Root-colonizing bacteria enhance the levels of (E)-β-caryophyllene produced by maize roots in response to rootworm feeding
- 617 Downloads
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.
KeywordsRoot-colonizing bacteria Diabrotica balteata (E)-β-caryophyllene Terpene synthase Maize
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.
Author contribution statement
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.
- Capinera JL (2011) Banded Cucumber Beetle, Diabrotica balteata LeConte (Insecta: Coleoptera: Chrysomelidae) 1. Inst Food Agric 93:1–3Google Scholar
- 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 CrossRefGoogle Scholar
- Chittenden FH (1912) Notes on the cucumber beetles. USDA. Bur Entomol Bull 82:67–75Google Scholar
- 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 CrossRefGoogle Scholar
- 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, SwitzerlandGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar