Oecologia

pp 1–10 | Cite as

Root-colonizing bacteria enhance the levels of (E)-β-caryophyllene produced by maize roots in response to rootworm feeding

  • Xavier M. Chiriboga
  • Huijuan Guo
  • Raquel Campos-Herrera
  • Gregory Röder
  • Nicola Imperiali
  • Christoph Keel
  • Monika Maurhofer
  • Ted C. J. Turlings
Special Topic: From Plants to Herbivores

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.

Keywords

Root-colonizing bacteria Diabrotica balteata (E)-β-caryophyllene Terpene synthase Maize 

Notes

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.

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.

Supplementary material

442_2017_4055_MOESM1_ESM.pdf (245 kb)
Supplementary material 1 (PDF 245 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Xavier M. Chiriboga
    • 1
  • Huijuan Guo
    • 1
    • 2
  • Raquel Campos-Herrera
    • 1
    • 3
  • Gregory Röder
    • 1
  • Nicola Imperiali
    • 4
  • Christoph Keel
    • 4
  • Monika Maurhofer
    • 5
  • Ted C. J. Turlings
    • 1
  1. 1.Fundamental and Applied Research in Chemical Ecology (FARCE Lab), Institute of BiologyUniversity of NeuchâtelNeuchâtelSwitzerland
  2. 2.State Key Laboratory of Integrated Management of Insect Pests and Rodents, Institute of ZoologyChinese Academy of SciencesBeijinChina
  3. 3.Centro para os Recursos Biológicos e Alimentos Mediterrânicos (MeditBio), FCTUniversidade do AlgarveFaroPortugal
  4. 4.Department of Fundamental MicrobiologyUniversity of LausanneLausanneSwitzerland
  5. 5.Plant Pathology, Institute of Integrative BiologySwiss Federal Institute of TechnologyZurichSwitzerland

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