Abstract
Soil microbes present a novel and cost-effective method of increasing plant resistance to insect pests and thus create a sustainable opportunity to reduce current pesticide application. However, the use of microbes in integrated pest management programs is still in its infancy. This can be attributed primarily to the variations in microbial inoculum performance under laboratory and field conditions. Soil inoculants containing single, indigenous microbial species have shown promising results in increasing chemical defenses of plants against foliar feeding insects. Conversely, commercial inoculants containing multiple species tend to show no effects on herbivore infestation in the field. We present here a simple model that endeavours to explain how single and multiple species in microbial inoculants differentially govern insect population dynamics via changes in plant chemical profiles. We discuss further how this knowledge can be applied to manipulate soil microbial species and develop ‘tailored’ microbial inoculants that could be used in plant protection against antagonists.
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Allizadeh H et al (2013) Induced systemic resistance in cucumber and Arabidopsis thaliana by the combination of Trichoderma harzianum Tr6 and Pseudomonas sp Ps14. Biol Control 65:14–23
Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
Babikova Z et al (2013) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol Lett 16:835–843
Bakker PA, Berendsen RL, Doornbos RF, Wintermans PC, Pieterse CM (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4. doi:10.3389/fpls.2013.00165
Be’Er A, Zhang H, Florin EL, Payne SM, Ben-Jacob E, Swinney HL (2009) Deadly competition between sibling bacterial colonies. Proc Natl Acad Sci U S A 106:428–433
Boutard-Hunt C, Smart CD, Thaler J, Nault BA (2009) Impact of plant growth-promoting rhizobacteria and natural enemies on Myzus persicae (Hemiptera: Aphididae) infestations in pepper. J Econ Entomol 102:2183–2191
Brock AK, Berger B, Mewis I, Ruppel S (2013) Impact of the PGPB Enterobacter radicincitans DSM 16656 on growth, glucosinolate profile, and immune responses of Arabidopsis thaliana. Microb Ecol 65:661–670
Brockwell J, Bottomley PJ (1995) Recent advances in inoculant technology and prospects for the future. Soil Biol Biochem 27:683–697
Ceballos I, Ruiz M, Fernández C, Peña R, Rodríguez A, Sanders IR (2013) The in vitro mass-produced model mycorrhizal fungus, Rhizophagus irregularis, significantly increases yields of the globally important food security crop cassava. PLoS ONE 8:e70633
Ciccazzo S, Esposito A, Rolli E, Zerbe S, Daffonchio D, Brusetti L (2014) Different pioneer plant species select specific rhizosphere bacterial communities in a high mountain environment. Springerplus 3:391
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
Corkidi L, Allen EB, Merhaut D, Allen MF, Downer J, Bohn J, Evans M (2004) Assessing the infectivity of commercial mycorrhizal inoculants in plant nursery conditions. J Environ Hortic 22:149–154
Daniell T, Husband R, Fitter A, Young J (2001) Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol Ecol 36:203–209
Engelmoer DJ, Behm JE, Toby Kiers E (2014) Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance. Mol Ecol 23:1584–1593
Faure D, Vereecke D, Leveau JH (2009) Molecular communication in the rhizosphere. Plant Soil 321:279–303
Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009) The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843
Gadhave KR (2015) Interactions between plant growth promoting rhizobacteria, foliar-feeding insects and higher trophic levels. PhD thesis, University of London
Gange AC (2001) Species‐specific responses of a root‐and shoot‐feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol 150:611–618
Gange A, West H (1994) Interactions between arbuscular mycorrhizal fungi and foliar‐feeding insects in Plantago lanceolata L. New Phytol 128:79–87
Gange AC, Brown VK, Aplin DM (2005) Ecological specificity of arbuscular mycorrhizae: evidence from foliar-and seed-feeding insects. Ecology 86:603–611
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, UK, pp 170–188
Gehring C, Bennett A (2009) Mycorrhizal fungal–plant–insect interactions: the importance of a community approach. Environ Entomol 38:93–102
Germida JJ, Siciliano SD, Renato de Freitas J, Seib AM (1998) Diversity of root‐associated bacteria associated with field‐grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol Ecol 26:43–50
Gollotte A, Gianinazzi-Pearson V, Giovannetti M, Sbrana C, Avio L, Gianinazzi S (1993) Cellular localization and cytochemical probing of resistance reactions to arbuscular mycorrhizal fungi in a ‘locus a’myc−mutant of Pisum sativum L. Planta 191:112–122
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
Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152
Hoffmann D, Vierheilig H, Schausberger P (2011a) Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey‐related cues. Physiol Entomol 36:90–95
Hoffmann D, Vierheilig H, Schausberger P (2011b) Mycorrhiza-induced trophic cascade enhances fitness and population growth of an acarine predator. Oecologia 166:141–149
Hortal S, Bastida F, Armas C, Lozano Y, Moreno J, García C, Pugnaire F (2013) Soil microbial community under a nurse-plant species changes in composition, biomass and activity as the nurse grows. Soil Biol Biochem 64:139–146
Hourston JE (2015) Do mycorrhizal fungi facilitate root defence signalling in belowground predator–prey interactions? PhD thesis, University of London
Jaber LR, Vidal S (2010) Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation. Ecol Entomol 35:25–36
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
Kerry B (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 38:423–441
Klemptner RL, Sherwood JS, Tugizimana F, Dubery IA, Piater LA (2014) Ergosterol, an orphan fungal microbe‐associated molecular pattern (MAMP). Mol Plant Pathol 15:747–761
Kloepper JW, Ryu C-M (2006) Bacterial endophytes as elicitors of induced systemic resistance. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer, Verlag, Berlin, Heidelberg, pp 33–52
Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844
Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097
Kröber M 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 5:252
Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251
Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748
Martinuz A, Schouten A, Menjivar R, Sikora R (2012) Effectiveness of systemic resistance toward Aphis gossypii (Hom., Aphididae) as induced by combined applications of the endophytes Fusarium oxysporum Fo162 and Rhizobium etli G12. Biol Control 62:206–212
McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310
Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–1587
Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22:973–990
Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450
Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLoS ONE 7:e35498
Pangesti N, Weldegergis BT, Langendorf B, van Loon JJ, Dicke M, Pineda A (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
Patiño-Ruiz JD, Schausberger P (2014) Spider mites adaptively learn recognizing mycorrhiza-induced changes in host plant volatiles. Exp Appl Acarol 64:455–463
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
Pineda A, Zheng SJ, Van Loon J, Dicke M (2012) Rhizobacteria modify plant–aphid interactions: a case of induced systemic susceptibility. Plant Biol 14:83–90
Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556
Schausberger P, Peneder S, Juerschik S, Hoffmann D (2012) Mycorrhiza changes plant volatiles to attract spider mite enemies. Funct Ecol 26:441–449
Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, Pringle A (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol Lett 9:501–515
Shaul O, Galili S, Volpin H, Ginzberg I, Elad Y, Chet I, Kapulnik Y (1999) Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves. Mol Plant Microbe Interact 12:1000–1007
Toju H, Guimarães PR, Olesen JM, Thompson JN (2014) Assembly of complex plant–fungus networks. Nat Commun 5:5273
Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. BioMed Res Int. doi:10.1155/2013/863240
Trabelsi D, Ammar HB, Mengoni A, Mhamdi R (2012) Appraisal of the crop-rotation effect of rhizobial inoculation on potato cropping systems in relation to soil bacterial communities. Soil Biol Biochem 54:1–6
Valenzuela-Soto JH, Estrada-Hernandez MG, Ibarra-Laclette E, Delano-Frier JP (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 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
Van Wees S, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448
Vannette RL, Hunter MD (2013) Mycorrhizal abundance affects the expression of plant resistance traits and herbivore performance. J Ecol 101:1019–1029
Walder F, Niemann H, Natarajan M, Lehmann MF, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797
Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348
Werner GDA, Kiers ET (2014) Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol 205:1515–1524
Zehnder G, Kloepper J, Yao C, Wei G (1997) Induction of systemic resistance in cucumber against cucumber beetles (Coleoptera: Chrysomelidae) by plant growth-promoting rhizobacteria. J Econ Entomol 90:391–396
Zhang L et al (2014) Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiol 164:352–364
Acknowledgments
We are grateful to Andreas Ebertz for help in producing artwork, to three anonymous authors for constructive feedback, and to Royal Holloway, University of London and the Natural Environment Research Council for providing the financial support to carry out field studies.
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Gadhave, K.R., Hourston, J.E. & Gange, A.C. Developing Soil Microbial Inoculants for Pest Management: Can One Have Too Much of a Good Thing?. J Chem Ecol 42, 348–356 (2016). https://doi.org/10.1007/s10886-016-0689-8
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DOI: https://doi.org/10.1007/s10886-016-0689-8