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Journal of Chemical Ecology

, Volume 41, Issue 2, pp 149–158 | Cite as

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

  • Lorena del Rosario Cappellari
  • Maricel Valeria Santoro
  • Herminda Reinoso
  • Claudia Travaglia
  • Walter Giordano
  • Erika Banchio
Article

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.

Keywords

Glandular trichome Mint Secondary metabolites Stomatal density Lamiaceae sustainable agriculture 

Notes

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.

References

  1. 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 135:2025–2037CrossRefPubMedCentralPubMedGoogle Scholar
  2. Arnon DI (1949) Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefPubMedCentralPubMedGoogle Scholar
  3. Bakker PAHM, Pieterse CMJ, Van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathol 97:239–243CrossRefGoogle Scholar
  4. 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 311:812–815CrossRefPubMedGoogle Scholar
  5. 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 53:6903–6906CrossRefPubMedGoogle Scholar
  6. 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 36:766771CrossRefGoogle Scholar
  7. Banchio E, Xie X, Zhang H, Paré PW (2009) Soil bacteria elevate essential oil accumulation and emissions in sweet basil. J Agric Food Chem 5:653–657CrossRefGoogle Scholar
  8. 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 58:650–654CrossRefPubMedGoogle Scholar
  9. 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 169:1737–1746CrossRefPubMedGoogle Scholar
  10. Berry JA, Beerling DJ, Franks PJ (2010) Stomata: key players in the Earth system, past and present. Curr Opin Plant Biol 13:233–240CrossRefPubMedGoogle Scholar
  11. 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 151:67–76CrossRefGoogle Scholar
  12. 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 11–64Google Scholar
  13. Boughton AJ, Hoover K, Felton GW (2005) Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J Chem Ecol 31:2211–2216CrossRefPubMedGoogle Scholar
  14. Bouwmeester HJ, Roux C, Lopez-Raez JA, Becard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230CrossRefPubMedGoogle Scholar
  15. 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 70:16–22CrossRefGoogle Scholar
  16. 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 9:463–465CrossRefGoogle Scholar
  17. 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 44:501–509CrossRefGoogle Scholar
  18. Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531CrossRefPubMedGoogle Scholar
  19. 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 16:485–494CrossRefPubMedGoogle Scholar
  20. D’Ambrogio de Argüeso A (1986) Manual de técnicas en histología vegetal. Buenos Aires, Hemisferio SurGoogle Scholar
  21. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149CrossRefGoogle Scholar
  22. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280CrossRefPubMedCentralPubMedGoogle Scholar
  23. 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 21–43CrossRefGoogle Scholar
  24. 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:e17393CrossRefPubMedCentralPubMedGoogle Scholar
  25. 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 38:170175CrossRefGoogle Scholar
  26. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 4:109–117CrossRefGoogle Scholar
  27. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signalling processes. Soil Biol Biochem 37:395–412CrossRefGoogle Scholar
  28. 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 81:77–79CrossRefPubMedGoogle Scholar
  29. 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, NetherlandsGoogle Scholar
  30. 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 104:5467–5472CrossRefPubMedCentralPubMedGoogle Scholar
  31. 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 29:691–700CrossRefPubMedGoogle Scholar
  32. 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 49:715–720CrossRefPubMedGoogle Scholar
  33. Karousou R, Grammatikopoulos G, Lanaras T, Manetas Y, Kokkini S (1998) Effects of UV-B radiation on Mentha spicata essential oils. Phytochemistry 49:2273–2277CrossRefGoogle Scholar
  34. 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 16:443–446CrossRefPubMedGoogle Scholar
  35. 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 255–273Google Scholar
  36. Lamiri A, Lhaloui S, Benjilali B, Berrada M (2001) Insecticidal effects of essential oils against Hessian fly, Mayetiola destructor (Say). Field Crops Res 71:9–15CrossRefGoogle Scholar
  37. Lange BM, Ahkami A (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes—current status and future opportunities. Plant Biotech J 11:169–196CrossRefGoogle Scholar
  38. Lange BM, Turner GW (2012) Terpenoid biosynthesis in trichomes—current status and future opportunities. Plant Biotech J 11:2–22CrossRefGoogle Scholar
  39. 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 108:16944–16949CrossRefPubMedCentralPubMedGoogle Scholar
  40. Lawrence BM (2007) Mint: the genus mentha. Medicinal and aromatic plants—industrial profiles. CRC Press/Taylor & Francis, Boca RatonGoogle Scholar
  41. 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 16:126–143CrossRefPubMedCentralPubMedGoogle Scholar
  42. Lind K, Lafer G, Schloffer K, Innerhoffer G, Meister H (2004) Organic fruit growing. UK. CABI Publishing, WallingfordGoogle Scholar
  43. Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth promoting rhizobacteria. Anton van Lee Int JG 86:1–25CrossRefGoogle Scholar
  44. 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 109:569–577Google Scholar
  45. Mc Kinney G (1938) Some absorption spectra of leaf extract. Plant Physiol 13:128–140Google Scholar
  46. McCaskill D, Croteau R (1995) Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha × piperita) rely exclusively on plastid-derived isopentenyl diphosphate. Planta 197:49–56CrossRefGoogle Scholar
  47. MIRC (2010) Mint Industry Res. Council, Great Falls, MT. Available at http://usmintindustry.org/ (accessed March 2014)
  48. 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 158:579–591CrossRefGoogle Scholar
  49. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assay with tobacco tissue culture. Physiol Plant 15:473–497CrossRefGoogle Scholar
  50. 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 197–216CrossRefGoogle Scholar
  51. Panou-Filotheou H, Bosabalidis AM, Karataglis S (2001) Effects of copper toxicity on leaves of oregano (Origanum vulgare subsp. hirtum). Ann Bot 88:207–214CrossRefGoogle Scholar
  52. 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 15:507–514CrossRefPubMedGoogle Scholar
  53. Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398CrossRefPubMedGoogle Scholar
  54. 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 152:2105–2119CrossRefPubMedCentralPubMedGoogle Scholar
  55. Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268:285–292CrossRefGoogle Scholar
  56. Sangwan NS, Farooqi AHA, Shabih F, Sangwan RS (2001) Regulation of essential oil production in plants. Plant Growth Regul 24:3–21CrossRefGoogle Scholar
  57. 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 49:1177–1182CrossRefPubMedGoogle Scholar
  58. 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 87:177–183CrossRefGoogle Scholar
  59. 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 54:867–874CrossRefPubMedGoogle Scholar
  60. 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 110:1025–1046CrossRefGoogle Scholar
  61. 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 11:165–171CrossRefGoogle Scholar
  62. 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 32:803–811Google Scholar
  63. 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 7:25–32CrossRefGoogle Scholar
  64. Turner GW, Gershenzon J, Croteau RB (2000) Development of peltate glandular trichomes of peppermint. Plant Physiol 124:665–680CrossRefPubMedCentralPubMedGoogle Scholar
  65. Unsicker S, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485CrossRefPubMedGoogle Scholar
  66. Van Loon LC (2007) Plant response to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254CrossRefGoogle Scholar
  67. 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 21:919–930CrossRefPubMedGoogle Scholar
  68. Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volátiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641CrossRefPubMedCentralPubMedGoogle Scholar
  69. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586CrossRefGoogle Scholar
  70. 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 337–360CrossRefGoogle Scholar
  71. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291CrossRefPubMedGoogle Scholar
  72. Wenke K, Kai M, Piechulla B (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506CrossRefPubMedGoogle Scholar
  73. Werker E (2000) Trichome diversity and development. In: Hallahan DL, Gray JC (eds) Advances in botanical research. Academic, San Diego, pp 37–75Google Scholar
  74. Zahir AZ, Arshad M, Frankenberger ET Jr (2004) Plant growth promoting rhizobacteria: application and respectives in agriculture. Adv Agron 81:97–168CrossRefGoogle Scholar
  75. Zamioudis C, Pieterse CM (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe 25:139–150CrossRefGoogle Scholar
  76. 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 23:253–265CrossRefPubMedGoogle Scholar
  77. 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 226:839–851CrossRefPubMedGoogle Scholar
  78. 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 56:264–273CrossRefPubMedGoogle Scholar
  79. Zheljazkov VD, Cantrell CL, Astatkie T, Ebelhar MW (2010) Productivity, oil content and composition of two spearmint species in Mississippi. Agron J102:129–133CrossRefGoogle Scholar
  80. 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 58:186–191Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Lorena del Rosario Cappellari
    • 1
  • Maricel Valeria Santoro
    • 1
  • Herminda Reinoso
    • 2
  • Claudia Travaglia
    • 2
  • Walter Giordano
    • 1
  • Erika Banchio
    • 1
  1. 1.Departamento Biología Molecular, FCEFQyNUniversidad Nacional de Río CuartoRío CuartoArgentina
  2. 2.Departamento Ciencias Naturales, FCEFQyNUniversidad Nacional de Río CuartoRío CuartoArgentina

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