Skip to main content
Log in

Impact of Soil Rhizobacteria Inoculation and Leaf-Chewing Insect Herbivory on Mentha piperita Leaf Secondary Metabolites

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

Abstract

Secondary metabolites commonly play important physiological roles in plants and can be modified quantitatively and qualitatively by exposure to biotic and abiotic interactions. Plant growth promoting rhizobacteria (PGPR) and herbivory induce systemic resistance. In the present study, we analyzed the induction of secondary metabolites in peppermint plants in response to chewing insect herbivory on PGPR-inoculated Mentha piperita plants. The secondary metabolites of M. piperita plants were increased when plants were inoculated with PGPR and also exposed to caterpillar herbivory. It was found that the total essential oil yield in inoculated plants with insect damage was ~2.6-fold higher than in controls. The yield was similar to that of plants either damaged by insects or inoculated, indicating that there was no synergism. The same trend was observed for phenolic compounds. In contrast, VOC emissions were significantly higher in plants infested by insects, independent of whether they were inoculated. Insect damaged plants had 5.5 times higher monoterpene emissions than control plants, and ~ 2-fold higher emissions than on PGPR-inoculated plants without insects. To gain a better understanding of how herbivory on PGPR-inoculated plants can cause an increase in secondary metabolites of peppermint, we examined changes in plant defense hormones in inoculated plants after herbivory. We found that the combination of both treatments increased the endogenous jasmonic and salicylic acid levels to the same extent as in plants only inoculated or only insect-damaged. Because different interactions can alter the phytochemistry of plants such as M. piperita, this topic is both ecologically and economically relevant.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

EO:

essential oil

JA:

jasmonic acid

PGPR:

plant growth-promoting rhizobacteria

SA:

salicylic acid

SM:

secondary metabolites

TPC:

total phenolic content

VOC:

volatile organic compounds

References

  • Abdala-Roberts L, Reyes-Hernández M, Quijano-Medina T, Moreira X, Francisco M, Angulo DF, Parra-Tabla V, Virgen A, Rojas JC (2019) Effects of amount and recurrence of leaf herbivory on the induction of direct and indirect defences in wild cotton. Plant Biol 21:1063–1071

    PubMed  CAS  Google Scholar 

  • Agliassa C, Maffei ME (2018) Origanum vulgare terpenoids induce oxidative stress and reduce the feeding activity of Spodoptera littoralis. Int J Mol Sci 19:2805

    PubMed Central  Google Scholar 

  • Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 9:1473

    PubMed  PubMed Central  Google Scholar 

  • Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils - a review. Food Chem Toxicol 46:446–475

    PubMed  CAS  Google Scholar 

  • Banchio E, Valladares G, Zygadlo J, Bogino PC, Rinaudi LV, Giordano W (2007) Changes in composition of essential oils and volatile emissions of Minthostachys mollis, induced by leaf punctures of Liriomyza huidobrensis. Biochem Syst Ecol 35:68–74

    CAS  Google Scholar 

  • Banchio E, Zygadlo J, Valladares GR (2005) Effects of mechanical wounding on essential oil composition and emission of volatiles from Minthostachys mollis. J Chem Ecol 31:719–727

    PubMed  CAS  Google Scholar 

  • Bano A, Muqarab R (2016) Plant defence induced by PGPR against Spodoptera litura in tomato (Solanum lycopersicum L.). Plant Biol 19:406–412

    Google Scholar 

  • Bautista-Lozada A, Bravo-Monzón AE, Espinosa-García FJ (2012) Importancia ecológica de la emisión de compuestos volátiles vegetales. In: Rojas JC, Malo EA (eds) Temas Selectos en Ecología Química de Insectos. El Colegio de la Frontera Sur, México, pp 268–286

    Google Scholar 

  • Beardon E, Scholes J, Ton J (2014) How do beneficial microbes induce systemic resistance? In: Walters DR, Newton AC, Lyon GD (eds) Induced resistance for plant defense: a sustainable approach to crop protection, 2nd edn. UK, Wiley Blackwell, pp 232–248

    Google Scholar 

  • Browse J, Howe GA (2008) New weapons and a rapid response against insect attack. Plant Physiol 146:832–838

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bukovinszky T, van Veen FJ, Jongema Y, Dicke M (2008) Direct and indirect effects of resource quality on food web structure. Science 319:804–807

    PubMed  CAS  Google Scholar 

  • Caarls L, Pieterse CMJ, van Wees SCM (2015) How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6:170

    PubMed  PubMed Central  Google Scholar 

  • Cappellari L, Chiappero J, Santoro M, Giordano W, Banchio E (2017) Inducing phenolic production and volatile organic compounds emission by inoculating Mentha piperita with plant growth-promoting rhizobacteria. Sci Hortic 220:193–198

    CAS  Google Scholar 

  • Cappellari L, Santoro M, Reinoso H, Travaglia C, Giordano W, Banchio E (2015) Anatomical, morphological, and phytochemical effects of inoculation with plant growth promoting rhizobacteria on peppermint (Mentha piperita). J Chem Ecol 41:149–158

    CAS  Google Scholar 

  • Cappellari L, Santoro VM, Schmidt A, Gershenzon J, Banchio E (2019) Induction of essential oil production in Mentha x piperita by plant growth promoting bacteria was correlated with an increase in jasmonate and salicylate levels and a higher density of glandular trichomes. Plant Physiol Biochem 141:142–153

    PubMed  CAS  Google Scholar 

  • Cheynier V (2012) Phenolic compounds: from plants to foods. Phytochem Rev 11:153–177

    CAS  Google Scholar 

  • De Bobadilla MF, Friman J, Pangesti N, Dicke M, van Loon JJA, Pineda A (2017) Does drought stress modify the effects of plant-growth promoting rhizobacteria on an aboveground chewing herbivore? Insect Sci 24:1034–1044

    PubMed  Google Scholar 

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:67–175

    Google Scholar 

  • Diezel C, von Dahl CC, Gaquerel E, Baldwin IT (2009) Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol 150:1576–1586

    PubMed  PubMed Central  CAS  Google Scholar 

  • Dong F, Fu X, Watanabe N, Su X, Yang Z (2016) Recent advances in the emission and functions of plant vegetative volatiles. Molecules 21:124

    PubMed  PubMed Central  Google Scholar 

  • Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32

    PubMed  CAS  Google Scholar 

  • Durak R, Bednarski W, Formela-Luboińska M, Woźniak A, et. al. (2019) Defense responses of Thuja orientalis to infestation of anholocyclic species aphid Cinara tujafilina. J Plant Physiol 232:160–170

  • Farmer EE, Alméras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378

    PubMed  CAS  Google Scholar 

  • Farnad N, Heidari R, Aslanipour B (2014) Phenolic composition and comparison of antioxidant activity of alcoholic extracts of peppermint (Mentha piperita). J Food Meas Charact 8:113–121

    Google Scholar 

  • Freeman BC, Beattie GA (2008) An Overview of Plant Defenses against Pathogens and Herbivores. In: An overview of plant defenses against pathogens and herbivores. Plant Health Instr

    Google Scholar 

  • Greene GL, Leppla NC, Dickerson WA (1976) Velvetbean caterpillar: a rearing procedure and artificial medium. J Econ Entomol 69:487–488

    Google Scholar 

  • Güenther E (1948) The essential oils - Vol. I: history - origin in plants - production - analysis. New York, Estados Unidos. D. van Nostrand company

  • Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272

    PubMed  CAS  Google Scholar 

  • Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184

    PubMed  CAS  Google Scholar 

  • Jullien F (2007) Mint. In: Pua EC, Davey MR (eds) Biotechnology in agriculture and forestry, vol 59. Springer-Verlag, Heidelberg, Germany, pp 435–466

    Google Scholar 

  • Kalske A, Shiojiri K, Uesugi A, Sakata Y, Morrell K, Kessler A (2019) Insect herbivory selects for volatile-mediated plant-plant communication. Curr Biol 29:3128–3133

    PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University Chicago Press, Chicago, pp 33–38

    Google Scholar 

  • Lattanzio V (2013) Phenolic compounds: introduction. In: Ramawat KG, Mérillon JM (eds) Natural products. Springer, Berlin Heidelberg, pp 1543–1580

    Google Scholar 

  • Lubbe A, Verpoorte R (2011) Cultivation of medicinal and aromatic plants for specialty industrial materials. Ind Crop Prod 34:785–801

    CAS  Google Scholar 

  • Martínez-Medina A, Fernández I, Sánchez-Guzmán MJ, Jung SC, Pascual JA, Pozo MJ (2013) Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front Plant Sci 4:206

    PubMed  PubMed Central  Google Scholar 

  • Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse CMJ, Pozo MJ, Ton J, van Dam NM, Conrath U (2016) Recognizing plant defense priming. Trends Plant Sci 21:818–822. https://doi.org/10.1016/j.tplants.2016.07.009

    Article  PubMed  CAS  Google Scholar 

  • Park YG, Mun BG, Kang SM, Hussain A, Shahzad R, Seo C-W, Kim A-Y, Lee S-U, Oh KY, Lee DY, Lee I-J (2017) Yun B-W (2017) Bacillus aryabhattai SRB02 tolerates oxidative and nitrosative stress and promotes the growth of soybean by modulating the production of phytohormones. PLoS One 12(3):e0173203

    PubMed  PubMed Central  Google Scholar 

  • Pieterse CMJ, van Wees SC, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

    PubMed  CAS  Google Scholar 

  • Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514

    PubMed  CAS  Google Scholar 

  • Raguso R, Boland W, Hartmann T, Pickett J, Strack D (2011) Plant-insect interactions. Phytochemistry 72:1495–1496

    PubMed  CAS  Google Scholar 

  • Rashid MHO, Chung YR (2017) Induction of systemic resistance against insect herbivores in plants by beneficial soil microbes. Front Plant Sci 8:1816

    PubMed  PubMed Central  Google Scholar 

  • Rimoldi F, Fogel MN, Schneider MI, Ronco AE (2012) Lethal and sublethal effects of cypermethrin and methoxyfenozide on the larvae of Rachiplusia nu (Guenee) (Lepidoptera: Noctuidae). Invertebr Reprod Dev 56:200–208

    CAS  Google Scholar 

  • Romeiro RS (2007) Control biológico de plantas: fundamentos. Viçosa, Editora UFV, p 269

    Google Scholar 

  • Saharkhiz MJ, Esmaeili S, Merikhi M (2010) Essential oil analysis and phytotoxic activity of two ecotypes of Zataria multiflora Boiss. Growing in Iran. Nat Product Res 24:1598–1609

    CAS  Google Scholar 

  • Santoro MV, Zygadlo J, Giordano W, Banchio E (2011) Volatile organic compounds from rhizobacteria increase biosynthesis of essential oils and growth parameters in peppermint (Mentha piperita). Plant Physiol Biochem 49:1177–1182

    PubMed  CAS  Google Scholar 

  • Santoro VM, Bogino PC, Nocelli N, Cappellari L, Giordano WF, Banchio E (2016) Analysis of plant growth-promoting effects of fluorescent Pseudomonas strains isolated from Mentha piperita rhizosphere and effects of their volatile organic compounds on essential oil composition. Front Microbiol 7:1085

    PubMed  PubMed Central  Google Scholar 

  • Santoro M, Cappellari L, Giordano W, Banchio E (2015) Plant growth promoting effects of native Pseudomonas strains on Mentha piperita (peppermint): an in vitro study. Plant Biol 17:1218–1226

    PubMed  CAS  Google Scholar 

  • Schmidt A, Nagel R, Krekling T, Christiansen E, Gershenzon J, Krokene P (2011) Induction of isoprenyl diphosphate synthases, plant hormones and defense signalling genes correlates with traumatic resin duct formation in Norway spruce (Picea abies). Plant Mol Biol 77:577–590

    PubMed  PubMed Central  CAS  Google Scholar 

  • Schweiger R, Baier MC, Persicke M, Müller C (2014) High specificity in plant leaf metabolic responses to arbuscular mycorrhiza. Nat Commun 5:3886

    PubMed  CAS  Google Scholar 

  • Shikano I, Rosa C, Tan CW, Felton GW (2017) Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annu Rev Phytopathol 55:313–331

    PubMed  CAS  Google Scholar 

  • Singh P, Pandey AK (2018) Prospective of essential oils of the genus Mentha as biopesticides: a review. Front Plant Sci 9:1295

    PubMed  PubMed Central  Google Scholar 

  • Specht A, Guedes JVC, Sulzbach F, Vogt TG (2006) Ocorrência de Rachiplusia nu (Guenée) (Lepidoptera: Noctuidae) em fumo (Nicotiana tabacum L.) no Rio Grande do Sul. Neotrop Entomol 35:705–706

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tissier A, Morgan JA, Dudareva N (2017) Plant volatiles: going 'In' but not 'out' of trichome cavities. Trends Plant Sci 22:930–938

    PubMed  CAS  Google Scholar 

  • Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant-Microbe Interact 18:555–561

    PubMed  CAS  Google Scholar 

  • Turlings TCJ, Erb M (2018) Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu Rev Entomol 63:433–452

    PubMed  CAS  Google Scholar 

  • Valladares GR, Zapata A, Zygadlo J, Banchio E (2002) Phytochemical induction by herbivores could affect quality of essential oil from aromatic plants. J Agr Food Chem 50:4059–4061

    CAS  Google Scholar 

  • Van de Mortel JE, De Vos RCH, Dekkers E, Pineda A, Guillod L, Bouwmeester K, van Loon JJA, Dicke M, Raaijmakers JM (2012) Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160:2173–2188

    PubMed  PubMed Central  Google Scholar 

  • Van der Ent S, Van Hulten MHA, Pozo MJ, Czechowski T, Udvardi MK, Pieterse CM, Ton J (2009) Priming of plant innate immunity by rhizobacteria and β-aminobutyric acid: differences and similarities in regulation. New Phytol 183:419–431

    PubMed  Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    PubMed  Google Scholar 

  • Van Loon LC, van Strien EA (1999) The families of pathogenesis related proteins, their activities, and comparative analysis of PR-1type proteins. Physiol Mol Plant Pathol 55:85–97

    Google Scholar 

  • van Oosten VR, Bodenhausen N, Reymond P, van Pelt JA, van Loon LC, Dicke M, Pieterse CM (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol Plant Microbe Int 21:919–930

    Google Scholar 

  • Vos IA, Moritz L, Pieterse CM, van Wees SC (2015) Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions. Front Plant Sci 6:639. https://doi.org/10.3389/fpls.2015.00639

    Article  PubMed  PubMed Central  Google Scholar 

  • Wasternack C, Strnad M (2017) Jasmonates are signals in the biosynthesis of secondary metabolites - pathways, transcription factors and applied aspects - a brief review. New Biotechnol 48:1–11

    Google Scholar 

  • Yang L, Wen K-S, Ruan X, Zhao Y-X, Wei F, Wang Q (2018) Response of plant secondary metabolites to environmental factors. Molecules 23:762

    PubMed Central  Google Scholar 

  • Zhang L, Zhang F, Melotto M, Yao J, He SY (2017b) Jasmonate signaling and manipulation by pathogens and insects. J Exp Bot 68:1371–1385

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang X, Sun X, Zhao H, Xue M, Wang D (2017a) Phenolic compounds induced by Bemisia tabaci and Trialeurodes vaporariorum in Nicotiana tabacum L. and their relationship with the salicylic acid signaling pathway. Arthropod-Plant Interact 11:659–667

    Google Scholar 

  • Zebelo S, Bertea CM, Bossi S, Occhipinti A, Gnavi G, Maffei ME (2011) Chrysolina herbacea modulates terpenoid biosynthesis of Mentha aquatica L. PLoS One 6:e17195

    CAS  Google Scholar 

  • Zebelo S, Song Y, Kloepper JW, Fadamiro H (2016) Rhizobacteria activates (+)-δ-cadinene synthase genes and induces systemic resistance in cotton against beet armyworm (Spodoptera exigua). Plant Cell Env 39:935–943

    CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from the Secretaría de Ciencia y Técnica de la Universidad Nacional de Río Cuarto, the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), MinCyT Córdoba, and the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) PICT 0636-14, Argentina. EB obtained financial support from a Georg Forster-Research Fellowship of the Alexander von Humboldt Foundation. We thank AgIdea (Agricultural Innovation Applied Research-Argentina) company for providing the insects. The authors are grateful to Dr. Paul Hobson, native speaker, for editorial assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erika Banchio.

Electronic supplementary material

ESM 1

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

del Rosario Cappellari, L., Chiappero, J., Palermo, T.B. et al. Impact of Soil Rhizobacteria Inoculation and Leaf-Chewing Insect Herbivory on Mentha piperita Leaf Secondary Metabolites. J Chem Ecol 46, 619–630 (2020). https://doi.org/10.1007/s10886-020-01193-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-020-01193-3

Keywords

Navigation