Skip to main content
SpringerLink
Log in

Interactions Involving Rhizobacteria and Foliar-Feeding Insects

  • Chapter
  • First Online:
Aboveground–Belowground Community Ecology

Part of the book series: Ecological Studies ((ECOLSTUD,volume 234))

Abstract

Rhizobacteria are key belowground drivers of plant–insect higher trophic interactions aboveground. Conventionally, rhizobacteria have been studied in the context of their effects on plant growth and yield in agricultural situations. However, the focus of rhizobacterial studies shifted recently to explore their effects on plant biochemistry, defense signaling, the plant microbiome, and insect herbivores. Here, we review the interactions between rhizobacteria and foliar-feeding insects and consider some of the mechanisms by which these interactions occur. To develop a robust understanding of whether and how rhizobacteria govern plant–insect interactions, a multidisciplinary approach involving ecological and -omics approaches is imperative. Such an approach will not only elucidate the key mechanisms underpinning these intricate interactions, including a wide range of variables at spatiotemporal scales, but also open new avenues for their applicability in agricultural and allied fields. This review attempts to (1) synthesize existing knowledge of rhizobacteria–plant–herbivore interactions, (2) identify and address the key issues in the current study systems, and (3) discuss the potential importance of rhizobacteria in insect community ecology.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12

    Article  CAS  Google Scholar 

  • Akhtar MS, Panwar J (2013) Efficacy of root-associated fungi and PGPR on the growth of Pisum sativum (cv. Arkil) and reproduction of the root-knot nematode Meloidogyne incognita. J Basic Microbiol 53:318–326

    Article  CAS  Google Scholar 

  • Aziz M, Nadipalli RK, Xie X et al (2016) Augmenting sulphur metabolism and herbivore defence in Arabidopsis by bacterial volatile signaling. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00458

  • Ballhorn DJ, Kautz S, Schädler M (2013) Induced plant defense via volatile production is dependent on rhizobial symbiosis. Oecologia 172:833–846

    Article  Google Scholar 

  • Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol Adv 16:729–770

    Article  CAS  Google Scholar 

  • Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  CAS  Google Scholar 

  • Boutard-Hunt C, Smart CD, Thaler J et al (2009) Impact of plant growth-promoting rhizobacteria and natural enemies on Myzus persicae (Hemiptera: Aphididae) infestations in pepper. J Econ Entomol 102:2183–2191

    Article  CAS  Google Scholar 

  • Brunner SM, Goos RJ, Swenson SJ et al (2015) Impact of nitrogen fixing and plant growth-promoting bacteria on a phloem-feeding soybean herbivore. Appl Soil Ecol 86:71–81

    Article  Google Scholar 

  • Bukovinszky T, Poelman EH, Gols R et al (2009) Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160:299–308

    Article  Google Scholar 

  • Bulgarelli D, Rott M, Schlaeppi K et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95

    Article  CAS  Google Scholar 

  • Chaudhry V, Sharma S, Bansal K et al (2016) Glimpse into the genomes of rice endophytic bacteria: diversity and distribution of Firmicutes. Front Microbiol 7:2115. https://doi.org/10.3389/fmicb.2016.02115

  • Conn VM, Franco CM (2004) Effect of microbial inoculants on the indigenous actinobacterial endophyte population in the roots of wheat as determined by terminal restriction fragment length polymorphism. Appl Environ Microbiol 70:6407–6413

    Article  CAS  Google Scholar 

  • de Campos SB, Youn JW, Farina R et al (2013) Changes in root bacterial communities associated to two different development stages of canola (Brassica napus L. var oleifera) evaluated through next-generation sequencing technology. Microb Ecol 65:593–601

    Article  Google Scholar 

  • Dean JM, Mescher MC, De Moraes CM (2009) Plant-rhizobia mutualism influences aphid abundance on soybean. Plant Soil 323:187–196

    Article  CAS  Google Scholar 

  • Dean JM, Mescher MC, De Moraes CM (2014) Plant dependence on rhizobia for nitrogen influences induced plant defences and herbivore performance. Int J Mol Sci 15:1466–1480

    Article  Google Scholar 

  • Dudareva N, Negre F, Nagegowda DA et al (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440

    Article  CAS  Google Scholar 

  • Eisenhauer N (2012) Aboveground-belowground interactions as a source of complementarity effects in biodiversity experiments. Plant Soil 351:1–22

    Article  CAS  Google Scholar 

  • Elsas J, Dijkstra A, Govaert J et al (1986) Survival of Pseudomonas fluorescens and Bacillus subtilis introduced into two soils of different texture in field microplots. FEMS Microbiol Lett 38:151–160

    Article  Google Scholar 

  • Friesen ML, Porter SS, Stark SC et al (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46. https://doi.org/10.1146/annurev-ecolsys-102710-145039

    Article  Google Scholar 

  • Gadhave KR (2015) Interactions between plant growth promoting rhizobacteria, foliar-feeding insects and higher trophic levels. PhD Thesis, Royal Holloway, University of London

    Google Scholar 

  • Gadhave KR, Gange AC (2016) Plant-associated Bacillus spp. alter life-history traits of the specialist insect Brevicoryne brassicae L. Agric For Entomol 18:35–42

    Article  Google Scholar 

  • Gadhave KR, Finch P, Gibson TM et al (2016a) Plant growth-promoting Bacillus suppress Brevicoryne brassicae field infestation and trigger density-dependent and density-independent natural enemy responses. J Pest Sci 89:985–992

    Article  Google Scholar 

  • Gadhave KR, Hourston JE, Gange AC (2016b) Developing soil microbial inoculants for pest management: can one have too much of a good thing? J Chem Ecol 42:348–356

    Article  CAS  Google Scholar 

  • Gadhave KR, Devlin PF, Ebertz A et al (2018) Soil inoculation with Bacillus spp. modifies root endophytic bacterial diversity, evenness and community composition in a context specific manner. Microb Ecol. https://doi.org/10.1007/s00248-018-1160-x

    Article  CAS  Google Scholar 

  • Gange AC, Eschen R, Schroeder V (2012) The soil microbial community and plant foliar defences against insects. In: Iason GR, Dicke M, Hartley SE (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp 170–188

    Chapter  Google Scholar 

  • Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Herrmann L, Lesueur D (2013) Challenges of formulation and quality of biofertilizers for successful inoculation. Appl Microbiol Biotechnol 97:8859–8873

    Article  CAS  Google Scholar 

  • Hiltner L (1904) Uber neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter besonderden berucksichtigung und Brache. Arb Dtsch Landwirtsch Gesellschaft 98:59–78

    Google Scholar 

  • Hinsinger P, Bengough AG, Vetterlein D et al (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152

    Article  CAS  Google Scholar 

  • Humphrey PT, Nguyen TT, Villalobos MM et al (2014) Diversity and abundance of phyllosphere bacteria are linked to insect herbivory. Mol Ecol 23:1497–1515

    Article  CAS  Google Scholar 

  • Iavicoli A, Boutet E, Buchala A et al (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant Microbe Interact 16:851–858

    Article  CAS  Google Scholar 

  • Jin H, Yang XY, Yan ZQ et al (2014) Characterization of rhizosphere and endophytic bacterial communities from leaves, stems and roots of medicinal Stellera chamaejasme L. Syst Appl Microbiol 37:376–385

    Article  Google Scholar 

  • Johri B, Sharma A, Virdi J (2003) Rhizobacterial diversity in India and its influence on soil and plant health. Biotechnology 84:49–89

    CAS  Google Scholar 

  • Karthiba L, Saveetha K, Suresh S (2010) PGPR and entomopathogenic fungus bioformulation for the synchronous management of leaffolder pest and sheath blight disease of rice. Pest Manag Sci 66:555–564

    Article  CAS  Google Scholar 

  • Katayama N, Zhang ZQ, Ohgushi T (2011) Community-wide effects of below-ground rhizobia on above-ground arthropods. Ecol Entomol 36:43–51

    Article  Google Scholar 

  • Katayama N, Silva AO, Kishida O et al (2014) Herbivorous insect decreases plant nutrient uptake: the role of soil nutrient availability and association of below-ground symbionts. Ecol Entomol 39:511–518

    Article  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

    Article  Google Scholar 

  • Kröber M, Wibberg D, Grosch R et al (2014) Effect of the strain Bacillus amyloliquefaciens FZB42 on the microbial community in the rhizosphere of lettuce under field conditions analyzed by whole metagenome sequencing. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00252

  • Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci USA 109:14058–14062

    Article  CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  CAS  Google Scholar 

  • Mayer J, Scheid S, Widmer F et al (2010) How effective are ‘effective microorganisms®(EM) results from a field study in temperate climate. Appl Soil Ecol 46:230–239

    Article  Google Scholar 

  • Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663

    Article  CAS  Google Scholar 

  • Niu DD, Liu HX, Jiang CH et al (2011) The plant growth–promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol Plant Microbe Interact 24:533–542

    Article  CAS  Google Scholar 

  • Ongena M, Jourdan E, Adam A et al (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090

    Article  CAS  Google Scholar 

  • Pangesti N, Weldegergis BT, Langendorf B et al (2015) Rhizobacterial colonization of roots modulates plant volatile emission and enhances the attraction of a parasitoid wasp to host-infested plants. Oecologia 178:1169–1180

    Article  Google Scholar 

  • Pangesti N, Reichelt M, Van de Mortel JE et al (2016) Jasmonic acid and ethylene signaling pathways regulate glucosinolate levels in plants during rhizobacteria-induced systemic resistance against a leaf-chewing herbivore. J Chem Ecol 42:1212–1225

    Article  CAS  Google Scholar 

  • Parray JA, Jan S, Kamili AN et al (2016) Current perspectives on plant growth-promoting rhizobacteria. Plant Growth Regul 35:877–902

    Article  CAS  Google Scholar 

  • Partida-Martinez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2:100. https://doi.org/10.3389/fpls.2011.00100

  • Pineda A, Zheng SJ, Van Loon JJA et al (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514. https://doi.org/10.1016/j.tplants.2010.05.007

    Article  CAS  PubMed  Google Scholar 

  • Pineda A, Dicke M, Pieterse CMJ et al (2013a) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Funct Ecol 27:574–586

    Article  Google Scholar 

  • Pineda A, Soler R, Weldegergis BT et al (2013b) Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling. Plant Cell Environ 36:393–404

    Article  CAS  Google Scholar 

  • Pineda A, Soler R, Pozo MJ et al (2015) Editorial: above-belowground interactions involving plants, microbes and insects. Front Plant Sci 6:318. https://doi.org/10.3389/fpls.2015.00318

    Article  PubMed  PubMed Central  Google Scholar 

  • Pineda A, Kaplan I, Bezemer TM (2017) Steering soil microbiomes to suppress aboveground insect pests. Trends Plant Sci 22:770–778

    Article  CAS  Google Scholar 

  • Ping L, Boland W (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci 9:263–266

    Article  CAS  Google Scholar 

  • Pitzschke A (2007) Agrobacterium infection and plant defence—transformation success hangs by a thread. Front Plant Sci 4:115–126

    Google Scholar 

  • Qingwen Z, Ping L, Gang W et al (1998) On the biochemical mechanism of induced resistance of cotton to cotton bollworm by cutting young seedling at plumular axis. Acta Phytophylacica Sin 25:209–212

    Google Scholar 

  • Ramamoorthy V, Viswanathan R, Raguchander T et al (2001) Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Prot 20:1–11

    Article  CAS  Google Scholar 

  • Rotroff DM, Motsinger-Reif AA (2016) Embracing integrative multiomics approaches. Int J Genomics 2016:1715985. https://doi.org/10.1155/2016/1715985

    Article  Google Scholar 

  • Ryu CM, Farag MA, Hu CH et al (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    Article  CAS  Google Scholar 

  • Saravanakumar D, Muthumeena K, Lavanya N et al (2007) Pseudomonas induced defence molecules in rice plants against leaffolder (Cnaphalocrocis medinalis) pest. Pest Manag Sci 63:714–721

    Article  CAS  Google Scholar 

  • Saveetha K, Karthiba L, Raveendran M et al (2010) Transcriptional analysis of molecular interactions between Pseudomonas fluorescens strain TDK1, Oryza sativa and Cnaphalocrocis medinalis. J Appl Entomol 134:762–773

    Article  Google Scholar 

  • Schmidt R, Köberl M, Mostafa A et al (2014) Effects of bacterial inoculants on the indigenous microbiome and secondary metabolites of chamomile plants. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00064

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

    Google Scholar 

  • Schuhegger R, Ihring A, Gantner S et al (2006) Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–918

    Article  CAS  Google Scholar 

  • Seaver SM, Henry CS, Hanson AD (2012) Frontiers in metabolic reconstruction and modeling of plant genomes. J Exp Bot 63:2247–2258

    Article  CAS  Google Scholar 

  • Senthilraja G, Anand T, Durairaj C (2010) A new microbial consortia containing entomopathogenic fungus, Beauveria bassiana and plant growth promoting rhizobacteria, Pseudomonas fluorescens for simultaneous management of leafminers and collar rot disease in groundnut. Biocontrol Sci Technol 20:449–464

    Article  Google Scholar 

  • Siemann E (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79:2057–2070

    Article  Google Scholar 

  • Sills J, Robinson GE, Hackett KJ et al (2011) Creating a buzz about insect genomes. Science 331:1386–1387

    Article  Google Scholar 

  • Sudhakar N, Thajuddin N, Murugesan K et al (2011) Plant growth-promoting rhizobacterial mediated protection of tomato in the field against cucumber mosaic virus and its vector Aphis gossypii. Biocontrol Sci Technol 21:367–386

    Article  Google Scholar 

  • Tailor A, Joshi BH (2014) Harnessing plant growth promoting rhizobacteria beyond nature: a review. J Plant Nutr 37:1534–1571

    Article  CAS  Google Scholar 

  • Thamer S, Schadler M, Bonte D et al (2011) Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defence against a specialist herbivore in a cyanogenic plant. Plant Soil 341:209–219

    Article  CAS  Google Scholar 

  • Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. Biomed Res Int. https://doi.org/10.1155/2013/863240

    Article  Google Scholar 

  • Urban M, Irvine AG, Cuzick A et al (2015) Using the pathogen-host interactions database (PHI-base) to investigate plant pathogen genomes and genes implicated in virulence. Front Plant Sci 6:605

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Van der Ent S, Van Wees S, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588

    Article  Google Scholar 

  • Van der Heijden MGA, 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

    Article  Google Scholar 

  • Van der Heijden MGA, de Bruin S, Luckerhoff L et al (2016) A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J 10:389–399

    Article  Google Scholar 

  • Van Loon LC, Bakker P, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    Article  Google Scholar 

  • Van Oosten VR, Bodenhausen N, Reymond P et al (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol Plant Microbe Interact 21:919–930

    Article  Google Scholar 

  • Vijayasamundeeswari A, Ladhalakshmi D, Sankaralingam A et al (2009) Plant growth promoting rhizobacteria of cotton affecting the developmental stages of Helicoverpa armigera. J Plant Prot Res 49:239–243

    CAS  Google Scholar 

  • War AR, Paulraj MG, Ahmad T (2012) Mechanisms of plant defence against insect herbivores. Plant Signal Behav 7:1306–1320

    Article  Google Scholar 

  • Werner GDA, Kiers ET (2014) Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol. https://doi.org/10.1111/nph.13092

    Article  Google Scholar 

  • Whitaker MRL, Katayama N, Ohgushi T (2014) Plant-rhizobia interactions alter aphid honeydew composition. Arthropod Plant Interact 8:213–220

    Article  Google Scholar 

  • Winnenburg R, Urban M, Beacham A et al (2008) PHI-base update: additions to the pathogen–host interaction database. Nucleic Acids Res 36:572–576

    Article  Google Scholar 

  • Zebelo S, Song Y, Kloepper JW et al (2016) Rhizobacteria activates (+)-δ-cadinene synthase genes and induces systemic resistance in cotton against beet armyworm (Spodoptera exigua). Plant Cell Environ 39:935–943

    Article  CAS  Google Scholar 

  • Zehnder G, Kloepper J, Yao C et al (1997) Induction of systemic resistance in cucumber against cucumber beetles (Coleoptera: Chrysomelidae) by plant growth-promoting rhizobacteria. J Econ Entomol 90:391–396

    Article  Google Scholar 

Download references

Acknowledgments

We thank Royal Holloway, University of London, for funding some of our experimental work, Rajagopalbabu Srinivasan and Bhabesh Dutta for helpful discussions, and reviewers for constructive comments that greatly improved the manuscript.

Author information

Authors and Affiliations

  1. School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, UK

    Kiran R. Gadhave & Alan C. Gange

  2. Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, USA

    Kiran R. Gadhave

Authors
  1. Kiran R. Gadhave
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alan C. Gange
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kiran R. Gadhave .

Editor information

Editors and Affiliations

  1. Center for Ecological Research, Kyoto University, Shiga, Japan

    Takayuki Ohgushi

  2. Functional Biodiversity, Institute of Biology, Freie Universität, Berlin, Germany

    Susanne Wurst

  3. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW, Australia

    Scott N. Johnson

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Gadhave, K.R., Gange, A.C. (2018). Interactions Involving Rhizobacteria and Foliar-Feeding Insects. In: Ohgushi, T., Wurst, S., Johnson, S. (eds) Aboveground–Belowground Community Ecology. Ecological Studies, vol 234. Springer, Cham. https://doi.org/10.1007/978-3-319-91614-9_6

Download citation

Publish with us

Policies and ethics

Search

Navigation