Abstract
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.
Similar content being viewed by others
References
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. https://doi.org/10.3390/ijms12063723
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. https://doi.org/10.1371/journal.pone.0011339
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. https://doi.org/10.1007/BF02035149
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. https://doi.org/10.1007/s00425-017-2654-3
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. https://doi.org/10.1111/j.1365-313X.2010.04200.x
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. https://doi.org/10.1093/pcp/pcw187
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. https://doi.org/10.1371/journal.pone.0035191
Chung SH, Rosa C, Hoover K et al (2013a) Colorado potato beetle manipulates plant defenses in local and systemic leaves. Plant Signal Behav 8:e27592
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. https://doi.org/10.1073/pnas.1308867110
de Vos M, Kim JH, Jande G (2007) Biochemistry and molecular biology of Arabidopsis–aphid interactions. Bioassays 29:871–883. https://doi.org/10.1002/bies.20624
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. https://doi.org/10.1007/s00425-001-0698-9
Hilder VA, Gatehouse AMR, Sheerman SF, Barker RF, Boulter D (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 330:160–163. https://doi.org/10.1038/330160a0
Janson EM, Stireman JO, Singer MS, Abbot P (2008) Phytophagous insect-microbe mutualism and adaptive evolutionary diversification. Evolution 62:997–1012. https://doi.org/10.1111/j.1558-5646.2008.00348.x
Kakade ML, Simons N, Liener IE (1969) An evaluation of natural versus synthetic substrates for measuring the antitryptic activity of soybean samples. Cereal Chem 46:518
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328. https://doi.org/10.1146/annurev.arplant.53.100301.135207
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. https://doi.org/10.1104/pp.105.071993
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. https://doi.org/10.1046/j.0960-7412.2001.01215.x
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. https://doi.org/10.1104/pp.104.054460
Mittler R, Vanderauwera S, Suzuki N et al (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309. https://doi.org/10.1016/j.tplants.2011.03.007
Musser RO et al (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416(6881):599–600. https://doi.org/10.1038/416599a
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. https://doi.org/10.1105/tpc.13.1.179
Pieterse CMJ, Zamioudis C, Berendsen RL et al (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. https://doi.org/10.1146/annurev-phyto-082712-102340
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. https://doi.org/10.1111/pce.12257
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. https://doi.org/10.1016/j.jip.2016.03.006
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. https://doi.org/10.1111/ppa.12743
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. https://doi.org/10.1111/1365-2435.12405
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. https://doi.org/10.3389/fpls.2014.00446
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. https://doi.org/10.1073/pnas.95.25.15107
Zarate SI, Kempema LA, Walling LL (2007) 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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sorokan, A.V., Burkhanova, G.F., Benkovskaya, G.V. et al. Colorado potato beetle microsymbiont Enterobacter BC-8 inhibits defense mechanisms of potato plants using crosstalk between jasmonate- and salicylate-mediated signaling pathways. Arthropod-Plant Interactions 14, 161–168 (2020). https://doi.org/10.1007/s11829-019-09732-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-019-09732-w