Abstract
Plants are the major food source for most insects. While insects have developed various feeding strategies, plants respond by activating distinct signaling pathways resulting in the production of defensive compounds. Important regulators in this signaling system are compounds in the insect saliva, which are often modified plant molecules. The perception of these elicitor initiates signaling events like calcium release, oxidative burst, and several protein kinases, resulting in the activation of the octadecanoid signaling pathway with jasmonic acid (JA) as the major regulator of herbivore-specific defense response. JA is essential in inducing the production of toxic secondary metabolites, volatile organic compounds, and antidigestive proteins like proteinase inhibitors and polyphenol oxidases. Additionally, natural enemies of the attacking insect herbivore are attracted by volatiles release or the production of extrafloral nectar. Taken together, these measures provide a broad protection against insect herbivores. A detailed understanding of the underlying mechanisms will give us new insights into the coevolutionary processes that govern plant-insect interactions and may also lead to new approaches for the development of more ecological pest management strategies in an increasing agricultural environment.
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References
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
Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH, Schmelz EA, Teal PE (2007) Disulfooxy fatty acids from the American bird grasshopper schistocerca Americana, elicitors of plant volatiles. Proc Natl Acad Sci USA 104:12976–12981
Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defense genes in lima bean leaves. Nature 406:512–515
Arimura G, 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 Physiol 146:965–973
Baldwin IT (1990) Herbivory simulations in ecological research. Trends Ecol Evol 5:91–93
Baldwin IT, Schultz JC (1983) Rapid changes in tree leaf chemistry induced by damage-evidence for communication between plants. Science 221:277–279
Bate NJ, Rothstein SJ (1998) C-6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J 16:561–569
Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory—primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511–1530
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
Chen H, Gonzales-Vigil E, Wilkerson CG, Howe GA (2007) Stability of plant defense proteins in the gut of insect herbivores. Plant Physiol 143:1954–1967
Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, GarcÃa-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671
Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant–pathogen interactions. TIPS 7:210–216
Constabel CP, Bergey DR, Ryan CA (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 92:407–411
Croft KPC, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from phaseolus vulgaris (L.) leaves inoculated with pseudomonas syringae pv phaseolicola. Plant Physiol 101:13–24
De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580
Dogimont C, Bendahmane A, Pitrat M, Burget-Bigeard E, Hagen L, et al. (2007) U.S. Patent No. 20,070,016,977
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
Du B, Zhang W, Liu B, Hu J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, He G (2009) Identification and characterization of Bph14, a gene conferring resistance to brown plant hopper in rice. Proc Natl Acad Sci USA 106:22163–22168
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
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. MPMI 20:707–716
Felton GW, Bi JL, Summers CB, Mueller AJ, Duffey SS (1994) Potential role of lipoxygenases in defense against insect herbivory. J Chem Ecol 20:651–666
Frey M, Chomet P, Glawischnig E, Stettner C, Grun S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277:696–699
Gardener HW, Dornbos DL, Desjardins AE (1990) Hexanal, trans-2-hexenal, and trans-2-nonenal inhibit soybean, glycine max, seed germination. J Agri Food Chem 38:1316–1320
Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169
Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves—possible defense mechanism against insects. Science 175:776–777
Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore manduca sexta (Lepidoptera, sphingidae) and its natural host nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717
Halitschke R, Ziegler J, Keinänen M, Baldwin IT (2004) Silencing of hydroperoxide lyase and allene oxide synthase reveals substrate and defense signaling crosstalk in nicotiana attenuata. Plant J 40:35–46
Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333
Heil M, Bueno CS (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
Hildebrand DF, Brown GC, Jackson DM, Hamilton-Kemp TR (1993) Effects of some leaf-emitted volatile compounds on aphid population increase. J Chem Ecol 19:1875–1887
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66
Jones JDG, Dangle JL (2006) The plant immune system. Nature 444:323–329
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
Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against manduca sexta. Plant Cell 18:3303–3320
Karban R, Baldwin IT (1997) Induced responses to herbivory. University Chicago Press, Chicago
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
Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10:255–266
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144
Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and nicotiana attenuata. Oecologia 148:280–292
Konno K, Hirayama C, Nakamura M, Tateishi K, Tamura Y, Hattori M, Kohno K (2004) Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J 37:370–378
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275
Lee DS, Nioche P, Hamberg M, Raman CS (2008) Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature 455:363–368
Leitner M, Boland W, Mithoefer A (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in medicago truncatula. New Phytol 167:597–606
Levy M, Wang Q, Kaspi R, Parrella MP, Abel S (2005) Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense. Plant J 43:79–96
Lison P, Rodrigo I, Conejero V (2006) A novel function for the cathepsin D inhibitor in tomato. Plant Physiol 142:1329–1339
Maffei M, Bossi S, Spiteller D, Mithoefer 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
Maffei ME, Mithoefer A, Arimura G, 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
Maischak H, Grigoriev PA, Vogel H, Boland W, Mithoefer A (2007) Oral secretions from herbivorous lepidopteran larvae exhibit ion channel-forming activities. FEBS Lett 581:898–904
Malone M, Alarcon JJ, Palumbo L (1994) An hydraulic interpretation of rapid, long-distance wound signaling in the tomato. Planta 193:181–185
Mattiacci L, Dicke M, Posthumous MA (1995) Beta-glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci USA 92:2036–2040
Mendelsohn R, Balick MJ (1995) The value of undiscovered pharmaceuticals in tropical forests. Econ Bot 49:223–228
Mithoefer 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 137:1160–1168
Mohan S, Ma PWK, Pechan T, Bassford ER, Williams WP, Luthe DS (2006) Degradation of the S. Frugiperda peritrophic matrix by an inducible maize cysteine protease. J Insect Physiol 52:21–28
Musser RO, Cipollini DF, Hum-Musser SM, Williams SA, Brown JK, Felton GW (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Archives Insect Biochem Physiol 58:128–137
Nombela G, Williamson VM, Muniz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly bemisia tabaci. MPMI 16:645–649
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
Orozco-Cardenas ML, Narvaez-Vasquez 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
Pare PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167
Pare PW, Alborn HT, Tumlinson JH (1998) Concerted biosynthesis of an insect elicitor of plant volatiles. Proc Natl Acad Sci USA 95:13971–13975
Park YS, Kunze S, Ni X, Feussner I, Kolomiets MW (2010) Comparative molecular and biochemical characterization of segmentally duplicated 9-lipoxygenase genes ZmLOX4 and ZmLOX5 of maize. Planta 231:1425–1437
Pauwels L, Inze D, Goossens A (2009) Jasmonate-inducible gene: what does it mean? Trends Plant Sci 14:87–91
Peiffer M, Tooker JF, Luthe DS, Felton GW (2009) Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184:644–656
Pohnert G, Jung V, Haukioja E, Lempa K, Boland W (1999) New fatty acid amides from regurgitant of lepidopteran (noctuidae, geometridae) caterpillars. Tetrahedron 55:11275–11280
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
Reymond P, Bodenhausen N, Van Poecke RM, Krishnamurthy V, Dicke M, Farmer EE (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–147
Rhoades DF (1983) Responses of alder and willow to attack by tent caterpillars and webworms-evidence for pheromonal sensitivity of willows. ACS Symp Ser 208:55–68
Roese USR, Manukian A, Heath RR, Tumlinson JH (1996) Volatile semiochemicals released from undamaged cotton leaves: a systemic response of living plants to caterpillar damage. Plant Physiol 111:487–495
Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci USA 95:9750–9754
Ryan CA (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28:425–449
Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290
Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377
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
Schmelz EA, LeClere S, Carroll MJ, Alborn HT, Teal PE (2007) Cowpea chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiol 144:793–805
Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH, Teal PE (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc Natl Acad Sci USA 106:653–657
Shen B, Zheng Z, Dooner HK (2000) A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wild-type and mutant alleles. Proc Natl Acad Sci USA 97:14807–14812
Shiojiri K, Ozawa R, Takabayashi J (2006) Plant volatiles, rather than light, determine the nocturnal behavior of a caterpillar. PLoS Biol 4:e164
Spiteller D, Boland W (2003) N-(15,16-dihydroxylinoleoyl)-glutamine and N-(15,16-epoxylinoleoyl)-glutamine isolated from oral secretions of lepidopteran larvae. Tetrahedron 59:135–139
Spiteller D, Oldham NJ, Boland W (2004) N-(17-phosphonooxylinolenoyl)glutamine and N-(17-phosphonooxylinoleoyl)glutamine from insect gut: the first backbone-phosphorylated fatty acid derivatives in nature. J Org Chem 69:1104–1109
Stankovic B, Davies E (1997) Intercellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato. Planta 202:402
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
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu GH, Nomura He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665
Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26
Truitt CL, Wei HX, Pare PW (2004) A plasma membrane protein from Zea Mays binds with the herbivore elicitor volicitin. Plant Cell 16:523–532
Tumlinson JH, Engelberth J (2008) Fatty acid derived signals that induce or regulate plant defenses against herbivory. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Amsterdam, The Netherlands
Turlings TC, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-injured corn. Proc Natl Acad Sci USA 89:8399–8402
Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castanera P, Sanchez-Serrano JJ (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc Natl Acad Sci USA 98:8139–8144
Wang JH, Constabel CP (2004) Polyphenol oxidase overexpression in transgenic populus enhances resistance to herbivory by forest tent caterpillar (malacosoma disstria). Planta 220:87–96
Wang L, Allmann S, Wu J, Baldwin IT (2008) Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of nicotiana attenuata. Plant Physiol 146:904–915
Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24
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
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 lituralis larvae. Proc Natl Acad Sci USA 105:18058–18063
Zavala JA, Patankar AG, Gase K, Hui DQ, Baldwin IT (2004) Manipulation of endogenous trypsin proteinase inhibitor production in nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 134:1181–1190
Zeringue HJ (1992) Effects of C6-C10 alkenals and alkanals on eliciting a defence response in the developing cotton boll. Phytochemistry 31:2305–2308
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 149:1593–1600
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This work was supported by grants from the National Science Foundation (IOS-0925615) and USDA, NIFA (Grant No.03836).
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Engelberth, J. (2012). Plant Resistance to Insect Herbivory. In: Witzany, G., Baluška, F. (eds) Biocommunication of Plants. Signaling and Communication in Plants, vol 14. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-23524-5_16
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