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.
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Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12
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
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
Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol Adv 16:729–770
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
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
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
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
Bulgarelli D, Rott M, Schlaeppi K et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
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
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
Dean JM, Mescher MC, De Moraes CM (2009) Plant-rhizobia mutualism influences aphid abundance on soybean. Plant Soil 323:187–196
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
Dudareva N, Negre F, Nagegowda DA et al (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440
Eisenhauer N (2012) Aboveground-belowground interactions as a source of complementarity effects in biodiversity experiments. Plant Soil 351:1–22
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
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
Gadhave KR (2015) Interactions between plant growth promoting rhizobacteria, foliar-feeding insects and higher trophic levels. PhD Thesis, Royal Holloway, University of London
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
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
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
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
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
Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342
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
Herrmann L, Lesueur D (2013) Challenges of formulation and quality of biofertilizers for successful inoculation. Appl Microbiol Biotechnol 97:8859–8873
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
Hinsinger P, Bengough AG, Vetterlein D et al (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152
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
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
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
Johri B, Sharma A, Virdi J (2003) Rhizobacterial diversity in India and its influence on soil and plant health. Biotechnology 84:49–89
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
Katayama N, Zhang ZQ, Ohgushi T (2011) Community-wide effects of below-ground rhizobia on above-ground arthropods. Ecol Entomol 36:43–51
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
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
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
Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556
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
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
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
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
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
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
Parray JA, Jan S, Kamili AN et al (2016) Current perspectives on plant growth-promoting rhizobacteria. Plant Growth Regul 35:877–902
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
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
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
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
Pineda A, Kaplan I, Bezemer TM (2017) Steering soil microbiomes to suppress aboveground insect pests. Trends Plant Sci 22:770–778
Ping L, Boland W (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci 9:263–266
Pitzschke A (2007) Agrobacterium infection and plant defence—transformation success hangs by a thread. Front Plant Sci 4:115–126
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
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
Rotroff DM, Motsinger-Reif AA (2016) Embracing integrative multiomics approaches. Int J Genomics 2016:1715985. https://doi.org/10.1155/2016/1715985
Ryu CM, Farag MA, Hu CH et al (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026
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
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
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
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
Seaver SM, Henry CS, Hanson AD (2012) Frontiers in metabolic reconstruction and modeling of plant genomes. J Exp Bot 63:2247–2258
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
Siemann E (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79:2057–2070
Sills J, Robinson GE, Hackett KJ et al (2011) Creating a buzz about insect genomes. Science 331:1386–1387
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
Tailor A, Joshi BH (2014) Harnessing plant growth promoting rhizobacteria beyond nature: a review. J Plant Nutr 37:1534–1571
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
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
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
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
Van der Ent S, Van Wees S, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588
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
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
Van Loon LC, Bakker P, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483
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
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
War AR, Paulraj MG, Ahmad T (2012) Mechanisms of plant defence against insect herbivores. Plant Signal Behav 7:1306–1320
Werner GDA, Kiers ET (2014) Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol. https://doi.org/10.1111/nph.13092
Whitaker MRL, Katayama N, Ohgushi T (2014) Plant-rhizobia interactions alter aphid honeydew composition. Arthropod Plant Interact 8:213–220
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
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
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
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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.
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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
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