Skip to main content
Log in

Herbivore Oral Secreted Bacteria Trigger Distinct Defense Responses in Preferred and Non-Preferred Host Plants

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Insect symbiotic bacteria affect host physiology and mediate plant-insect interactions, yet there are few clear examples of symbiotic bacteria regulating defense responses in different host plants. We hypothesized that plants would induce distinct defense responses to herbivore- associated bacteria. We evaluated whether preferred hosts (horsenettle) or non-preferred hosts (tomato) respond similarly to oral secretions (OS) from the false potato beetle (FPB, Leptinotarsa juncta), and whether the induced defense triggered by OS was due to the presence of symbiotic bacteria in OS. Both horsenettle and tomato damaged by antibiotic (AB) treated larvae showed higher polyphenol oxidase (PPO) activity than those damaged by non-AB treated larvae. In addition, application of OS from AB treated larvae induced higher PPO activity compared with OS from non-AB treated larvae or water treatment. False potato beetles harbor bacteria that may provide abundant cues that can be recognized by plants and thus mediate corresponding defense responses. Among all tested bacterial isolates, the genera Pantoea, Acinetobacter, Enterobacter, and Serratia were found to suppress PPO activity in tomato, while only Pantoea sp. among these four isolates was observed to suppress PPO activity in horsenettle. The distinct PPO suppression caused by symbiotic bacteria in different plants was similar to the pattern of induced defense-related gene expression. Pantoea inoculated FPB suppressed JA-responsive genes and triggered a SA-responsive gene in both tomato and horsenettle. However, Enterobacter inoculated FPB eliminated JA-regulated gene expression and elevated SA-regulated gene expression in tomato, but did not show evident effects on the expression levels of horsenettle defense-related genes. These results indicate that suppression of plant defenses by the bacteria found in the oral secretions of herbivores may be a more widespread phenomenon than previously indicated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW (2015) Cues from chewing insects - the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol 26:80–86

    Article  CAS  PubMed  Google Scholar 

  • Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH, Currie CR, Suen G, Raffa KF (2013) Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol 79:3468–3475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barr KL, Hearne LB, Briesacher S, Clark TL, Davis GE (2010) Microbial symbionts in insects influence down-regulation of defense genes in maize. PLoS One 5:e11339

    Article  PubMed  PubMed Central  Google Scholar 

  • Biere A, Bennett AE (2013) Three-way interactions between plants, microbes and insects. Funct Ecol 27:567–573

    Article  Google Scholar 

  • Bosch M, Berger S, Schaller A, Stintzi A (2014) Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage is important for defense against Spodoptera exigua but not against Manduca sexta. BMC Plant Biol 14:257

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Broderick NA, Raffa KF, Goodman RM, Handelsman J (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 70:293–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunner F, Rosahl S, Lee J, Rudd JJ, Geiler C, Kauppinen S, Rasmussen G, Scheel D, Nürnberger T (2002) Per-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO J 21:6681–6688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casteel CL, Hansen AK (2014) Evaluating insect-microbiomes at the plant-insect interface. J Chem Ecol 40:836–847

    Article  CAS  PubMed  Google Scholar 

  • Chuang W-P, Ray S, Acevedo FE, Peiffer M, Felton GW, Luthe DS (2014) Herbivore cues from the fall armyworm (Spodoptera frugiperda) larvae trigger direct defenses in maize. Mol Plant-Microbe Interact 27:461–470

    Article  CAS  PubMed  Google Scholar 

  • Chung SH, Felton GW (2011) Specificity of induced resistance in tomato against specialist lepidopteran and coleopteran species. J Chem Ecol 37:378–386

    Article  CAS  PubMed  Google Scholar 

  • Chung SH, Rosa C, Hoover K, Luthe DS, Felton GW (2013a) Colorado potato beetle manipulates plant defenses in local and systemic leaves. Plant Signal Behav 8:e27592

    Article  PubMed  PubMed Central  Google Scholar 

  • Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe DS, Felton GW (2013b) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci U S A 110:15728–15733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark EL, Karley AJ, Hubbard SF (2010) Insect endosymbionts: manipulators of insect herbivore trophic interactions? Protoplasma 244:25–51

    Article  PubMed  Google Scholar 

  • Constabel C (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci U S A 92:407–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper WR, Goggin FL (2005) Effects of jasmonate-induced defenses in tomato on the potato aphid, Macrosiphum euphorbiae. Entomol Exp Appl 115:107–115

    Article  CAS  Google Scholar 

  • Douglas AE (2013) Microbial brokers of insect-plant interactions revisited. J Chem Ecol 39:952–961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felton GW (2005) Indigestion is a plant’s best defense. Proc Natl Acad Sci U S A 102:18771–18772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felton GW, Donato K, Del Vecchio RJ, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J Chem Ecol 15:2667–2694

    Article  CAS  PubMed  Google Scholar 

  • Fowler JH, Narváez-Vásquez J, Aromdee DN, Pautot V, Holzer FM, Walling LL (2009) Leucine aminopeptidase regulates defense and wound signaling in tomato downstream of jasmonic acid. Plant Cell 21:1239–1251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giron D, Frago E, Glevarec G, Pieterse CM, Dicke M (2013) Cytokinins as key regulators in plant-microbe-insect interactions: connecting plant growth and defence. Funct Ecol 27:599–609

    Article  Google Scholar 

  • Gitaitis R, Walcott R, Culpepper S, Sanders H, Zolobowska L, Langston D (2002) Recovery of Pantoea ananatis, causal agent of center rot of onion, from weeds and crops in Georgia, USA. Crop Prot 21:983–989

    Article  Google Scholar 

  • Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777

    Article  CAS  PubMed  Google Scholar 

  • Gündüz EA, Douglas A (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc Roy Soc Lond B 276:987–991

    Article  Google Scholar 

  • Gurtler V, Stanisich VA (1996) New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology 142:3–16

    Article  PubMed  Google Scholar 

  • Hansen AK, Moran NA (2014) The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol 23:1473–1496

    Article  PubMed  Google Scholar 

  • Jacques RL (1988) The potato beetles: The genus Leptinotarsa in North America (Coleoptera, Chrysomelidae). In: Flora and fauna handbook No. 3. E.J. Brill, New York

    Google Scholar 

  • Jr RLJ, Fasulo TR (2015) Colorado potato beetle, Leptinotarsa decemlineata (say), and false potato beetle, Leptinotarsa juncta (Germar) (Insecta: Coleoptera: Chrysomelidae). EDIS website. http://edis.ifas.ufl.edu/in303. Accessed November 2015

  • Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc Biol Sci 277:2311–2319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kariyat RR, Mena-Alí J, Forry B, Mescher MC, Moraes CM, Stephenson AG (2012) Inbreeding, herbivory, and the transcriptome of Solanum carolinense. Entomol Exp Appl 144:134–144

    Article  Google Scholar 

  • Kim J, Tooker JF, Luthe DS, De Moraes CM, Felton GW (2012) Insect eggs can enhance wound response in plants: a study system of tomato Solanum lycopersicum L. And Helicoverpa zea Boddie. PLoS One 7:e37420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohl KD, Dearing MD (2012) Experience matters: prior exposure to plant toxins enhances diversity of gut microbes in herbivores. Ecol Lett 15:1008–1015

    Article  PubMed  Google Scholar 

  • Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci U S A 99:6416–6421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ÄÄCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Louis J, Peiffer M, Ray S, Luthe DS, Felton GW (2013) Rapid report host-specific salivary elicitor ( s ) of European corn borer induce defenses in tomato and maize. New Phytol 199:66–73

    Article  CAS  PubMed  Google Scholar 

  • Miller A (1961) The mouth parts and digestive tract of adult dung beetles (Coleoptera: Scarabaeidae), with reference to the ingestion of helminth eggs. J Parasitol 47:735–744

    Article  CAS  PubMed  Google Scholar 

  • Musser RO, Farmer E, Peiffer M, Williams SA, Felton GW (2006) Ablation of caterpillar labial salivary glands: technique for determining the role of saliva in insect–plant interactions. J Chem Ecol 32:981–992

    Article  CAS  PubMed  Google Scholar 

  • Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55:247–266

    Article  CAS  PubMed  Google Scholar 

  • Pautot V, Holzer FM, Reisch B, Walling LL (1993) Leucine aminopeptidase: an inducible component of the defense response in Lycopersicon esculentum (tomato). Proc Natl Acad Sci U S A 90:9906–9910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peiffer M, Felton GW (2005) The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in larval Helicoverpa zea. Arch Insect Biochem Physiol 58:106–113

    Article  CAS  PubMed  Google Scholar 

  • Peiffer M, Felton GW (2009) Do caterpillars secrete “oral secretions”? J Chem Ecol 35:326–335

    Article  CAS  PubMed  Google Scholar 

  • Peiffer M, Tooker JF, Luthe DS, Felton GW (2009) Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184:644–656

    Article  CAS  PubMed  Google Scholar 

  • Petek M, Rotter A, Kogovšek P, Baebler Š, Mithöfer A, Gruden K (2014) Potato virus Y infection hinders potato defence response and renders plants more vulnerable to Colorado potato beetle attack. Mol Ecol 23:5378–5391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pieterse MJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521

    Article  CAS  PubMed  Google Scholar 

  • Portman SL, Kariyat RR, Johnston MA, Stephenson AG, Marden JH (2015) Inbreeding compromises host plant defense gene expression and improves herbivore survival. Plant Signal Behav 10:e998548

    Article  PubMed  PubMed Central  Google Scholar 

  • Priya NG, Ojha A, Kajla MK, Raj A, Rajagopal R (2012) Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS One 7:e30768

    Article  PubMed  Google Scholar 

  • Robert CA, Frank DL, Leach KA, Turlings TC, Hibbard BE, Erb M (2013) Direct and indirect plant defenses are not suppressed by endosymbionts of a specialist root herbivore. J Chem Ecol 39:507–515

    Article  CAS  PubMed  Google Scholar 

  • Rotenberg D, Thompson TS, German TL, Willis DK (2006) Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. J Virol Methods 138:49–59

    Article  CAS  PubMed  Google Scholar 

  • Shinkai T, Kobayashi Y (2007) Localization of ruminal cellulolytic bacteria on plant fibrous materials as determined by fluorescence in situ hybridization and real-time PCR. Appl Environ Microbiol 73:1646–1652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stout MJ, Thaler JS, Thomma BP (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51:663–689

    Article  CAS  PubMed  Google Scholar 

  • Su Q, Oliver KM, Xie W, Wu Q, Wang S, Zhang Y (2015) The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato. Funct Ecol 29:1007–1018

    Article  Google Scholar 

  • Sugio A, Dubreuil G, Giron D, Simon JC (2015) Plant-insect interactions under bacterial influence: ecological implications and underlying mechanisms. J Exp Bot 66:467–478

    Article  CAS  PubMed  Google Scholar 

  • Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270

    Article  CAS  PubMed  Google Scholar 

  • Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wise MJ (2007) Evolutionary ecology of resistance to herbivory: an investigation of potential genetic constraints in the multiple-herbivore community of Solanum carolinense. New Phytol 175:773–784

    Article  PubMed  Google Scholar 

  • Xiang H, Wei GF, Jia S, Huang J, Miao XX, Zhou Z, Zhao LP, Huang YP (2006) Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Can J Microbiol 52:1085–1092

    Article  CAS  PubMed  Google Scholar 

  • Zarate SI, Kempema LA, Walling LL (2006) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    Article  PubMed  Google Scholar 

  • Zebelo S, Piorkowski J, Disi J, Fadamiro H (2014) Secretions from the ventral eversible gland of Spodoptera exigua caterpillars activate defense-related genes and induce emission of volatile organic compounds in tomato, Solanum lycopersicum. BMC Plant Biol 14:140

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The financial support provided by the National Science Foundation Grant IOS-1256326 (to G.W.F., C.R., and K.H.) and the China Scholarship Council (to J.W.) is acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jie Wang.

Electronic Supplementary Material

ESM 1

Supplementary Method S1 (DOCX 1108 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, J., Chung, S.H., Peiffer, M. et al. Herbivore Oral Secreted Bacteria Trigger Distinct Defense Responses in Preferred and Non-Preferred Host Plants. J Chem Ecol 42, 463–474 (2016). https://doi.org/10.1007/s10886-016-0712-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-016-0712-0

Keywords

Navigation