Colorado potato beetle microsymbiont Enterobacter BC-8 inhibits defense mechanisms of potato plants using crosstalk between jasmonate- and salicylate-mediated signaling pathways

  • Antonina V. SorokanEmail author
  • Guzel F. Burkhanova
  • Galina V. Benkovskaya
  • Igor V. Maksimov
Original Paper


One of the main insect potato pests is the Colorado potato beetle (Leptinotarsa decemlineata Say). It contains some microbial associates which can affect diverse interactions between host plant and the herbivorous insect. Previously, the most common L. decemlineata microsymbiont isolated from anterior and posterior parts of beetle gut was defined as Enterobacter BC-8. The role of Enterobacter BC-8 in manipulating plant defenses was investigated using antibiotics-treated beetles and model system simulating beetles attacks (wounding plants treated with Enterobacter BC-8 suspension). We demonstrated that the symbiotic bacteria suppressed plant defenses such as hydrogen peroxide and phenolic compounds accumulation and activity of peroxidases and trypsin inhibitors. It is worth noting that the influence of the insect symbionts on potato plants stimulated salicylate-sensitive genes and the marker of salicylate signaling pathway. Transcription activities of jasmonate-sensitive genes which encode some defense proteins against herbivores, were suppressed. So, Enterobacter BC-8 plays the role in salicylate/jasmonate crosstalks manipulating to suppress plant defense mechanisms.


Solanum tuberosum Leptinotarsa decemlineata Enterobacter Salicylic acid Jasmonic acid 



This research was granted by the Russian Federation State Program No. 116020350027-7 (2016–2018), Russian Foundation for basic research (RFBR) No. 17-44-020347 and RFBR No. 18-34-00021. Equipment of “Biomika” (Department of biochemical research methods and nanobiotechnology center “Agidel”) and USC “KODINK’” was used.


  1. Arimura G-I, Ozawa R, Maffei ME (2011) Recent advances in plant early signaling in response to herbivory. Int J Mol Sci 12(6):3723–3739. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Barr KL, Hearne LB, Briesacher S et al (2010) Microbial symbionts in insects influence down regulation of defense genes in maize. PLoS ONE 5:e11339. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory—primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511–1530. CrossRefPubMedGoogle Scholar
  4. Bittner N, Trauer-Kizilelma U, Hilker M (2017) Early plant defence against insect attack: Involvement of reactive oxygen species in plant responses to insect egg deposition. Planta. 245:993–996. CrossRefPubMedGoogle Scholar
  5. Bruessow F, Gouhier-Darimont G, Buchala A, Metraux J-P, Reymond F (2010) Insect eggs suppress plant defence against chewing herbivores. Plant J 62:876–885. CrossRefPubMedGoogle Scholar
  6. Caarls L, Van der Does D, Hickman R, Jansen W et al (2017) Assessing the role of ETHYLENE RESPONSE FACTOR transcriptional repressors in salicylic acid-mediated suppression of jasmonic acid-responsive genes. Plant Cell Physiol 58:266–278. CrossRefPubMedGoogle Scholar
  7. Casteel CL, Hansen AK, Walling LL, Paine TD (2012) Manipulation of plant defense responses by the tomato psyllid (Bactericerca cockerelli) and its associated endosymbiont Candidatus Liberibacter psyllaurous. PLoS ONE. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chung SH, Rosa C, Hoover K et al (2013a) Colorado potato beetle manipulates plant defenses in local and systemic leaves. Plant Signal Behav 8:e27592CrossRefGoogle Scholar
  9. Chung SH, Rosa C, Scully ED et al (2013b) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci USA 110:15728–15733. CrossRefPubMedGoogle Scholar
  10. de Vos M, Kim JH, Jande G (2007) Biochemistry and molecular biology of Arabidopsis–aphid interactions. Bioassays 29:871–883. CrossRefGoogle Scholar
  11. Ding CK, Wang CY, Gross KC (2002) Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 214:895–901. CrossRefPubMedGoogle Scholar
  12. Hilder VA, Gatehouse AMR, Sheerman SF, Barker RF, Boulter D (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 330:160–163. CrossRefGoogle Scholar
  13. Janson EM, Stireman JO, Singer MS, Abbot P (2008) Phytophagous insect-microbe mutualism and adaptive evolutionary diversification. Evolution 62:997–1012. CrossRefPubMedGoogle Scholar
  14. Kakade ML, Simons N, Liener IE (1969) An evaluation of natural versus synthetic substrates for measuring the antitryptic activity of soybean samples. Cereal Chem 46:518Google Scholar
  15. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328. CrossRefPubMedGoogle Scholar
  16. Maffei ME, Mithöfer A, Arimura G-I et al (2006) Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol 140:1022–1035. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Mellersh DG, Foulds IV, Higgins VJ (2002) H2O2 plays different roles in determining penetration failure in three diverse plant–fungal interactions. Plant J 29:257–268. CrossRefPubMedGoogle Scholar
  18. Mithofer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on Lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137(3):1160–1168. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Mittler R, Vanderauwera S, Suzuki N et al (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309. CrossRefGoogle Scholar
  20. Musser RO et al (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416(6881):599–600. CrossRefPubMedGoogle Scholar
  21. Orozco-Cárdenas ML, Narvaez-Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Pieterse CMJ, Zamioudis C, Berendsen RL et al (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. CrossRefPubMedGoogle Scholar
  23. Schweiger R, Heise A-M, Persicke M, Müller C (2014) Interactions between the jasmonic and salicylic acid pathway modulate the plant metabolome and affect herbivores of different feeding types. Plant, Cell Environ 37:1574–1585. CrossRefGoogle Scholar
  24. Sorokan AV, Ben’kovskaya GV, Maksimov IV (2016) The influence of potato endophytes on Leptinotarsa decemlineata endosymbionts promotes mortality of the pest. J Invertebr Pathol 136:65–67. CrossRefPubMedGoogle Scholar
  25. Sorokan AV, Burhanova GF, Maksimov IV (2018) Anionic peroxidase-mediated oxidative burst is required for jasmonic acid-dependent Solanum tuberosum L. defense against Phytophthora infestans (Mont) de Bary. Plant Pathol 67:349–357. CrossRefGoogle Scholar
  26. Su Q, Oliver KM, Xie W et al (2015) The whitefly associated facultative symbiont Hamiltonella defensa suppresses induced plant defenses in tomato. Funct Ecol 29:1007–1018. CrossRefGoogle Scholar
  27. Tanaka K, Choi J, Cao Y, Stacey G (2014) Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Front Plant Sci 5:19–29. CrossRefGoogle Scholar
  28. Thomma BPJ, Eggermont K, Penninckx IAMA et al (1999) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci 95(25):15107–15111. CrossRefGoogle Scholar
  29. Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Institute of Biochemistry and GeneticsUfa Federal Research CenterUfaRussia

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