydroxybenzoic acids. Physiol Mol Plant Pathol 33:377–384

    Article  CAS  Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    Article  PubMed  CAS  Google Scholar 

  • Dombrowski JE (2003) Salt stress activation of wound-related genes in tomato plants. Plant Physiol 132:2098–3107

    Article  PubMed  CAS  Google Scholar 

  • Dombrowski JE, Pearce G, Ryan CA (1999) Proteinase inhibitor-inducing activity of the prohormone prosystemin resides exclusively in the C-terminal systemin domain. Proc Natl Acad Sci USA 96:12947–12952

    Article  PubMed  CAS  Google Scholar 

  • Dombrowski JE, Hind SR, Martin RC, Stratmann JW (2011) Wounding systemically activates a mitogen-activated protein kinase in forage and turf grasses. Plant Sci 180:686–693

    Article  PubMed  CAS  Google Scholar 

  • Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552

    Article  PubMed  CAS  Google Scholar 

  • Doss RP, Oliver JE, Proebsting WM, Potter SW, Kuy S, Clement SL, Williamson RT, Carney JR, DeVilbiss ED (2000) Bruchins: insect-derived plant regulators that stimulate neoplasm formation. Proc Natl Acad Sci USA 97:6218–6223

    Article  PubMed  CAS  Google Scholar 

  • Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785

    Article  PubMed  CAS  Google Scholar 

  • Erb M, Flors V, Karlen D, de Lange E, Planchamp C, D’Alessandro M, Turlings TC, Ton J (2009) Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J 59:292–302

    Article  PubMed  CAS  Google Scholar 

  • Erb M, Köllner TG, Degenhardt J, Zwahlen C, Hibbard BE, Turlings TC (2011) The role of abscisic acid and water stress in root herbivore-induced leaf resistance. New Phytol 189:308–320

    Article  PubMed  CAS  Google Scholar 

  • Espunya MC, De Michele R, Gómez-Cadenas A, Martínez MC (2012) S-Nitrosoglutathione is a component of wound- and salicylic acid-induced systemic responses in Arabidopsis thaliana. J Exp Bot 63:3219–3227

    Article  PubMed  CAS  Google Scholar 

  • Farag MA, Paré PW (2002) C6-Green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61:545–554

    Article  PubMed  CAS  Google Scholar 

  • Farmer EE (2001) Surface-to-air signals. Nature 411:854–856

    Article  PubMed  CAS  Google Scholar 

  • Farmer EE, Ryan CA (1994) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716

    Article  Google Scholar 

  • Feechan A, Kwon E, Yun BW, Wang Y, Pallas A, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA 102:8054–8059

    Article  PubMed  CAS  Google Scholar 

  • Felix G, Boller T (1995) Systemin induces rapid ion fluxes and ethylene biosynthesis in Lycopersicon peruvianum cells. Plant Cell 7:381–389

    CAS  Google Scholar 

  • Felton GW, Workman J, Duffey SS (1992) Avoidance of antinutritive plant defense: role of midgut pH in Colorado potato beetle. J Chem Ecol 18:571–583

    Article  CAS  Google Scholar 

  • Fisher DB (1990) Measurement of phloem transport rates by an indicator-dilution technique. Plant Physiol 94:455–462

    Article  PubMed  CAS  Google Scholar 

  • Fraenkel GS (1959) The raison d’être of secondary plant substances. Science 129:466–1470

    Article  Google Scholar 

  • Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498

    Article  PubMed  Google Scholar 

  • Gfeller A, Liechti R, Farmer EE (2010) Arabidopsis jasmonate signaling pathway. Sci Signal 3:cm4

    Article  PubMed  CAS  Google Scholar 

  • Glauser G, Grata E, Dubugnon L, Rudaz S, Farmer EE, Wolfender J-L (2008) Spatial and temporal dynamics of jasmonate synthesis and accumulation in Arabidopsis in response to wounding. J Biol Chem 283:16400–16407

    Article  PubMed  CAS  Google Scholar 

  • Glauser G, Dubugnon L, Mousavi SAR, Rudaz S, Wolfender J-L, Farmer EE (2009) Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J Biol Chem 284:34506–34513

    Article  PubMed  CAS  Google Scholar 

  • Glendinning JI (2002) How do herbivorous insects cope with noxious secondary plant compounds in their diet? Entomol Exp Appl 104:15–25

    Article  CAS  Google Scholar 

  • Godard KA, White R, Bohlmann J (2008) Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69:1838–1849

    Article  PubMed  CAS  Google Scholar 

  • Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777

    Article  PubMed  CAS  Google Scholar 

  • Gupta JG (2011) Protein S-nitrosylation in plants: photorespiratory metabolism and NO signaling. Sci Signal 4:jc1

    Article  PubMed  CAS  Google Scholar 

  • Gutsche AR, Heng-Moss TM, Higley LG, Sarath G, Mornhinweg DW (2009) Physiological responses of resistant and susceptible barley, Horedum vulgare to the Russian wheat aphid, Diurpahis noxia (Mordvilko). Arthropod Plant Interact 3:233–240

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Heil M, Karban R (2009) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144

    Article  Google Scholar 

  • Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472

    Article  PubMed  CAS  Google Scholar 

  • Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272

    Article  PubMed  CAS  Google Scholar 

  • Heil M, Lion U, Boland W (2008) Defense-inducing volatiles: in search of the active motif. J Chem Ecol 34:601–604

    Article  PubMed  CAS  Google Scholar 

  • Heitz T, Bergey DA, Ryan CA (1997) A gene encoding a chloroplast-targeted lipoxygenase in tomato leaves is transiently induced by wounding, systemin, and methyl jasmonate. Plant Physiol 114:1085–1093

    Article  PubMed  CAS  Google Scholar 

  • Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Désaubry L, Holder E, Grausem B, Kandel S, Miesch M, Werck-Reichhart D, Pinot F (2012) Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone jasmonoyl-isoleucine for catabolic turnover. J Biol Chem 287:6296–6306

    Article  PubMed  CAS  Google Scholar 

  • Hind SR, Malinowski R, Yalamanchili R, Stratmann JW (2010) Tissue-type specific systemin perception and the elusive systemin receptor. Plant Signal Behav 5:42–44

    Article  PubMed  CAS  Google Scholar 

  • Hong JK, Yun BW, Kang JG, Raja MU, Kwon E, Sorhagen K, Chu C, Wang Y, Loake GJ (2008) Nitric oxide function and signalling in plant disease resistance. J Exp Bot 59:147–154

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 8:2067–2077

    PubMed  CAS  Google Scholar 

  • Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997–1008

    Article  PubMed  CAS  Google Scholar 

  • Huffaker A, Ryan CA (2007) Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc Natl Acad Sci USA 104:10732–10736

    Article  PubMed  CAS  Google Scholar 

  • Huffaker A, Pearce G, Ryan CA (2006) An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 103:10098–10103

    Article  PubMed  CAS  Google Scholar 

  • Huffaker A, Dafoe NJ, Schmelz EA (2011) ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol 155:1325–1338

    Article  PubMed  CAS  Google Scholar 

  • Huffaker A, Pearce G, Veyrat N, Erb M, Turlings TC, Sartor R, Shen Z, Briggs S, Vaughan MM, Alborn HT, Teal PE, Schmelz EA (2013) Plant elicitor peptides are conserved signals regulating direct and indirect anti-herbivore defense. Proc Natl Acad Sci USA. Published online before print March 18, 2013, doi: 10.1073/pnas.1214668110

    Google Scholar 

  • Jones CG, Hopper RF, Coleman JS, Krischik VA (1993) Control of systemically induced herbivore resistance by plant vascular architecture. Oecologia 93:452–456

    Article  Google Scholar 

  • Kallenbach M, Alagna F, Baldwin IT, Bonaventure G (2010) Nicotiana attenuata SIPK, WIPK, NPR1, and fatty acid-amino acid conjugates participate in the induction of jasmonic acid biosynthesis by affecting early enzymatic steps in the pathway. Plant Physiol 152:96–106

    Article  PubMed  CAS  Google Scholar 

  • Kallenbach M, Bonaventure G, Gilardoni PA, Wissgott A, Baldwin IT (2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations. Proc Natl Acad Sci USA 109:E1548–E1557

    Article  PubMed  CAS  Google Scholar 

  • 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 104:12205–12210

    Article  PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71

    Article  Google Scholar 

  • Karban R, Shiojiri K, Huntzinger M, McCall AC (2006) Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930

    Article  PubMed  Google Scholar 

  • Katsir L, Chung HS, Koo AJK, Howe GA (2008) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11:428–435

    Article  PubMed  CAS  Google Scholar 

  • Kazan K, Manners JM (2008) Jasmonate signaling: toward an integrated view. Plant Physiol 146:1459–1468

    Article  PubMed  CAS  Google Scholar 

  • 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 Physiol 143:849–865

    Article  PubMed  CAS  Google Scholar 

  • Kerchev PI, Fenton B, Foyer CH, Hancock RD (2012) Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ 35:441–453

    Article  PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    Article  PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328

    Article  PubMed  CAS  Google Scholar 

  • Kim CY, Liu Y, Thorne ET, Yang H, Fukushige H, Gassmann W, Hildebrand D, Sharp RE, Zhang S (2003) Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 15:2707–2718

    Article  PubMed  CAS  Google Scholar 

  • Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TC, Gershenzon J, Degenhardt J (2008) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20:482–494

    Article  PubMed  CAS  Google Scholar 

  • Koo AJK, Howe GA (2012) Catabolism and deactivation of the lipid-derived hormone jasmonoyl-isoleucine. Front Plant Sci 3:19

    Article  PubMed  CAS  Google Scholar 

  • Koo AJ, Gao X, Jones AD, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59:974–986

    Article  PubMed  CAS  Google Scholar 

  • Koo AJ, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proc Natl Acad Sci USA 108:9298–9303

    Article  PubMed  CAS  Google Scholar 

  • 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 Physiol 147:1358–1368

    Article  PubMed  CAS  Google Scholar 

  • Krol E, Mentzel T, Chinchilla D, Boller T, Felix G, Kemmerling B, Postel S, Arents M, Jeworutzki E, Al-Rasheid KA, Becker D, Hedrich R (2010) Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J Biol Chem 285:13471–13479

    Article  PubMed  CAS  Google Scholar 

  • Kuĉśnierczyk A, Winge P, Jørstad TS, Troczyńska J, Rossiter JT, Bones AM (2008) Towards global understanding of plant defence against aphids – timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ 31:1097–1115

    Article  CAS  Google Scholar 

  • Lee GI, Howe GA (2003) The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. Plant J 33:567–576

    Article  PubMed  CAS  Google Scholar 

  • Leitner M, Boland W, Mithöfer A (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago trunculata. New Phytol 167:597–606

    Article  PubMed  CAS  Google Scholar 

  • Leon J, Rojo E, Sanchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52:1–9

    Article  PubMed  CAS  Google Scholar 

  • Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RA, Ritsema T, Pieterse CM (2009) Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol 149:1797–1809

    Article  PubMed  CAS  Google Scholar 

  • Leon-Reyes A, Du Y, Koornneef A, Proietti S, Körbes AP, Memelink J, Pieterse CM, Ritsema T (2010) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic Acid. Mol Plant Microbe Interact 23:187–197

    Article  PubMed  CAS  Google Scholar 

  • Li C, Williams MM, Loh Y-T, Lee GI, Howe GA (2002a) Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiol 130:494–503

    Article  PubMed  CAS  Google Scholar 

  • Li L, Li C, Lee GI, Howe GA (2002b) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99:6416–6421

    Article  PubMed  CAS  Google Scholar 

  • Li C, Liu G, Xu C, Lee GI, Bauer P, Ling HQ, Ganal MW, Howe GA (2003) The tomato suppressor of prosystemin-mediated responses2 (Spr2) gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15:1646–1661

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Li CY, Schilmiller AL, Liu GH, Lee GI, Jayanty S, Sageman C (2005) Role of beta-oxidation in jasmonate biosynthesis and distal wound signaling in tomato. Plant Cell 17:971–986

    Article  PubMed  CAS  Google Scholar 

  • Lindermayr C, Sell S, Müller B, Leister D, Durner J (2010) Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22:2894–2907

    Article  PubMed  CAS  Google Scholar 

  • Lippert D, Chowrira S, Ralph SG, Zhuang J, Aeschliman D, Ritland C, Ritland K, Bohlmann J (2007) Conifer defense against insects: proteome analysis of Sitka spruce (Picea sitchensis) bark induced by mechanical wounding or feeding by white pine weevils (Pissodes strodi). Proteomics 7:248–270

    Article  PubMed  CAS  Google Scholar 

  • Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 143:784–800

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386–3399

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410:490–494

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 8:532–540

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ma Y, Walker RK, Zhao Y, Berkowitz GA (2012) Linking ligand perception by PEPR pattern recognition receptors to cytosolic Ca2+ elevation and downstream immune signaling in plants. Proc Natl Acad Sci USA 109:19852–19857

    Article  PubMed  CAS  Google Scholar 

  • Maffei M, Bossi S, Spiteller D, Mithofer 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 134:1752–1762

    Article  PubMed  CAS  Google Scholar 

  • Maffei ME, Mithöfer A, Arimura GI, Uchtenhagen H, Bossi S, Bertea CM, Cucuzza LS, Novero M, Volpe V, Quadro S, Boland W (2006) Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol 140:1022–1035

    Article  PubMed  CAS  Google Scholar 

  • Malone M (1993) Hydraulic signals. Philos Trans R Soc Lond, Ser B Biol Sci 341:33–39

    Article  Google Scholar 

  • Malone M (1996) Rapid, long-distance signal transmission in higher plants. In: Callow JA (ed) Advances in botanical research, vol 22. Academic, San Diego, CA, pp 163–228

    Google Scholar 

  • Malone M, Alarcon JJ (1995) Only xylem-borne factors can account for systemic wound signaling in the tomato plant. Planta 196:740–746

    Article  CAS  Google Scholar 

  • Malone M, Palumbo L, Boari F, Monteleone M, Jones HG (1994) The relationship between wound-induced proteinase-inhibitors and hydraulic signals in tomato seedlings. Plant Cell Environ 17:81–87

    Article  CAS  Google Scholar 

  • Matsui K, Kurishita S, Hisamitsu A, Kajiwara T (2000) A lipid-hydrolysing activity involved in hexenal formation. Biochem Soc Trans 28:857–860

    Article  PubMed  CAS  Google Scholar 

  • McConn M, Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8:403–416

    PubMed  CAS  Google Scholar 

  • McGurl B, Pearce G, Orozco-Cárdenas M, Ryan CA (1992) Structure, expression, and antisense inhibition of the systemin precursor gene. Science 225:1570–1573

    Article  Google Scholar 

  • McGurl B, Orozco-Cárdenas M, Pearce G, Ryan CA (1994) Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc Natl Acad Sci USA 91:9799–9902

    Article  PubMed  CAS  Google Scholar 

  • Meindl T, Boller T, Felix G (1998) The plant wound hormone systemin binds with the N-terminal part to its receptor but needs the C-terminal part to activate it. Plant Cell 10:1561–1570

    PubMed  CAS  Google Scholar 

  • Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67:2450–2462

    Article  PubMed  CAS  Google Scholar 

  • Michereff MF, Laumann RA, Borges M, Michereff-Filho M, Diniz IR, Neto AL, Moraes MC (2011) Volatiles mediating a plant–herbivore-natural enemy interaction in resistant and susceptible soybean cultivars. J Chem Ecol 37:273–285

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45

    Article  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  PubMed  CAS  Google Scholar 

  • Moloi MJ, van der Westhuizen AJ (2006) The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. J Plant Physiol 163:1118–1125

    Article  PubMed  CAS  Google Scholar 

  • Moloi MJ, van der Westhuizen AJ (2008) Antioxidative responses and the Russian wheat aphid (Diuraphis noxia) resistance responses in wheat (Triticum aestivum). Plant Biol 10:403–407

    Article  PubMed  CAS  Google Scholar 

  • Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085

    Article  PubMed  CAS  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    Article  PubMed  CAS  Google Scholar 

  • Narvaez-Vasquez J, Ryan CA (2002) The systemin precursor gene regulates both defensive and developmental genes in Solanum tuberosum. Proc Natl Acad Sci USA 99:15818–15821

    Article  PubMed  CAS  Google Scholar 

  • Nárvaez-Vasquez J, Orozco-Cardenas ML, Ryan CA (1994) A sulfhydryl reagent modulates systemic signaling for wound-induced and systemin-induced proteinase inhibitor synthesis. Plant Physiol 105:725–730

    PubMed  Google Scholar 

  • Narvaez-Vasquez J, Pearce G, Ryan CA (2005) The plant cell wall matrix harbors a precursor of defense signaling peptides. Proc Natl Acad Sci USA 102:12974–12977

    Article  PubMed  CAS  Google Scholar 

  • Narvaez-Vasquez J, Orozco-Cardenas ML, Ryan CA (2007) Systemic wound signaling in tomato plants is cooperatively regulated by multiple plant peptides. Plant Mol Biol 65:711–718

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Orians CM, Pomerleau J, Ricco R (2000) Vascular architecture generates fine scale variation in systemic induction of proteinase inhibitors in tomato. J Chem Ecol 26:471–485

    Article  CAS  Google Scholar 

  • Orozco-Cardenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96:6553–6557

    Article  PubMed  CAS  Google Scholar 

  • Orozco-Cárdenas ML, Ryan CA (2002) Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol 130:487–493

    Article  PubMed  CAS  Google Scholar 

  • Orozco-Cárdenas M, McGurl B, Ryan CA (1993) Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proc Natl Acad Sci USA 90:8273–8276

    Article  PubMed  Google Scholar 

  • Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191

    PubMed  Google Scholar 

  • Park SJ, Huang Y, Ayoubi P (2006) Identification of expression profiles of sorghum genes in response to green-bug phloem-feeding using cDNA subtraction microarray analysis. Planta 223:932–947

    Article  PubMed  CAS  Google Scholar 

  • Partida-Martinez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2:100

    Article  PubMed  Google Scholar 

  • Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Perez AC, Chico JM, Bossche RV, Sewell J, Gil E, Garcia-Casado G, Witters E, Inze D, Long JA, De Jaeger G, Solano R, Goossens A (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791

    Article  PubMed  CAS  Google Scholar 

  • Pearce G (2011) Systemin, hydroxyproline-rich systemin and the induction of protease inhibitors. Curr Protein Pept Sci 12:399–408

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induced wound-inducible proteinase inhibitor proteins. Science 253:895–898

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Johnson S, Ryan CA (1993) Purification and characterization from tobacco (Nicotiana tabacum) leaves of six small, wound-inducible, proteinase isoinhibitors of the potato inhibitor II family. Plant Physiol 102:639–644

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Moura DS, Stratmann J, Ryan CA (2001) Production of multiple plant hormones from a single polyprotein precursor. Nature 411:817–820

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Siems WF, Bhattacharya RC, Chen Y-C, Ryan CA (2007) Three hydroxyproline-rich glycopeptides from a single petunia polyproline precursor activate defensin I, a pathogen defense response gene. J Biol Chem 282:17777–17784

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Yamaguchi Y, Barona G, Ryan CA (2010) A subtilisin-like protein from soybean contains an embedded cryptic signal that activates defense-related genes. Proc Natl Acad Sci USA 107:14921–14925

    Article  PubMed  CAS  Google Scholar 

  • Peña-Cortés H, Fisahn J, Willmitzer L (1995) Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc Natl Acad Sci USA 92:4106–4113

    Article  PubMed  Google Scholar 

  • Peñuelas J, Llusià J (2004) Plant VOC emissions: making use of the unavoidable. Trends Ecol Evol 19:402–404

    Article  PubMed  Google Scholar 

  • Peuke AD, Windt C, Van As H (2006) Effects of cold-girdling on flows in the transport phloem in Ricinus communis: is mass flow inhibited? Plant Cell Environ 29:15–25

    Article  PubMed  Google Scholar 

  • Philippe RN, Ralph SG, Mansfield SD, Bohlmann J (2010) Transcriptome profiles of hybrid poplar (Populus trichocarpa × deltoids) reveal rapid changes in undamaged, systemic sink leaves after simulated feeding by forest tent caterpillar (Malacosoma disstria). New Phytol 188:787–802

    Article  PubMed  CAS  Google Scholar 

  • Ponce De León I, Schmelz EA, Gaggero C, Castro A, ÁLvarez A, Montesano M (2012) Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Mol Plant Pathol 13:960–974

    Article  PubMed  Google Scholar 

  • Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP (2009) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23:80–92

    Article  PubMed  CAS  Google Scholar 

  • Qi Z et al (2010) Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels. Proc Natl Acad Sci USA 107:21193–21198

    Article  PubMed  CAS  Google Scholar 

  • Ralph SG, Yueh H, Friedmann M, Aeschliman D, Zeznik JA, Nelson CC, Butterfield YS, Kirkpatrick R, Liu J, Jones SJ, Marra MA, Douglas CJ, Ritland K, Bohlmann J (2006) Conifer defence against insects: microarray gene expression profiling of Sitka spruce (Picea sitchensis) induced by mechanical wounding or feeding by spruce budworms (Choristoneura occidentalis) or white pine weevils (Pissodes strobi) reveals large scale changes of the host transcriptome. Plant Cell Environ 29:1545–1570

    Article  PubMed  Google Scholar 

  • Ralph SG, Chun HJE, Cooper D, Kirkpatrick R, Kolosova N, Gunter L, Tuskan GA, Douglas CJ, Holt RA, Jones SJM, Marra MA, Bohlmann J (2008) Analysis of 4664 high-quality sequence-finished poplar full-length cDNA clones and their utility for the discovery of genes responding to insect feeding. BMC Genomics 9:57

    Article  PubMed  CAS  Google Scholar 

  • Ramadan A, Muroi A, Arimura G (2011) Herbivore-induced maize volatiles serve as priming cues for resistance against post-attack by the specialist armyworm Mythimna separata. J Plant Interact 6:SI155–SI158

    Article  CAS  Google Scholar 

  • Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TC (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737

    Article  PubMed  CAS  Google Scholar 

  • Rempt M, Pohnert G (2010) Novel acetylenic oxylipins from the moss Dicranum scoparium with antifeeding activity against herbivorous slugs. Angew Chem Int Ed 49:4755–4758

    Article  CAS  Google Scholar 

  • Ren F, Lu Y-T (2006) Overexpression of tobacco hydroxyproline-rich glycopeptide systemin precursor A in transgenic tobacco enhances resistance against Heliocoverpa armigera larvae. Plant Sci 171:286–292

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Rhodes JD, Thain JF, Wildon CD (1996) The pathway for systemic electrical signal conduction in the wounded tomato plant. Planta 200:50–57

    Article  CAS  Google Scholar 

  • Rhodes JD, Thain JF, Wildon CD (1999) Evidence for physically distinct systemic signalling pathways in the wounded tomato plant. Ann Bot 84:109–116

    Article  CAS  Google Scholar 

  • Rocco M, Corrado G, Arena S, D’Ambrosio C, Tortiglione C, Sellaroli S, Marra M, Rao R, Scaloni A (2008) The expression of tomato prosystemin gene in tobacco plants highly affects host proteomic repertoire. J Proteomics 71:176–185

    Article  PubMed  CAS  Google Scholar 

  • Rocha-Granados MC (2004) Sobre-expresión de la prosistemina y sistemina de jitomate (Lycopersicon esculentum) en plantas de tabaco (Nicotiana tabacum) y su influencia sobre la resistencia a insectos. Ph.D. Thesis. Cinvestav-Unidad Irapuato, México

    Google Scholar 

  • Rocha-Granados MDC, Sanchez-Hernandez C, Sanchez-Hernandez C, Martinez-Gallardo NA, Ochoa-Alejo N, Delano-Frier JP (2005) The expression of the hydroxyproline-rich glycopeptide systemin precursor A in response to (a) biotic stress and elicitors is indicative of its role in the regulation of the wound response in tobacco (Nicotiana tubacum L.). Planta 222:794–810

    Article  CAS  Google Scholar 

  • Rodriguez-Saona CR, Rodriguez-Saona LE, Frost CJ (2009) Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J Chem Ecol 35:163–175

    Article  PubMed  CAS  Google Scholar 

  • Rustérucci C, Espunya MC, Díaz M, Chabannes M, Martínez MC (2007) S-Nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 143:1282–1292

    Article  PubMed  CAS  Google Scholar 

  • Ruther J, Kleier S (2005) Plant–plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J Chem Ecol 31:2217–2222

    Article  PubMed  CAS  Google Scholar 

  • Ryan CA (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477:112–121

    Article  PubMed  CAS  Google Scholar 

  • Ryan CA, Moura DS (2002) Systemic signaling in plants: a new perception. Proc Natl Acad Sci USA 99:6519–6520

    Article  PubMed  CAS  Google Scholar 

  • Ryan CA, Pearce G (2003) Systemins – A functionally defined family of peptide signals that regulate defensive genes in Solanaceae species. Proc Natl Acad Sci 100:14573–14577

    Google Scholar 

  • Ryan CA, Huffaker A, Yamaguchi Y (2007) New insights into innate immunity in Arabidopsis. Cell Microbiol 9:1902–1908

    Article  PubMed  CAS  Google Scholar 

  • Sato C, Seto Y, Nabeta K, Matsuura H (2009) Kinetics of the accumulation of jasmonic acid and its derivatives in distal leaves of tobacco (Nicotiana tabacum cv. Xanthi nc) and translocation of deuterium-labeled jasmonic acid from the wounding site to the distal site. Biosci Biotechnol Biochem 73:1962–1970

    Article  PubMed  CAS  Google Scholar 

  • Sato C, Aikawa K, Sugiyama S, Nabeta K, Masuta C, Matsuura H (2011) Distal transport of exogenously applied jasmonoyl–isoleucine with wounding stress. Plant Cell Physiol 52:509–517

    Article  PubMed  CAS  Google Scholar 

  • Schaller A, Oecking C (1999) Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263–272

    PubMed  CAS  Google Scholar 

  • Schaller A, Stintzi A (2009) Enzymes in jasmonate biosynthesis: structure, function, regulation. Phytochemistry 70:1532–1538

    Article  PubMed  CAS  Google Scholar 

  • Schaller F, Schaller A, Stintzi A (2005) Biosynthesis and metabolism of jasmonates. J Plant Growth Regul 23:179–199

    Google Scholar 

  • Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377

    Article  PubMed  CAS  Google Scholar 

  • Schittko U, Baldwin IT (2003) Constraints to Herbivore-induced systemic responses: bidirectional signaling along orthostichies in Nicotiana attenuata. J Chem Ecol 29:763–770

    Article  PubMed  CAS  Google Scholar 

  • Schittko U, Preston CA, Baldwin IT (2000) Eating the evidence? Manduca sexta larvae can not disrupt specific jasmonate induction in Nicotiana attenuata by rapid consumption. Planta 210:343–346

    Article  PubMed  CAS  Google Scholar 

  • Schmeltz I (1971) Nicotine and other tobacco alkalioids. In: Jacobson MCD (ed) Naturally occurring insecticides. Mercel Dekker, New York, pp 99–136

    Google Scholar 

  • Schmelz EA, Alborn HT, Tumlinson JH (2003) Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays. Physiol Plant 117:403–412

    Article  PubMed  CAS  Google Scholar 

  • Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PE (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci USA 103:8894–8899

    Article  PubMed  CAS  Google Scholar 

  • Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH 3rd, Teal PE (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc Natl Acad Sci USA 106:653–657

    Article  PubMed  CAS  Google Scholar 

  • Schmidt S, Baldwin IT (2006) Systemin in black nightshade (Solanum nigrum). The tomato homologous polypeptide does not mediate direct defense responses. Plant Physiol 142:1751–1758

    Article  PubMed  CAS  Google Scholar 

  • Schmidt S, Baldwin IT (2009) Down-regulation of systemin after herbivory is associated with increased root allocation and competitive ability in Solanum nigrum. Oecologia 159:473–482

    Article  PubMed  Google Scholar 

  • Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D, Carrington JC (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:e230

    Article  PubMed  CAS  Google Scholar 

  • Schowalter TD, Hargrove WW, Crossley DA (1986) Herbivory in forested ecosystems. Annu Rev Entomol 31:177–196

    Article  Google Scholar 

  • Schwachtje J, Minchin PE, Jahnke S, van Dongen JT, Schittko U, Baldwin IT (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci USA 103:12935–12940

    Article  PubMed  CAS  Google Scholar 

  • 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 270:1988–1992

    Article  PubMed  CAS  Google Scholar 

  • Seo S, Sano H, Ohashi Y (1999) Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell 11:289–298

    PubMed  CAS  Google Scholar 

  • Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, Hwang I, Lee JS, Choi YD (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA 98:4788–4793

    Article  PubMed  CAS  Google Scholar 

  • Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J (2006) Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc Natl Acad Sci USA 103:16672–16676

    Article  PubMed  CAS  Google Scholar 

  • Shulaev V, Silverman P, Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385:718–721

    Article  CAS  Google Scholar 

  • Snoeren TA, Mumm R, Poelman EH, Yang Y, Pichersky E, Dicke M (2010) The herbivore-induced plant volatile methyl salicylate negatively affects attraction of the parasitoid Diadegma semiclausum. J Chem Ecol 36:479–489

    Article  PubMed  CAS  Google Scholar 

  • Spoel SH, Loake GJ (2011) Redox-based protein modifications: the missing link in plant immune signalling. Curr Opin Plant Biol 14:358–364

    Article  PubMed  CAS  Google Scholar 

  • Stahl E (1888) Pfianzen und Scbnecken. Biologische Studie ueber die Scbutzmittel der Pfianzen gegen Scbneckenfrass. Jenaische Zeitschrift fuer Naturwissenschaft 22:557–685

    Google Scholar 

  • Stahlberg R, Cosgrove DJ (1997) The propagation of slow wave potentials in pea epicotyls. Plant Physiol 113:209–217

    PubMed  CAS  Google Scholar 

  • Stamler JS (1995) S-nitrosothiols and the bioregulatory actions of nitrogen oxides through reactions with thiol groups. Curr Top Microbiol Immunol 196:19–36

    Article  PubMed  CAS  Google Scholar 

  • Stankovic B, Davies E (1996) Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett 390:275–279

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627

    Article  PubMed  CAS  Google Scholar 

  • Steppuhn A, Baldwin IT (2008) Induced defenses and the cost-benefit paradigm. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Germany, pp 61–83

    Chapter  Google Scholar 

  • Stitz M, Baldwin IT, Gaquerel E (2011) Diverting the flux of the JA pathway in Nicotiana attenuata compromises the plant’s defense metabolism and fitness in nature and glasshouse. PLoS One 6:e25925

    Article  PubMed  CAS  Google Scholar 

  • Stratmann JW (2003) Long distance run in the wound response—jasmonic acid is pulling ahead. Trends Plant Sci 8:247–250

    Article  PubMed  CAS  Google Scholar 

  • Stratmann JW, Ryan CA (1997) Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. Proc Natl Acad Sci USA 94:11085–11089

    Article  PubMed  CAS  Google Scholar 

  • Stratmann J, Paputsoglu G, Oertel W (1996) Differentiation of Ulva mutabilis (Chlorophyta) gametangia and gamete release are controlled by extracellular inhibitors. J Phycol 32:1009–1021

    Article  CAS  Google Scholar 

  • Suza WP, Staswick PE (2008) The role of JAR1 in jasmonoyl-L-isoleucine production in Arabidopsis wound response. Planta 227:1221–1232

    Article  PubMed  CAS  Google Scholar 

  • Suza WP, Rowe ML, Hamberg M, Staswick PE (2010) A tomato enzyme synthesizes (+)-7-iso-jasmonoyl-L-isoleucine in wounded leaves. Planta 231:717–728

    Article  PubMed  CAS  Google Scholar 

  • Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956

    Article  PubMed  CAS  Google Scholar 

  • Tejeda-Sartorius M, Martínez de la Vega O, Délano-Frier J (2008) Jasmonic acid influences mycorrhizal colonization in tomato plants by modifying the expression of genes involved in carbohydrate partitioning. Physiol Plant 133:339–353

    Article  PubMed  CAS  Google Scholar 

  • Thaler JS, Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85:48–58

    Article  Google Scholar 

  • Thaler JS, Fidantsef AL, Bostock RM (2002) Antagonism between jasmonate- and salicylate-mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato. J Chem Ecol 28:1131–1159

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Theodoulou FL, Job K, Slocombe SP, Footitt S, Holdsworth M, Baker A, Larson TR, Graham IA (2005) Jasmonoic acid levels are reduced in COMATOSE ATP-binding cassette transporter mutants. Implications for transport of jasmonate precursors into peroxisomes. Plant Physiol 137:835–840

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755–766

    Article  PubMed  CAS  Google Scholar 

  • Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annu Rev Entomol 36:65–89

    Article  Google Scholar 

  • Tortiglione C, Fogliano V, Ferracane R, Fanti P, Pennacchio F, Monti LM, Rao R (2003) An insect peptide engineered into the tomato prosystemin gene is released in transgenic tobacco plants and exerts biological activity. Plant Mol Biol 53:891–902

    Article  PubMed  CAS  Google Scholar 

  • Toth GB, Pavia H (2007) Induced herbivore resistance in seaweeds: a meta-analysis. J Ecol 95:425–434

    Article  Google Scholar 

  • Truitt CL, Pare PW (2004) In situ translocation of volicitin by beet armyworm larvae to maize and systemic immobility of the herbivore elicitor in planta. Planta 218:999–1007

    Article  PubMed  CAS  Google Scholar 

  • Turlings TC, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253

    Article  PubMed  CAS  Google Scholar 

  • Van Dam NM, Horn M, Mareš M, Baldwin IT (2001) Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 27:547–568

    Article  PubMed  Google Scholar 

  • van Eck L, Schultz T, Leach JE, Scofield SR, Peairs FB, Botha AM, Lapitan NHV (2010) Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance. Plant Biotechnol J 8:1023–1032

    Article  PubMed  CAS  Google Scholar 

  • Verhage A, Vlaardingerbroek I, Raaymakers C, Van Dam NM, Dicke M, Van Wees SCM, Pieterse CMJ (2011) Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory. Front Plant Sci 2:47

    Article  PubMed  Google Scholar 

  • von Dahl CC, Baldwin IT (2007) Deciphering the role of ethylene in plant-herbivore interactions. J Plant Growth Reg 26:201–209

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866

    Article  PubMed  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  PubMed  CAS  Google Scholar 

  • Weber H, Vick BA, Farmer EE (1997) Dinor-oxo-phytodienoic acid: a new hexadecanoid signal in the jasmonate family. Proc Natl Acad Sci USA 94:10473–10478

    Article  PubMed  CAS  Google Scholar 

  • Wei Z, Hu W, Lin Q, Cheng X, Tong M, Zhu L, Chen R, He G (2009) Understanding rice plant resistance to the brown planthopper (Nilaparvata lugens): a proteomic approach. Proteomics 9:2798–2808

    Article  PubMed  CAS  Google Scholar 

  • Wichard T, Göbel C, Feussner I, Pohnert G (2005) Unprecedented lipoxygenase/hydroperoxide lyase pathways in the moss Physcomitrella patens. Angew Chem Int Ed 44:158–161

    Article  CAS  Google Scholar 

  • Wildon DC, Thain JF, Minchin PEH, Gubb IR, Reilly AJ, Skipper YD, Doherty HM, O’Donnell PJ, Bowles DJ (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360:62–65

    Article  CAS  Google Scholar 

  • Will T, van Bel AJE (2008) Induction as well as suppression: How aphid saliva may exert opposite effects on plant defense. Plant Signal Behav 3:427–430

    Article  PubMed  Google Scholar 

  • Wittstock U, Gershenzon J (2002) Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr Opin Plant Biol 5:300–307

    Article  PubMed  CAS  Google Scholar 

  • 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 19:1096–1122

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Wang L, Baldwin I (2008) Methyl jasmonate-elicited herbivore resistance: does MeJA function as a signal without being hydrolyzed to JA? Planta 227:1161–1168

    Article  PubMed  CAS  Google Scholar 

  • Wünsche H, Baldwin IT, Wu J (2011) S-Nitrosoglutathione reductase (GSNOR) mediates the biosynthesis of jasmonic acid and ethylene induced by feeding of the insect herbivore Manduca sexta and is important for jasmonate-elicited responses in Nicotiana attenuata. J Exp Bot 62:4605–4616

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi Y, Huffaker A (2011) Endogenous peptide elicitors in higher plants. Curr Opin Plant Biol 14:351–357

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi Y, Pearce G, Ryan CA (2006) The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc Natl Acad Sci USA 103:10104–10109

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22:508–522

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi Y, Barona G, Ryan CA, Pearce G (2011) GmPep914, an eight-amino acid peptide isolated from soybean leaves, activates defense-related genes. Plant Physiol 156:932–942

    Article  PubMed  CAS  Google Scholar 

  • Zangerl AR (1999) Locally-induced responses in plants: The ecology and evolution of restrained defense. In: Agrawal AA, Tuzun S, Bent E (eds) Induced plant defenses against pathogens and herbivores. APS Press, St. Paul, Minnesota, pp 231–249

    Google Scholar 

  • Zangerl AR, Rutledge CE (1996) The probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. Am Nat 147:599–608

    Article  Google Scholar 

  • Zimmermann MR, Maischak H, Mithofer A, Boland W, Felle HH (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol 149:1593–1600

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

J.W.S. was supported by National Science Foundation grant IOS-0745545.

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Authors and Affiliations

  1. Unit for Plant Biotechnology and Genetic Engineering, Center for Research and Advanced Studies (Cinvestav) at Irapuato, 36821, Irapuato, Gto., Mexico

    John P. Delano-Frier

  2. Division of Natural Sciences and Mathematics, Lewis-Clark State College, 500 8th Ave., Lewiston, ID, 83501, USA

    Gregory Pearce

  3. Chemistry Research Unit, USDA-ARS Center for Medical, Agricultural & Veterinary Entomology, 1700 SW 23rd Dr, Gainesville, FL, 32608, USA

    Alisa Huffaker

  4. Department of Biological Sciences, University of South Carolina, Coker Life Science Bldg 715 Sumter Street, Columbia, SC, 29208, USA

    Johannes W. Stratmann

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  1. John P. Delano-Frier
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  2. Gregory Pearce
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  4. Johannes W. Stratmann
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Correspondence to Gregory Pearce .

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  1. University of Bonn, IZMB, Kirschallee 1, Bonn, 53115, Nordrhein-Westfalen, Germany

    František Baluška

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Delano-Frier, J.P., Pearce, G., Huffaker, A., Stratmann, J.W. (2013). Systemic Wound Signaling in Plants. In: Baluška, F. (eds) Long-Distance Systemic Signaling and Communication in Plants. Signaling and Communication in Plants, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36470-9_17

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