Skip to main content

Advertisement

SpringerLink
Log in

Anatomical, Morphological, and Phytochemical Effects of Inoculation with Plant Growth- Promoting Rhizobacteria on Peppermint (Mentha piperita)

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

Abstract

Plant growth-promoting rhizobacteria (PGPR) generally exert their effects through enhancement of plant nutrient status and/or phytohormone production. The effects of PGPR on aromatic plant species are poorly known. We measured plant growth parameters, chlorophyll content, trichome density, stomatal density, and levels of secondary metabolites in peppermint (Mentha piperita) seedlings inoculated with PGPR strains Bacillus subtilis GB03, Pseudomonas fluorescens WCS417r, P. putida SJ04, or a combination of WCS417r + SJ04. The treated plants, in comparison with controls, showed increases in shoot biomass, root biomass, leaf area, node number, trichome density, and stomatal density, and marked qualitative and quantitative changes in monoterpene content. Improved knowledge of the factors that control or affect biosynthesis of secondary metabolites and monoterpene accumulation will lead to strategies for improved cultivation and productivity of aromatic plants and other agricultural crops without the use of chemical fertilizers or pesticides.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135:2025–2037

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bakker PAHM, Pieterse CMJ, Van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathol 97:239–243

    Article  Google Scholar 

  • Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant-plant interactions: “Talking trees” in the genomics era. Science 311:812–815

    Article  CAS  PubMed  Google Scholar 

  • Banchio E, Zygadlo J, Valladares G (2005) Quantitative variations in the essential oil of Minthostachys mollis (Kunth.) Griseb. in response to insects with different feeding habits. J Agric Food Chem 53:6903–6906

    Article  CAS  PubMed  Google Scholar 

  • Banchio E, Bogino P, Zygadlo J, Giordano W (2008) Plant growth promoting rhizobacteria improve growth and essential oil yield in Origanum majorana L. Biochem Syst Ecol 36:766771

    Article  Google Scholar 

  • Banchio E, Xie X, Zhang H, Paré PW (2009) Soil bacteria elevate essential oil accumulation and emissions in sweet basil. J Agric Food Chem 5:653–657

    Article  Google Scholar 

  • Banchio E, Bogino P, Santoro MV, Torres L, Zygadlo J, Giordano W (2010) Systemic induction of monoterpene biosynthesis in Origanum x majoricum by soil bacteria. J Agric Food Chem 58:650–654

    Article  CAS  PubMed  Google Scholar 

  • Barbieri G, Vallone S, Orsini F, Paradiso R, De Pascale S, Negre-Zakharov F, Maggio A (2012) Stomatal density and metabolic determinants mediate salt stress adaptation and water use efficiency in basil (Ocimum basilicum L.). J Plant Physiol 169:1737–1746

    Article  CAS  PubMed  Google Scholar 

  • Berry JA, Beerling DJ, Franks PJ (2010) Stomata: key players in the Earth system, past and present. Curr Opin Plant Biol 13:233–240

    Article  PubMed  Google Scholar 

  • Bhattarai T, Hess D (1993) Yield responses of Nepalese spring wheat (Triticum aestivum L.) cultivars to inoculation with Azospirillum spp. of Nepalese origin. Plant Soil 151:67–76

    Article  CAS  Google Scholar 

  • Bosabalidis AM (2002) Structural features of Origanum sp. In: Kintzios SE (ed) Medicinal and aromatic plants-Industrial profiles, Oregano. The genera Origanum and Lippia. Taylor and Francis, London, pp 11–64

    Google Scholar 

  • Boughton AJ, Hoover K, Felton GW (2005) Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J Chem Ecol 31:2211–2216

    Article  CAS  PubMed  Google Scholar 

  • Bouwmeester HJ, Roux C, Lopez-Raez JA, Becard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230

    Article  CAS  PubMed  Google Scholar 

  • Cappellari L, Santoro MV, Nievas F, Giordano W, Banchio E (2013) Increase of secondary metabolite content in marigold by inoculation with plant growth-promoting rhizobacteria. Appl Soil Ecol 70:16–22

    Article  Google Scholar 

  • Chalchat JC, Garry RP, Michet A (1997) Variation of the chemical composition of essential oil of Mentha piperita L. during the growing time. J Essent Oil Res 9:463–465

    Article  CAS  Google Scholar 

  • Colla G, Rouphael Y, Cardarelli M, Tullio M, Rivera CM, Rea E (2008) Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol Fert Soils 44:501–509

    Article  CAS  Google Scholar 

  • Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531

    Article  CAS  PubMed  Google Scholar 

  • Copetta A, Lingua G, Berta G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum brasilicum L. var. Genovese. Mycorrhiza 16:485–494

    Article  CAS  PubMed  Google Scholar 

  • D’Ambrogio de Argüeso A (1986) Manual de técnicas en histología vegetal. Buenos Aires, Hemisferio Sur

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Figueiredo MVB, Seldin L, de Araujo FF, Mariano RLR (2010) Plant growth promoting rhizobacteria: fundamentals and applications. In: Maheshwari DK (ed) Plant growth and health promoting bacteria. Springer, Berlin Heidelberg, pp 21–43

    Chapter  Google Scholar 

  • Ghirardo A, Gutknecht J, Zimmer I, Brüggemann N, Schnitzler JP (2011) Biogenic volatile organic compound and respiratory CO2 emissions after 13C-labeling: online tracing of C translocation dynamics in poplar plants. PLoS One 6:e17393

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Giri B, Kapoor R, Mukerji KG (2003) Influence of Arbuscular mycorrhizal fungi and salinity on growth, biomass and mineral nutrition of Acacia auriculiformis. Biol Fert Soils 38:170175

    Article  Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 4:109–117

    Article  Google Scholar 

  • Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signalling processes. Soil Biol Biochem 37:395–412

    Article  CAS  Google Scholar 

  • Gupta ML, Prasad A, Ram M, Kumar S (2002) Effect of the vesicular-arbuscular mycorrhizal (VAM) fungus Glomus fasciculatum on the essential oil yield related characters and nutrient acquisition in the crops of different cultivars of menthol mint (Mentha arvensis) under field conditions. Bioresour Technol 81:77–79

    Article  CAS  PubMed  Google Scholar 

  • Harrewijn P, Van Oosten AM, Piron PGM (2001) Natural terpenoids as messengers: a multidisciplinary study of their production, biological functions, and practical applications. Springer, Kluwer Academic Publisher, Netherlands

    Google Scholar 

  • Heil M, Silva Bueno JC (2007) Within-plant signalling by volatiles leads to induction and priming of an indirect plant defence in nature. Proc Natl Acad Sci U S A 104:5467–5472

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hudaib M, Speroni E, Di Pietra AM, Cavrini V (2002) GC/MS evaluation of thyme (Thymus vulgaris L.) oil composition and variations during the vegetative cycle. J Pharm Biomed Anal 29:691–700

    Article  CAS  PubMed  Google Scholar 

  • Hummelbrunner LA, Isman MB (2001) Acute, sublethal, antifeedant, and synergistic effects of monoterpenoid essential oil compounds on the tobacco cutworm, Spodoptera litura (Lep., Noctuidae). J Agric Food Chem 49:715–720

    Article  CAS  PubMed  Google Scholar 

  • Karousou R, Grammatikopoulos G, Lanaras T, Manetas Y, Kokkini S (1998) Effects of UV-B radiation on Mentha spicata essential oils. Phytochemistry 49:2273–2277

    Article  CAS  Google Scholar 

  • Khaosaad T, Vierheiling H, Nell M, Zitterl-Eglsser K, Novak J (2006) Arbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16:443–446

    Article  CAS  PubMed  Google Scholar 

  • Kloepper JW (1993) Plant-growth-promoting rhizobacteria as biological control agents. In: Metting FB (ed) Soil microbial ecology: applications in agricultural and environmental management. Marcel Dekker, New York, pp 255–273

    Google Scholar 

  • Lamiri A, Lhaloui S, Benjilali B, Berrada M (2001) Insecticidal effects of essential oils against Hessian fly, Mayetiola destructor (Say). Field Crops Res 71:9–15

    Article  Google Scholar 

  • Lange BM, Ahkami A (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes—current status and future opportunities. Plant Biotech J 11:169–196

    Article  CAS  Google Scholar 

  • Lange BM, Turner GW (2012) Terpenoid biosynthesis in trichomes—current status and future opportunities. Plant Biotech J 11:2–22

    Article  Google Scholar 

  • Lange BM, Mahmoud SS, Wildung MR, Turner GW, Davis EM (2011) Improving peppermint essential oil yield and composition by metabolic engineering. Proc Natl Acad Sci U S A 108:16944–16949

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lawrence BM (2007) Mint: the genus mentha. Medicinal and aromatic plants—industrial profiles. CRC Press/Taylor & Francis, Boca Raton

    Google Scholar 

  • Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA (2004) The tomato homolog of Coronatine-Insensitive 1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16:126–143

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lind K, Lafer G, Schloffer K, Innerhoffer G, Meister H (2004) Organic fruit growing. UK. CABI Publishing, Wallingford

    Google Scholar 

  • Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth promoting rhizobacteria. Anton van Lee Int JG 86:1–25

    Article  CAS  Google Scholar 

  • Marimuthu S, Subbian P, Ramamoorthy V, Samiyappan R (2002) Synergistic effect of combined application of Azospirillum and Pseudomonas fluorescens with inorganic fertilizer on root rot incidence and yield of cotton. J Plant Dis Protect 109:569–577

    Google Scholar 

  • Mc Kinney G (1938) Some absorption spectra of leaf extract. Plant Physiol 13:128–140

    Google Scholar 

  • McCaskill D, Croteau R (1995) Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha × piperita) rely exclusively on plastid-derived isopentenyl diphosphate. Planta 197:49–56

    Article  CAS  Google Scholar 

  • MIRC (2010) Mint Industry Res. Council, Great Falls, MT. Available at http://usmintindustry.org/ (accessed March 2014)

  • Mucciarelli M, Scannerini S, Bertea C, Maffei M (2003) In vitro and in vivo peppermint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. New Phytol 158:579–591

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assay with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Niranjan RS, Shetty HS, Reddy MS (2006) Plant growth promoting rhizobacteria: potential green alternative for plant productivity. In: Siddiqui ZA (ed) PGPR: Biocontrol and biofertilization. Springer, Netherlands, pp 197–216

    Chapter  Google Scholar 

  • Panou-Filotheou H, Bosabalidis AM, Karataglis S (2001) Effects of copper toxicity on leaves of oregano (Origanum vulgare subsp. hirtum). Ann Bot 88:207–214

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  CAS  PubMed  Google Scholar 

  • Rios-Estepa R, Lange I, Lee JM, Lange BM (2010) Mathematical modeling-guided evaluation of biochemical, developmental, environmental, and genotypic determinants of essential oil composition and yield in peppermint leaves. Plant Physiol 152:2105–2119

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268:285–292

    Article  CAS  Google Scholar 

  • Sangwan NS, Farooqi AHA, Shabih F, Sangwan RS (2001) Regulation of essential oil production in plants. Plant Growth Regul 24:3–21

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Schisler DA, Slininger PJ, Bothast RJ (1997) Effects of antagonist cell concentration and two strain mixtures on biological control of Fusarium dry rot of potatoes. Phytopathol 87:177–183

    Article  CAS  Google Scholar 

  • Schlüter U, Muschak M, Berger D, Altmann T (2003) Photosynthetic performance of an Arabidopsis mutant with elevated stomatal density (sdd1-1) under different light regimes. J Exp Bot 54:867–874

    Article  PubMed  Google Scholar 

  • Schmidt CS, Agostini F, Simon AM, Whyte J, Townend J, Lifert C, Killham K, Mullins C (2004) Influence of soil type and pH on the colonization of sugar beet seedlings by antagonistic Pseudomonas and Bacillus strains, and on their control of Pythium dampingoff. Eur J Plant Pathol 110:1025–1046

    Article  Google Scholar 

  • Shukla A, Abad Farooqi AH, Shukla YN, Sharma S (1992) Effect of triacontanol and chlormequat on growth, plant hormones andartemisinin yield in Artemisia annua L. Plant Growth Regul 11:165–171

    Article  CAS  Google Scholar 

  • Singh N, Luthra R, Sangwan RS (1991) Mobilization of starch and essential oil biogenesis during leaf ontogeny of lemongrass (Cymbopogon flexuosus Stapf.). Plant Cell Physiol 32:803–811

    CAS  Google Scholar 

  • Subramanian KS, Charest C (1997) Nutritional, growth, and reproductive responses of maize (Zea mays L.) to arbuscular mycorrhizal inoculation during and after drought stress at tasselling. Mycorrhiza 7:25–32

    Article  Google Scholar 

  • Turner GW, Gershenzon J, Croteau RB (2000) Development of peltate glandular trichomes of peppermint. Plant Physiol 124:665–680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Unsicker S, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485

    Article  CAS  PubMed  Google Scholar 

  • Van Loon LC (2007) Plant response to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volátiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Vestberg M, Cassells AC (2009) The use of AMF and PGPR inoculants singly and combined, to promote microplant establishment, growth and health. In: Varma A, Kharkwal AC (eds) Symbiotic fungi: principles and practice. Springer, New York, pp 337–360

    Chapter  Google Scholar 

  • Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291

    Article  CAS  PubMed  Google Scholar 

  • Wenke K, Kai M, Piechulla B (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506

    Article  CAS  PubMed  Google Scholar 

  • Werker E (2000) Trichome diversity and development. In: Hallahan DL, Gray JC (eds) Advances in botanical research. Academic, San Diego, pp 37–75

    Google Scholar 

  • Zahir AZ, Arshad M, Frankenberger ET Jr (2004) Plant growth promoting rhizobacteria: application and respectives in agriculture. Adv Agron 81:97–168

    Article  CAS  Google Scholar 

  • Zamioudis C, Pieterse CM (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe 25:139–150

    Article  CAS  Google Scholar 

  • Zeng Y, Gu LP, Che DB, Hao ZP, Wang JY, Huang LQ, Yang G, Cui XM, Yang L, Wu ZX, Chen ML, Zhang Y (2013) Arbuscular mycorrhizal symbiosys and active ingredients of medicinal plants: current research status and prospectives. Mycorrhiza 23:253–265

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273

    Article  CAS  PubMed  Google Scholar 

  • Zheljazkov VD, Cantrell CL, Astatkie T, Ebelhar MW (2010) Productivity, oil content and composition of two spearmint species in Mississippi. Agron J102:129–133

    Article  Google Scholar 

  • Zhu XC, Song FB, Liu SQ, Liu TD, Zhou X (2012) Arbuscular mycorrhizae improves photosynthesis and water status of Zea mays L. under drought stress. Plant Soil Environ 58:186–191

    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), Argentina. CT, EB, and WG are Career Members of CONICET. LC and MVS received fellowships from CONICET- MinCyT. The authors are grateful to Dr. S. Anderson for English editing of the manuscript.

Author information

Authors and Affiliations

  1. Departamento Biología Molecular, FCEFQyN, Universidad Nacional de Río Cuarto, Campus Universitario, 5800, Río Cuarto, Argentina

    Lorena del Rosario Cappellari, Maricel Valeria Santoro, Walter Giordano & Erika Banchio

  2. Departamento Ciencias Naturales, FCEFQyN, Universidad Nacional de Río Cuarto, Campus Universitario, 5800, Río Cuarto, Argentina

    Herminda Reinoso & Claudia Travaglia

Authors
  1. Lorena del Rosario Cappellari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maricel Valeria Santoro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Herminda Reinoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claudia Travaglia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Walter Giordano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Erika Banchio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Erika Banchio.

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., Santoro, M.V., Reinoso, H. et al. Anatomical, Morphological, and Phytochemical Effects of Inoculation with Plant Growth- Promoting Rhizobacteria on Peppermint (Mentha piperita). J Chem Ecol 41, 149–158 (2015). https://doi.org/10.1007/s10886-015-0549-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-015-0549-y

Keywords

Search

Navigation