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The Role of Roots in Plant Defense Responses to Aboveground Herbivores

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Part of the book series: Soil Biology ((SOILBIOL,volume 40))

Abstract

Plants have developed sophisticated strategies to protect themselves against insect herbivores. The impact insect herbivores cause on world agriculture has resulted in intense research on plant defense mechanisms against insect herbivory. Roots are increasingly being recognized as important contributors to plant defenses not only against belowground insect herbivores but also against aboveground herbivores (AGH). Transcriptional profiling of roots during AGH has revealed that plants are capable of fine-tuning their response depending on which part of the plant, the root or the shoot, is under attack. Roots also serve as the sites of synthesis of numerous defensive compounds that exert anti-herbivore effects in the shoots. Roots act as sites of storage during herbivore induced resource sequestration. The interaction of roots with a wide variety of soil microbes also influences the outcome of plant–insect interactions. This chapter summarizes the current status of research on roots as important contributors to plant defense against AGH.

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References

  • Ankala A, Luthe D, Williams W, Wilkinson J (2009) Integration of ethylene and jasmonic acid signaling pathways in the expression of maize defense protein Mir1-CP. Mol Plant Microbe Interact 22:1555–1564

    CAS  PubMed  Google Scholar 

  • Ankala A, Kelley RY, Rowe DE, Williams WP, Luthe DS (2013) Foliar herbivory triggers local and long distance defense responses in maize. Plant Sci 199–200:103–112

    PubMed  Google Scholar 

  • Babikova Z, Johnson D, Bruce T, Pickett JA, Gilbert L (2013a) How rapid is aphid-induced signal transfer between plants via common mycelial networks? Commun Integr Biol 6:e25904

    PubMed Central  PubMed  Google Scholar 

  • Babikova Z, Gilbert L, Bruce TJ, Birkett M, Caulfield JC, Woodcock C, Pickett JA, Johnson D (2013b) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol Lett 16:835–843

    PubMed  Google Scholar 

  • Babst BA, Ferrieri RA, Gray DW, Lerdau M, Schlyer DJ, Schueller M, Thorpe MR, Orians CM (2005) Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 167:63–72

    CAS  PubMed  Google Scholar 

  • Babst BA, Ferrieri RA, Thorpe MR, Orians CM (2008) Lymantria dispar herbivory induces rapid changes in carbon transport and partitioning in Populus nigra. Entomol Exp Appl 128:117–125

    CAS  Google Scholar 

  • Bais HP, Loyola-Vargas VM, Flores HE, Vivanco JM (2001) Root-specific metabolism: the biology and biochemistry of underground organs. Vitro Cell Dev Biol Plant 37:730–741

    CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    CAS  PubMed  Google Scholar 

  • Baldwin IT, Schmelz EA, Ohnmeiss TE (1994) Wound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana sylvestris spegazzini and comes. J Chem Ecol 20:2139–2157

    CAS  PubMed  Google Scholar 

  • Barto EK, Weidenhamer JD, Cipollini D, Rillig MC (2012) Fungal superhighways: do common mycorrhizal networks enhance below ground communication? Trends Plant Sci 17:633–637

    CAS  PubMed  Google Scholar 

  • Bednarek P, Piślewska-Bednarek M, Svatoš A, Schneider B, Doubský J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101–106

    CAS  PubMed  Google Scholar 

  • Bent E (2006) Induced systemic resistance mediated by plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF). In: Tuzun S, Bent E (eds) Multigenic and induced systemic resistance in plants. Springer, Berlin, pp 225–258

    Google Scholar 

  • Berenbaum M (1978) Toxicity of a furanocoumarin to armyworms: a case of biosynthetic escape from insect herbivores. Science 201:532–534

    CAS  PubMed  Google Scholar 

  • Bezemer TM, van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624

    PubMed  Google Scholar 

  • Blossey B, Hunt-Joshi TR (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annu Rev Entomol 48:521–547

    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:e1001216

    PubMed Central  PubMed  Google Scholar 

  • Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580

    CAS  PubMed  Google Scholar 

  • Carolan JC, Fitzroy CIJ, Ashton PD, Douglas AE, Wilkinson TL (2009) The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9:2457–2467

    CAS  PubMed  Google Scholar 

  • Chen M-S (2008) Inducible direct plant defense against insect herbivores: A review. Insect Sci 15:101–114

    Google Scholar 

  • Cipollini D, Enright S, Traw M, Bergelson J (2004) Salicylic acid inhibits jasmonic acid‐induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol Ecol 13:1643–1653

    CAS  PubMed  Google Scholar 

  • Dawson RF (1941) The localization of the nicotine synthetic mechanism in the Tobacco plant. Science 94:396–397

    CAS  PubMed  Google Scholar 

  • De Jong TJ, Van Der Meijden E (2000) On the correlation between allocation to defence and regrowth in plants. Oikos 88:503–508

    Google Scholar 

  • De Vos M, Jander G (2009) Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ 32:1548–1560

    PubMed  Google Scholar 

  • Dempsey D, Klessig DF (2012) SOS–too many signals for systemic acquired resistance? Trends Plant Sci 17:538–545

    CAS  PubMed  Google Scholar 

  • Doornbos R, van Loon L, Bakker P (2010) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev 32:227–243

    Google Scholar 

  • Erb M (2009) Modification of plant resistance and metabolism by above-and belowground herbivores. University of Neuchatel, p. 131

    Google Scholar 

  • Erb M (2012) The role of roots in plant defence. In: Mérillon JMM, Ramawat KGG (eds) Plant defence: biological control. Springer, Netherlands, pp 291–309

    Google Scholar 

  • Erb M, Lenk C, Degenhardt J, Turlings TCJ (2009a) The underestimated role of roots in defense against leaf attackers. Trends Plant Sci 14:653–659

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ferrieri AP, Agtuca B, Appel HM, Ferrieri RA, Schultz JC (2013) Temporal changes in allocation and partitioning of new carbon as 11C elicited by simulated herbivory suggest that roots shape aboveground responses in Arabidopsis. Plant Physiol 161:692–704

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fritz M, Jakobsen I, Lyngkjær MF, Thordal-Christensen H, Pons-Kühnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419

    PubMed  Google Scholar 

  • Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297

    PubMed Central  PubMed  Google Scholar 

  • Gómez S, Ferrieri RA, Schueller M, Orians CM (2010) Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytol 188:835–844

    PubMed  Google Scholar 

  • Gómez S, Steinbrenner AD, Osorio S, Schueller M, Ferrieri RA, Fernie AR, Orians CM (2012) From shoots to roots: transport and metabolic changes in tomato after simulated feeding by a specialist lepidopteran. Entomol Exp Appl 144:101–111

    Google Scholar 

  • Halford N, Hey S (2009) Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem J 419:247–259

    CAS  PubMed  Google Scholar 

  • Harmel N, Létocart E, Cherqui A, Giordanengo P, Mazzucchelli G, Guillonneau F, De Pauw E, Haubruge E, Francis F (2008) Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae. Insect Mol Biol 17:165–174

    CAS  PubMed  Google Scholar 

  • He XH, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Crit Rev Plant Sci 22:531–567

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hempel S, Stein C, Unsicker SB, Renker C, Auge H, Weisser WW, Buscot F (2009) Specific bottom–up effects of arbuscular mycorrhizal fungi across a plant–herbivore–parasitoid system. Oecologia 160:267–277

    PubMed Central  PubMed  Google Scholar 

  • Herman M, Nault B, Smart C (2008) Effects of plant growth-promoting rhizobacteria on bell pepper production and green peach aphid infestations in New York. Crop Prot 27:996–1002

    Google Scholar 

  • Hermsmeier D, Schittko U, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth-and defense-related plant mRNAs. Plant Physiol 125:683–700

    CAS  PubMed Central  PubMed  Google Scholar 

  • Holland JN, Cheng W, Crossley D (1996) Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107:87–94

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664

    CAS  PubMed  Google Scholar 

  • Kandoth PK, Mitchum MG (2013) War of the worms: how plants fight underground attacks. Curr Opin Plant Biol 16:457–463

    PubMed  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S, Denno RF (2008) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851

    PubMed  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Karban R, Agrawal AA, Mangel M (1997) The benefits of induced defenses against herbivores. Ecology 78:1351–1355

    Google Scholar 

  • Kehr J, Buhtz A (2008) Long distance transport and movement of RNA through the phloem. J Exp Bot 59:85–92

    CAS  PubMed  Google Scholar 

  • Kehr J, Buhtz A (2012) Endogenous RNA constituents of the phloem and their possible roles in long-distance signaling. In: Thompson GA, van Bel AJE (eds) Phloem: molecular cell biology, systemic communication, biotic interactions. Wiley, Cichester, p 186

    Google Scholar 

  • Kempel A, Brandl R, Schädler M (2009) Symbiotic soil microorganisms as players in aboveground plant–herbivore interactions–the role of rhizobia. Oikos 118:634–640

    Google Scholar 

  • Kobe RK, Iyer M, Walters MB (2010) Optimal partitioning theory revisited: nonstructural carbohydrates dominate root mass responses to nitrogen. Ecology 91:166–179

    PubMed  Google Scholar 

  • Kunkel NB, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    CAS  PubMed  Google Scholar 

  • Lindigkeit R, Biller A, Buch M, Schiebel HM, Boppré M, Hartmann T (1997) The two faces of pyrrolizidine alkaloids: the role of the tertiary amine and its N-Oxide in chemical defense of insects with acquired plant alkaloids. Eur J Biochem 245:626–636

    CAS  PubMed  Google Scholar 

  • Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544

    CAS  PubMed  Google Scholar 

  • Lopez L, Camas A, Shivaji R, Ankala A, Williams P, Luthe D (2007) Mir1-CP, a novel defense cysteine protease accumulates in maize vascular tissues in response to herbivory. Planta 226:517–527

    CAS  PubMed  Google Scholar 

  • Ludwig-Müller J, Schubert B, Pieper K, Ihmig S, Hilgenberg W (1997) Glucosinolate content in susceptible and resistant Chinese cabbage varieties during development of clubroot disease. Phytochemistry 44:407–414

    Google Scholar 

  • Machado RA, Ferrieri AP, Robert CA, Glauser G, Kallenbach M, Baldwin IT, Erb M (2013) Leaf‐herbivore attack reduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling. New Phytol. doi:10.1111/nph.12438

    PubMed  Google Scholar 

  • Major IT, Constabel CP (2007) Shoot-root defense signaling and activation of root defense by leaf damage in poplar. Botany 85:1171–1181

    CAS  Google Scholar 

  • Mauricio R, Rausher MD, Burdick DS (1997) Variation in the defense strategies of plants: Are resistance and tolerance mutually exclusive? Ecology 78:1301–1311

    Google Scholar 

  • Mikkelsen BL, Rosendahl S, Jakobsen I (2008) Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol 180:890–898

    PubMed  Google Scholar 

  • Moll S, Anke S, Kahmann U, Hänsch R, Hartmann T, Ober D (2002) Cell-specific expression of homospermidine synthase, the entry enzyme of the pyrrolizidine alkaloid pathway in Senecio vernalis, in comparison with its ancestor, deoxyhypusine synthase. Plant Physiol 130:47–57

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morita M, Shitan N, Sawada K, Van Montagu MCE, Inzé D, Rischer H, Goossens A, Oksman-Caldentey K-M, Moriyama Y, Yazaki K (2009) Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proc Natl Acad Sci USA 106:2447–2452

    CAS  PubMed Central  PubMed  Google Scholar 

  • Murphy JF, Zehnder GW, Schuster DJ, Sikora EJ, Polston JE, Kloepper JW (2000) Plant growth-promoting rhizobacterial mediated protection in tomato against Tomato mottle virus. Plant Dis 84:779–784

    Google Scholar 

  • Mutti NS, Louis J, Pappan LK, Pappan K, Begum K, Chen M-S, Park Y, Dittmer N, Marshall J, Reese JC, Reeck GR (2008) A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc Natl Acad Sci USA 105:9965–9969

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nalam VJ, Keeretaweep J, Sarowar S, Shah J (2012) Root-derived oxylipins promote green peach aphid performance on Arabidopsis foliage. Plant Cell 24:1643–1653

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nalam VJ, Shah J, Nachappa P (2013) Emerging role of roots in plant responses to aboveground insect herbivory. Insect Sci 20:286–296

    CAS  PubMed  Google Scholar 

  • Ober D, Kaltenegger E (2009) Pyrrolizidine alkaloid biosynthesis, evolution of a pathway in plant secondary metabolism. Phytochemistry 70:1687–1695

    CAS  PubMed  Google Scholar 

  • Orians CM, Thorn A, Gómez S (2011) Herbivore-induced resource sequestration in plants: why bother? Oecologia 167:1–9

    PubMed  Google Scholar 

  • Padmanabhan C, Zhang X, Jin H (2009) Host small RNAs are big contributors to plant innate immunity. Curr Opin Plant Biol 12:465–472

    CAS  PubMed  Google Scholar 

  • Palacio S, Maestro M, Montserrat-Martí G (2007) Seasonal dynamics of non-structural carbohydrates in two species of Mediterranean sub-shrubs with different leaf phenology. Environ Exp Bot 59:34–42

    CAS  Google Scholar 

  • Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569

    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 Biol 5:308–316

    CAS  PubMed  Google Scholar 

  • Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514

    CAS  PubMed  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    CAS  PubMed  Google Scholar 

  • Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Hinanit K, Yoram K (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 193–207

    Google Scholar 

  • Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361

    CAS  Google Scholar 

  • Raps A, Vidal S (1998) Indirect effects of an unspecialized endophytic fungus on specialized plant–herbivorous insect interactions. Oecologia 114:541–547

    Google Scholar 

  • Rasmann S, Agrawal AA (2008) In defense of roots: A research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146:875–880

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schultz JC, Appel HM, Ferrieri AP, Arnold TM (2013) Flexible resource allocation during plant defense responses. Front Plant Sci 4:1–11

    Google Scholar 

  • Schwachtje J, Minchin PEH, 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Selosse MA, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21:621–628

    PubMed  Google Scholar 

  • Shah J (2009) Plants under attack: systemic signals in defence. Curr Opin Plant Biol 12:459–464

    CAS  PubMed  Google Scholar 

  • Shoji T, Yamada Y, Hashimoto T (2000) Jasmonate induction of putrescine N-methyltransferase genes in the root of Nicotiana sylvestris. Plant Cell Physiol 41:831–839

    CAS  PubMed  Google Scholar 

  • Sidwa-Gorycka M, Królicka A, Kozyra M, Głowniak K, Bourgaud F, Łojkowska E (2003) Establishment of a co-culture of Ammi majus L. and Ruta graveolens L. for the synthesis of furanocoumarins. Plant Sci 165:1315–1319

    CAS  Google Scholar 

  • Smith CM (2005) Plant resistance to arthropods: molecular and conventional approaches. Springer, Berlin

    Google Scholar 

  • Soler R, Schaper SV, Bezemer T, Cortesro AM, Hoffmeister TS, Van Der Putten WH, Vet LEM, Harvey JA (2009) Influence of presence and spatial arrangement of belowground insects on host-plant selection of aboveground insects: a field study. Ecol Entomol 34:339–345

    Google Scholar 

  • Soler R, Erb M, Kaplan I (2012a) Long distance root–shoot signalling in plant–insect community interactions. Trends Plant Sci 18:149–156

    PubMed  Google Scholar 

  • Soler R, Van der Putten WH, Harvey JA, Vet LEM, Dicke M, Bezemer TM (2012b) Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms. J Chem Ecol 38:755–767

    CAS  PubMed Central  PubMed  Google Scholar 

  • Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG (2010) Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One 5:e13324

    PubMed Central  PubMed  Google Scholar 

  • Song YY, Ye M, Li CY, Wang RL, Wei XC, Luo SM, Zeng RS (2013) Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J Chem Ecol 39:1036–1044

    PubMed  Google Scholar 

  • Taiz L, Zeiger E (2002) Plant physiology. Sinauer Associates Inc., Sunderland, MA

    Google Scholar 

  • Tao L, Hunter MD (2013) Allocation of resources away from sites of herbivory under simultaneous attack by aboveground and belowground herbivores in the common milkweed, Asclepias syriaca. Arthropod-Plant Interact 7:217–224

    Google Scholar 

  • Thorpe MR, Ferrieri AP, Herth MM, Ferrieri RA (2007) 11C-imaging: methyl jasmonate moves in both phloem and xylem, promotes transport of jasmonate, and of photoassimilate even after proton transport is decoupled. Planta 226:541–551

    CAS  PubMed  Google Scholar 

  • Tjallingii WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot 57:739–745

    CAS  PubMed  Google Scholar 

  • Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60:207–221

    CAS  PubMed  Google Scholar 

  • Tytgat TO, Verhoeven KJ, Jansen JJ, Raaijmakers CE, Bakx-Schotman T, McIntyre LM, van der Putten WH, Biere A, van Dam NM (2013) Plants know where it hurts: root and shoot jasmonic acid induction elicit differential responses in Brassica oleracea. PLoS One 8:e65502

    CAS  PubMed Central  PubMed  Google Scholar 

  • Valenzuela-Soto JH, Estrada-Hernández MG, Ibarra-Laclette E, Délano-Frier JP (2010) Inoculation of tomato plants (Solanum lycopersicum) with growth-promoting Bacillus subtilis retards whitefly Bemisia tabaci development. Planta 231:397–410

    CAS  PubMed  Google Scholar 

  • van Dam NM (2009) Belowground herbivory and plant defenses. Annu Rev Ecol Evol Syst 40:373–391

    Google Scholar 

  • Van Der Heijden MG, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    PubMed  Google Scholar 

  • Van der Putten WH, Vet LEM, Harvey JA, Wäckers FL (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554

    Google Scholar 

  • Van Loon L (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254

    Google Scholar 

  • Van Oosten VR, Bodenhausen N, Reymond P, Van Pelt JA, Van Loon LC, Dicke M, Pieterse CMJ (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol Plant Microbe Interact 21:919–930

    PubMed  Google Scholar 

  • Vidal, S. (1996) Changes in suitability of tomato for whiteflies mediated by a non-pathogenic endophytic fungus. In: Proceedings of the 9th international symposium on insect-plant relationships. Springer, pp 272–274

    Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Walling LL (2009) Adaptive defense responses to pathogens and insects. In: Loon LCV (ed) Advances in botanical research. Academic, London, pp 551–612

    Google Scholar 

  • Welter SC, Steggall JW (1993) Contrasting the tolerance of wild and domesticated tomatoes to herbivory: agroecological implications. Ecol Appl 271–278

    Google Scholar 

  • Will T, Tjallingii WF, Thönnessen A, van Bel AJE (2007) Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci USA 104:10536–10541

    CAS  PubMed Central  PubMed  Google Scholar 

  • Winz RA, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine n-methyltransferase transcripts. Plant Physiol 125:2189–2202

    CAS  PubMed Central  PubMed  Google Scholar 

  • Woldemariam MG, Baldwin IT, Galis I (2011) Transcriptional regulation of plant inducible defenses against herbivores: a mini-review. J Plant Interact 6:113–119

    CAS  Google Scholar 

  • Wu J, Baldwin IT (2009) Herbivory‐induced signalling in plants: perception and action. Plant Cell Environ 32:1161–1174

    CAS  PubMed  Google Scholar 

  • Yamane H, Konno K, Sabelis M, Takabayashi J, Sassa T, Oikawa H (2010) Chemical defence and toxins of plants. In: Mander L, Lui HW (eds) Comprehensive natural products II: Chemistry and biology, vol 4. Elsevier, Amsterdam, pp 339–385

    Google Scholar 

  • Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu-Salzman K, Liu T (2011) Insect herbivory-inducible proteins confer post-ingestive plant defenses. In: Liu T, Kang L (eds) Recent advances in entomological research: from molecular biology to pest management, vol 34. Springer, Heidelberg

    Google Scholar 

  • Zhu-Salzman K, Bi J-L, Liu T-X (2005) Molecular strategies of plant defense and insect counter-defense. Insect Sci 12:3–15

    CAS  Google Scholar 

  • Ziegler J, Facchini PJ (2008) Alkaloid biosynthesis: metabolism and trafficking. Annu Rev Plant Biol 59:735–769

    CAS  PubMed  Google Scholar 

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Nalam, V.J., Nachappa, P. (2014). The Role of Roots in Plant Defense Responses to Aboveground Herbivores. In: Morte, A., Varma, A. (eds) Root Engineering. Soil Biology, vol 40. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-54276-3_17

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