Abstract
When larvae of rootworms feed on maize roots they induce the emission of the sesquiterpene (E)-β-caryophyllene (EβC). EβC is attractive to entomopathogenic nematodes, which parasitize and rapidly kill the larvae, thereby protecting the roots from further damage. Certain root-colonizing bacteria of the genus Pseudomonas also benefit plants by promoting growth, suppressing pathogens or inducing systemic resistance (ISR), and some strains also have insecticidal activity. It remains unknown how these bacteria influence the emissions of root volatiles. In this study, we evaluated how colonization by the growth-promoting and insecticidal bacteria Pseudomonas protegens CHA0 and Pseudomonas chlororaphis PCL1391 affects the production of EβC upon feeding by larvae of the banded cucumber beetle, Diabrotica balteata Le Conte (Coleoptera: Chrysomelidae). Using chemical analysis and gene expression measurements, we found that EβC production and the expression of the EβC synthase gene (tps23) were enhanced in Pseudomonas protegens CHA0-colonized roots after 72 h of D. balteata feeding. Undamaged roots colonized by Pseudomonas spp. showed no measurable increase in EβC production, but a slight increase in tps23 expression. Pseudomonas colonization did not affect root biomass, but larvae that fed on roots colonized by P. protegens CHA0 tended to gain more weight than larvae that fed on roots colonized by P. chlororaphis PCL1391. Larvae mortality on Pseudomonas spp. colonized roots was slightly, but not significantly higher than on non-colonized control roots. The observed enhanced production of EβC upon Pseudomonas protegens CHA0 colonization may enhance the roots’ attractiveness to entomopathogenic nematodes, but this remains to be tested.
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07 March 2018
Unfortunately, family name of author “Xavier Chiriboga M” was incorrectly identified in the original publication and the same is corrected here. The original article has been corrected.
References
Ali JG, Alborn HT, Stelinski LL (2010) Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. J Chem Ecol 36:361–368. https://doi.org/10.1007/s10886-010-9773-7
Ali JG, Alborn HT, Stelinski LL (2011) Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J Ecol 99:26–35. https://doi.org/10.1111/j.1365-2745.2010.01758.x
Ali JG, Campos-Herrera R, Alborn HT, Duncan LW, Stelinski LL (2013) Sending mixed messages: a trophic cascade produced by a belowground herbivore-induced cue. J Chem Ecol 39:1140–1147. https://doi.org/10.1007/s10886-013-0332-x
Ballhorn DJ, Kautz S, Schädler M (2013) Induced plant defense via volatile production is dependent on rhizobial symbiosis. Oecologia 172:833–846. https://doi.org/10.1007/s00442-012-2539-x
Boff MIC, van Tol RWHM, Smits PH (2002) Behavioural response of Heterorhabditis megidis (strain NLH-E87.3) towards plant roots and insect larvae. BioControl 47:67–83
Brussaard L (1998) Soil fauna, guilds, functional groups and ecosystem processes. Appl Soil Ecol 9:123–135. https://doi.org/10.1016/S0929-1393(98)00066-3
Capinera JL (2011) Banded Cucumber Beetle, Diabrotica balteata LeConte (Insecta: Coleoptera: Chrysomelidae) 1. Inst Food Agric 93:1–3
Chiriboga XM, Campos-Herrera R, Jaffuel G, Röder G, Turlings TCJ (2017) Diffusion of the maize root signal (E)-β-caryophyllene in soils of different textures and the effects on the migration of the entomopathogenic nematode Heterorhabditis megidis. Rhizosphere 3:53–59. https://doi.org/10.1016/j.rhisph.2016.12.006
Chittenden FH (1912) Notes on the cucumber beetles. USDA. Bur Entomol Bull 82:67–75
D’Alessandro M, Erb M, Ton J, Brandenburg A, Karlen D, Zopfi J, Turlings TCJ (2014) Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tri-trophic interactions. Plant Cell Environ 37:813–826
Degenhardt J, Hiltpold I, Köllner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TCJ (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci 106:17606. https://doi.org/10.1073/pnas.0909073106
Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32
Erb M (2009) Modification of plant resistance and metabolism by above and belowground herbivores. PhD Thesis for the doctoral degree in natural sciences. Institute of Biology. University of Neuchatel, Switzerland
Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009) The effects of Arbuscular Mychorrizal Fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843. https://doi.org/10.1007/s10886-009-9654-0
Hiltpold I, Erb M, Robert CAM, Turlings TCJ (2011) Systemic root signalling in a belowground, volatile-mediated tritrophic interaction. Plant Cell Environ 34:1267–1275. https://doi.org/10.1111/j.1365-3040.2011.02327.x
Imperiali N, Chiriboga XM, Schlaeppi K, Fesselet M, Villacrés D, Jaffuel G, Bender SF, Dennert F, Blanco-Pérez R, van der Heijden MGA, Maurhofer M, Mascher F, Turlings TCJ, Keel C, Campos-Herrera R (2017) Combined field inoculations of Pseudomonas bacteria, arbuscular mycorrhizal fungi, and entomopathogenic nematodes and their effects on wheat performance. Front Plant Sci 8:1809. https://doi.org/10.3389/fpls.2017.01809
Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, Kogel K-H, Schafer P (2011) Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 156:726–740. https://doi.org/10.1104/pp.111.176446
Keel C (2016) A look into the toolbox of multi-talents: insect pathogenicity determinants of plant-beneficial pseudomonads. Environ Microbiol 18:3207–3209. https://doi.org/10.1111/1462-2920.13462
Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TCJ, Gershenzon J, Degenhardt J (2008) A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20:482–494. https://doi.org/10.1105/tpc.107.051672
Kupferschmied P, Maurhofer M, Keel C (2013) Promise for plant pest control: root-associated pseudomonads with insecticidal activities. Front Plant Sci 4:287. https://doi.org/10.3389/fpls.2013.00287
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556. https://doi.org/10.1146/annurev.micro.62.081307.162918
Maffei ME, Gertsch J, Appendino G (2011) Plant volatiles: production, function and pharmacology. Nat Prod Rep 28:1359–1380. https://doi.org/10.1039/c1np00021g
Pangesti N, Weldegergis BT, Langendorf B, van Loon JJ, Dicke M, Pineda A (2015a) Rhizobacterial colonization of roots modulates plant volatile emission and enhances the attraction of a parasitoid wasp to host-infested plants. Oecologia 178:1169–1180. https://doi.org/10.1007/s00442-015-3277-7
Pangesti N, Pineda A, Dicke M, van Loon JJA (2015b) Variation in plant-mediated interactions between rhizobacteria and caterpillars: potential role of soil composition. Plant Biol 17:474–483. https://doi.org/10.1111/plb.12265
Péchy-Tarr M, Bruck DJ, Maurhofer M, Fischer E, Vogner C, Henkels MD, Donahue KM, Grunder J, Loper JE, Keel C (2008) Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environ Microbiol 10:2368–2386. https://doi.org/10.1111/j.1462-2920.2008.01662.x
Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055
Pineda A, Zheng SJ, van Loon JJA, Pieterse C, Dicke M (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, Zheng SJ, van Loon JJA, Dicke M (2012) Rhizobacteria modify plant-aphid interactions: a case of induced systemic susceptibility. Plant Biol 14:83–90. https://doi.org/10.1111/j.1438-8677.2011.00549.x
Pineda A, Soler R, Weldegergis BT, Shimwela M, van Loon JJA, Dicke M (2013) Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling. Plant Cell Environ 36:393–404. https://doi.org/10.1111/j.1365-3040.2012.02581.x
Rasmann S, Turlings TCJ (2008) First insights into specificity of belowground tritrophic interactions. Oikos 117:362–369. https://doi.org/10.1111/j.2007.0030-1299.16204.x
Rasmann S, Turlings TCJ (2016) Root signals that mediate mutualistic interactions in the rhizosphere. Curr Opin Plant Biol 32:62–68. https://doi.org/10.1016/j.pbi.2016.06.017
Rasmann S, Köllner TG, Degenhardt J, Hiltplod I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737. https://doi.org/10.1038/nature03451
Robert CAM, Erb M, Duployer M, Zwahlen C, Doyen GR, Turlings TCJ (2012a) Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytol 194:1061–1069. https://doi.org/10.1111/j.1469-8137.2012.04127.x
Robert CAM, Veyrat N, Glauser G, Marti G, Doyen GR, Villard N, Gaillard M, Kollner TG, Giron D, Body M, Babst BA, Ferrieri RA, Turlings TCJ, Erb M (2012b) A specialist root herbivore exploits defensive metabolites to locate nutritious tissues. Ecol Lett 15:55–64. https://doi.org/10.1111/j.1461-0248.2011.01708.x
Ruffner B, Péchy-Tarr M, Ryffel F, Hoegger P, Obrist C, Rindlisbacher A, Keel C, Maurhofer M (2013) Oral insecticidal activity of plant-associated pseudomonads. Environ Microbiol 15:751–763. https://doi.org/10.1111/j.1462-2920.2012.02884.x
Saba F (1970) Host plant spectrum and temperature limitations of Diabrotica balteata. Can Entomol 102:684–691. https://doi.org/10.4039/Ent102684-6
Santos F, Peñaflor MFGV, Paré PW, Sanches P, Kamiya AC, Tonelli M, Nardi C, Bento JM (2014) A novel interaction between plant-beneficial rhizobacteria and roots: colonization induces corn resistance against the root herbivore Diabrotica speciosa. PLoS One. https://doi.org/10.1371/journal.pone.0113280
Schmelz EA, Alborn HT, Banchio E, Tumlinson JH (2003) Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory. Planta 216:665–673. https://doi.org/10.1007/s00425-002-0898-y
Strauss S, Agrawal A (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185. https://doi.org/10.1016/S0169-5347(98)01576-6
Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270. https://doi.org/10.1016/j.tplants.2012.02.010
Tonelli M, Peñaflor MFGV, Leite LG, Silva W, Martins F, Bento JM (2016) Attraction of entomopathogenic nematodes to sugarcane root volatiles under herbivory by a sap-sucking insect. Chemoecology 26:59–66. https://doi.org/10.1007/s00049-016-0207-z
Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(Suppl):S153–S164. https://doi.org/10.1105/tpc.000679
van Oosten VR, Bodenhausen N, Reymond P, van Pelt J, van Loon LC, Dicke M, Pieterse C (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol Plant-Microbe Interact 21:919–930. https://doi.org/10.1094/MPMI-21-7-0919
Walker V, Couillerot O, Von Felten A, Bellvert F, Jansa J, Maurhofer M, Bally R, Moënne-Loccoz Y, Comte G (2012) Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant Soil 356:151–163. https://doi.org/10.1007/s11104-011-0960-2
Zarate SI, Kempema LA, Walling LL (2006) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875. https://doi.org/10.1104/pp.106.090035
Acknowledgements
We thank Jean-Marc Freyermuth and Radu Sloboneanu for statistical advice, Geoffrey Jaffuel and Alan Kergunteuil for fruitful discussions, and Angela Köhler and Pamela Bruno for technical assistance. This study was supported by the NRP68 program “Sustainable use of soil as a resource” (Projects No 143065 and 406840_143141) from the Swiss National Science Foundation awarded to TCJT, CK, and MM. XCM was funded by an Excellence Scholarship of the Swiss Confederation, HG was supported with a Post-Doc Grant from the Chinese Academy of Sciences and R.C.-H. was supported with an Investigator Program Award (IF/00552/2014) from the government of Portugal.
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XCM, HG, TCJT and RC-H conceived the experiments, XCM and RC-H analyzed the data and wrote the first drafts of the paper, NI and GR provide technical assistance for microbiology techniques and GC–MS analysis, respectively. CK, MM and TCJT revised and edited the text.
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Communicated by Caroline Müller.
The original version of this article was revised: Family name of author “Xavier Chiriboga M” was incorrectly identified in the original publication and the same is corrected here.
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Chiriboga M., X., Guo, H., Campos-Herrera, R. et al. Root-colonizing bacteria enhance the levels of (E)-β-caryophyllene produced by maize roots in response to rootworm feeding. Oecologia 187, 459–468 (2018). https://doi.org/10.1007/s00442-017-4055-5
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DOI: https://doi.org/10.1007/s00442-017-4055-5