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Phytohormone Mediation of Interactions Between Herbivores and Plant Pathogens

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Abstract

Induced plant defenses against either pathogens or herbivore attackers are regulated by phytohormones. These phytohormones are increasingly recognized as important mediators of interactions between organisms associated with plants. In this review, we discuss the role of plant defense hormones in sequential tri-partite interactions among plants, pathogenic microbes, and herbivorous insects, based on the most recent literature. We discuss the importance of pathogen trophic strategy in the interaction with herbivores that exhibit different feeding modes. Plant resistance mechanisms also affect plant quality in future interactions with attackers. We discuss exemplary evidence for the hypotheses that (i) biotrophic pathogens can facilitate chewing herbivores, unless plants exhibit effector-triggered immunity, but (ii) facilitate or inhibit phloem feeders. (iii) Necrotrophic pathogens, on the other hand, can inhibit both phloem feeders and chewers. We also propose herbivore feeding mode as predictor of effects on pathogens of different trophic strategies, providing evidence for the hypotheses that (iv) phloem feeders inhibit pathogen attack by increasing SA induction, whereas (v) chewing herbivores tend not to affect necrotrophic pathogens, while they may either inhibit or facilitate biotrophic pathogens. Putting these hypotheses to the test will increase our understanding of phytohormonal regulation of plant defense to sequential attack by plant pathogens and insect herbivores. This will provide valuable insight into plant-mediated ecological interactions among members of the plant-associated community.

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References

  • Ali JG, Agrawal A (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302

    CAS  PubMed  Google Scholar 

  • Al-Naemi F, Hatcher PE (2013) Contrasting effects of necrotrophic and biotrophic plant pathogens on the aphid Aphis fabae. Entomol Exp Appl 148:234–245

    Google Scholar 

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844

    CAS  PubMed  Google Scholar 

  • Bacher S, Friedli J, Schär I (2002) Developing in diseased host plants increases survival and fecundity in a stem-boring weevil. Entomol Exp Appl 103:191–195

    Google Scholar 

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

    CAS  PubMed  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

    PubMed  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2013) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240

    PubMed  Google Scholar 

  • Bidart-Bouzat MG, Kliebenstein D (2011) An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores. Oecologia 167:677–689

    PubMed  Google Scholar 

  • Biere A, Bennett AE (2013) Three-way interactions between plants, microbes and insects. Funct Ecol 27:567–573

    Google Scholar 

  • Boege K (2005) Influence of plant ontogeny on compensation to leaf damage. Am J Bot 92:1632–1640

    PubMed  Google Scholar 

  • Bonaventure G (2012) Perception of insect feeding by plants. Plant Biol 14:872–880

    CAS  PubMed  Google Scholar 

  • 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:e1001126–e1001216

    Google Scholar 

  • Broekgaarden C, Voorrips RE, Dicke M, Vosman B (2011) Transcriptional responses of Brassica nigra to feeding by specialist insects of different feeding guilds. Insect Sci 18:259–272

    CAS  Google Scholar 

  • Brooks DM, Hernández-Guzmán G, Kloek AP, Alarcón-Chaidez F, Sreedharan A, Rangaswamy V et al (2004) Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringae pv. tomato DC3000. Molec Plant Microbe Interact 17:162–74

    CAS  Google Scholar 

  • Casteel C and Hansen AK (2014) Many hands make light work, but which ones? Evaluating insect-microbiomes at the plant-insect interface. J Chem Ecol In Press (this issue)

  • Cooper WC, Jia L, Goggin FL (2004) Acquired and R-gene-mediated resistance against the potato aphid in tomato. J Chem Ecol 30:2527–42

    CAS  PubMed  Google Scholar 

  • Cui J, Jander G, Racki LR, Kim PD, Pierce NE, Ausubel FM (2002) Signals involved in Arabidopsis resistance to Trichoplusia ni caterpillars induced by virulent and avirulent strains of the phytopathogen pseudomonas syringae. Plant Physiol 129:551–564

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, Pierce NE et al (2005) Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci U S A 102:1791–1796

    CAS  PubMed Central  PubMed  Google Scholar 

  • De Ilarduya OM, Xie Q, Kaloshian I (2003) Aphid-induced defense responses in Mi-1 -mediated compatible and incompatible tomato interactions. Molec Plant Microbe Interact 16:699–708

    Google Scholar 

  • De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ et al (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molec Plant Microbe Interact 18:923–937

    Google Scholar 

  • De Vos M, Van Zaanen W, Koornneef A, Korzelius JP, Dicke M, Van Loon LC et al (2006) Herbivore-induced resistance against microbial pathogens in arabidopsis. Plant Physiol 142:352–363

    PubMed Central  PubMed  Google Scholar 

  • Dicke M, Van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324

    CAS  PubMed  Google Scholar 

  • Ehrlich PR, Raven PH (1964) Butterflies and plants : a study in coevolution. Evolution 18:586–608

    Google Scholar 

  • Erb M, Meldau S, Howe G (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259

    CAS  PubMed Central  PubMed  Google Scholar 

  • Frago E, Dicke M, Godfray HCJ (2012) Insect symbionts as hidden players in insect-plant interactions. Trends Ecol Evol 27:705–711

    PubMed  Google Scholar 

  • Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863

    CAS  PubMed  Google Scholar 

  • Gimenez-Ibanez S, Solano R (2013) Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Front Plant Sci 4:1–11

    Google Scholar 

  • Giron D, Frago E, Glevarec G, Pieterse CMJ, Dicke M (2013) Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence. Funct Ecol 27:599–609

    Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–27

    CAS  PubMed  Google Scholar 

  • Goggin FL (2007) Plant-aphid interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10:399–408

    CAS  PubMed  Google Scholar 

  • Govrin EM, Levine A (2002) Infection of Arabidopsis with a necrotrophic pathogen, Botrytis cinerea, elicits various defense responses but does not induce systemic acquired resistance (SAR). Plant Mol Biol 48:267–76

    CAS  PubMed  Google Scholar 

  • Groen SC, Whiteman NK, Bahrami AK, Wilczek AM, Cui J, Russell JA et al (2013) Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis. Plant Cell 25:4755–4766

    CAS  PubMed  Google Scholar 

  • Grover PB, Shukle RH, Foster JE (1989) Interactions of Hessian fly (Diptera: Cecidomyiidae) biotypes on resistant wheat. Environ Entomol 18:687–690

    Google Scholar 

  • Guerrieri E, Digilio MC (2008) Aphid-plant interactions: a review. J Plant Interact 3:223–232

    Google Scholar 

  • Gururani MA, Venkatesh J, Upadhyaya CP, Nookaraju A, Pandey SK, Park SW (2012) Plant disease resistance genes: current status and future directions. Physiol Mol Plant Pathol 78:51–65

    CAS  Google Scholar 

  • Harrison MA (2012) Phytohormones and abiotic stress tolerance in plants. Springer, Berlin Heidelberg

    Google Scholar 

  • Hatcher PE, Moore J, Taylor JE, Tinney GW, Paul ND (2004) Phytohormones and plant-herbivore-pathogen-interactions: integrating the molecular with the ecological. Ecology 85:59–69

    Google Scholar 

  • Hogenhout S, Bos JIB (2011) Effector proteins that modulate plant-insect interactions. Curr Opin Plant Biol 14:422–428

    CAS  PubMed  Google Scholar 

  • Hogenhout S, Ammar E-D, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–59

    CAS  PubMed  Google Scholar 

  • Hopkins RJ, Van Dam NM, Van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Huffaker A, Pearce G, Veyrat N, Erb M, Turlings TCJ, Sartor R, Shen Z, Briggs SP, Vaughan MM, Alborn HT, Teal PEA, Schmelz EA (2013) Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. Proc Natl Acad Sci U S A 110:5707–5712

  • Humphrey PT, Nguyen TT, Villalobos MM, Whiteman NK (2014) Diversity and abundance of phyllosphere bacteria are linked to insect herbivory. Molec Ecol 23:1497–515

    CAS  Google Scholar 

  • Jiang RHY, Tyler BM (2012) Mechanisms and evolution of virulence in oomycetes. Annu Rev Phytopathol 50:295–318

    CAS  PubMed  Google Scholar 

  • Johansson ON, Fantozzi E, Fahlberg P, Nilsson AK, Buhot N, Tör M, et al. (2014) Role of the penetration resistance genes PEN1, PEN2 and PEN3 in the hypersensitive response and race specific resistance in Arabidopsis thaliana. The Plant Journal In Press

  • Johnson SN, Douglas AE, Woodward S, Hartley SE (2003) Microbial impacts on plant-herbivore interactions: the indirect effects of a birch pathogen on a birch aphid. Oecologia 134:388–396

    PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nat Rev 444:323–329

    CAS  Google Scholar 

  • Kanno H, Fujita Y (2003) Induced systemic resistance to rice blast fungus in rice plants infested by white-backed planthopper. Entomol Exp Appl 107:155–158

    Google Scholar 

  • Kanno H, Satoh M, Kimura T, Fujita Y (2005) Some aspects of induced resistance to rice blast fungus, Magnaporthe grisea, in rice plant infested by white-backed planthopper, Sogatella furcifera. Appl Entomol Zool 40:91–97

    Google Scholar 

  • Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994

    PubMed  Google Scholar 

  • Kawazu K, Mochizuki A, Sato Y, Sugeno W, Murata M, Seo S et al (2012) Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod-Plant Interact 6:221–230

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kliebenstein DJ, Rowe HC (2008) Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction. Plant Sci 174:551–556

    CAS  Google Scholar 

  • Kuśnierczyk 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 Environt 31:1097–115

    Google Scholar 

  • Lai Z, Mengiste T (2013) Genetic and cellular mechanisms regulating plant responses to necrotrophic pathogens. Curr Opin Plant Biol 16:505–512

    CAS  PubMed  Google Scholar 

  • Laluk K, Mengiste T (2010) Necrotroph attacks on plants: wanton destruction or covert extortion? the Arabidopsis book. Am Soc Plant Biol 8:1–34

    Google Scholar 

  • Latijnhouwers M, de Wit PJGM, Govers F (2003) Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol 11:462–469

    CAS  PubMed  Google Scholar 

  • Lawrence R, Potts BM, Whitham TG (2003) Relative importance of plant ontogeny, host genetic variation, and leaf age for a common herbivore. Ecology 84:1171–1178

    Google Scholar 

  • Lee B, Lee S, Ryu C-M (2012) Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper. Ann Bot 110:281–290

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li Q, Xie Q-G, Smith-Becker J, Navarre DA, Kaloshian I (2006) Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Molec Plant Microbe Interact 19:655–664

    CAS  Google Scholar 

  • Maffei ME, Mithöfer A, Boland W (2007) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68:2946–2959

    CAS  PubMed  Google Scholar 

  • Mai VC, Drzewiecka K, Jeleń H, Narożna D, Rucińska-Sobkowiak R, Kęsy J et al (2014) Differential induction of Pisum sativum defense signaling molecules in response to pea aphid infestation. Plant Sci 221–222:1–12

    PubMed  Google Scholar 

  • Mayer RT, Inbar M, McKenzie CL, Shatters R, Borowicz V, Albrecht U et al (2002) Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivores, and phytopathogens. Arch Insect Biochem Physiol 51:151–169

    CAS  PubMed  Google Scholar 

  • Mengiste T (2012) Plant immunity to necrotrophs. Annu Rev Phytopathol 50:267–294

    CAS  PubMed  Google Scholar 

  • Mishina TE, Zeier J (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50:500–513

    CAS  PubMed  Google Scholar 

  • Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450

    PubMed  Google Scholar 

  • Mok DWS, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mouttet R, Bearez P, Thomas C, Desneux N (2011) Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions. PLoS One 6:e18840

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mouttet R, Kaplan I, Bearez P, Amiens-Desneux E, Desneux N (2013) Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites. Oecologia 173:1379–86

    PubMed  Google Scholar 

  • Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105

    Google Scholar 

  • Oliver RP, Solomon PS (2010) New developments in pathogenicity and virulence of necrotrophs. Currt Opin Plant Biol 13:415–419

    CAS  Google Scholar 

  • Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–42

    CAS  PubMed  Google Scholar 

  • Paine TD, Raffa KF, Harrington TC (1997) Interactions among Scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42:179–206

    CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–9

    CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Bio 5:308–16

    CAS  Google Scholar 

  • Pieterse CMJ, der Does D, Van ZC, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Devel Biol 28:489–521

    CAS  Google Scholar 

  • Poelman EH, Van Loon JJA, Dicke M (2008) Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci 13:1360–1385

    Google Scholar 

  • Ponzio C, Gols R, Pieterse CMJ, Dicke M (2013) Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Funct Ecol 27:587–598

    Google Scholar 

  • Ponzio C, Gols R, Weldegergis BT and Dicke M (2014) Caterpillar-induced plant volatiles remain a reliable signal for foraging wasps during dual attack with a plant pathogen or non-host insect herbivore. Plant, Cell Environ In Press

  • Rostás M, Hilker M (2002) Asymmetric plant-mediated cross-effects between a herbivorous insect and a phytopathogenic fungus. Agric For Entomol 4:223–231

    Google Scholar 

  • Rostás M, Simon M, Hilker M (2003) Ecological cross-effects of induced plant responses towards herbivores and phytopathogenic fungi. Basic Appl Ecol 4:43–62

    Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–49

    CAS  PubMed  Google Scholar 

  • Satoh M, Gomi K, Matsumura M, Takabayashi J, Sasaki K, Ohashi Y, et al. (2009) Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. In: Heong KL and Hardy B (eds) International rice research institute, 327–340.

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schoonhoven LM, Van Loon JJA, Dicke M (2005) Insect-plant biology. Press, Oxford University

    Google Scholar 

  • Shapiro LR, Salvaudon L, Mauck KE, Pulido H, De Moraes CM, Stephenson AG et al (2013) Disease interactions in a shared host plant: effects of pre-existing viral infection on cucurbit plant defense responses and resistance to bacterial wilt disease. PLoS One 8:1–10

    Google Scholar 

  • Simon M, Hilker M (2003) Herbivores and pathogens on willow: do they affect each other? Agric For Entomol 5:275–284

    Google Scholar 

  • Simon M, Hilker M (2005) Does rust infection of willow affect feeding and oviposition behavior of willow leaf beetles? J Insect Behav 18:115–129

    Google Scholar 

  • Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A 104:18842–7

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stam JM, Kroes A, Li Y, Gols R, Van Loon JJA, Poelman EH et al (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:1–25

    Google Scholar 

  • Stout MJ, Thaler JS, Thomma BPHJ (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51:663–89

    CAS  PubMed  Google Scholar 

  • Sugio A, Kingdom HN, Maclean AM, Grieve VM, Hogenhout SA (2011) Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proc Natl Acad Sci U S A 108:1254–1263

    Google Scholar 

  • Tack AJM, Dicke M (2013) Plant pathogens structure arthropod communities across multiple spatial and temporal scales. Funct Ecol 27:633–645

    Google Scholar 

  • Thaler JS, Owen B, Higgins VJ (2004) The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol 135:530–538

    CAS  PubMed Central  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378

    CAS  PubMed Central  PubMed  Google Scholar 

  • Turlings TC, Loughrin JH, Mccall PJ, Röse US, Lewis JW et al (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci U S A 92:4169–4174

    CAS  PubMed Central  PubMed  Google Scholar 

  • Utsumi S, Ando Y, Miki T (2010) Linkages among trait-mediated indirect effects: a new framework for the indirect interaction web. Pop Ecol 52:485–497

    Google Scholar 

  • Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390

    PubMed Central  PubMed  Google Scholar 

  • Veronese P, Nakagami H, Bluhm B, AbuQuamar S, Chen X, Salmeron J et al (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18:257–273

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172

    Google Scholar 

  • Vleeshouwers VG, Raffaele S, Vossen JH, Champouret N, Oliva R, Segretin ME et al (2011) Understanding and exploiting late blight resistance in the age of effectors. Annu Rev Phytopathol 49:507–531

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Walling LL (2009) Adaptive defense responses to pathogens and insects. Adv Bot Res 51:551–612

    CAS  Google Scholar 

  • Xu YI, Chang P-FL, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM et al (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077–1085

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang JW, Yi HS, Kim H, Lee B, Lee S, Ghim SY et al (2011) Whitefly infestation of pepper plants elicits defence responses against bacterial pathogens in leaves and roots and changes the below-ground microflora. J Ecol 99:46–56

    CAS  Google Scholar 

  • Zhang T, Luan J-B, Qi J-F, Huang C-J, Li M, Zhou X-P et al (2012) Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Molec Ecol 21:1294–1304

    Google Scholar 

  • Zhang P-J, Broekgaarden C, Zheng S-J, Snoeren TAL, Van Loon JJA, Gols R et al (2013) Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol 197:1291–1299

    CAS  PubMed  Google Scholar 

  • Ziebell H, Murphy AM, Groen SC, Tungadi T, Westwood JH, Lewsey MG et al (2011) Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco. Sci Rep 1:187

    PubMed Central  PubMed  Google Scholar 

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Lazebnik, J., Frago, E., Dicke, M. et al. Phytohormone Mediation of Interactions Between Herbivores and Plant Pathogens. J Chem Ecol 40, 730–741 (2014). https://doi.org/10.1007/s10886-014-0480-7

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