, Volume 26, Issue 2, pp 123–131 | Cite as

Arbuscular mycorrhiza differentially affects synthesis of essential oils in coriander and dill

  • Jana Rydlová
  • Marcela Jelínková
  • Karel Dušek
  • Elena Dušková
  • Miroslav Vosátka
  • David Püschel
Original Paper


Research on the role of arbuscular mycorrhizal fungi (AMF) in the synthesis of essential oils (EOs) by aromatic plants has seldom been conducted in field-relevant conditions, and then, only limited spectra of EO constituents have been analyzed. The effect was investigated of inoculation with AMF on the synthesis of a wide range of EO in two aromatic species, coriander (Coriandrum sativum) and dill (Anethum graveolens), in a garden experiment under outdoor conditions. Plants were grown in 4-l pots filled with soil, which was either γ-irradiated (eliminating native AMF) or left non-sterile (containing native AMF), and inoculated or not with an isolate of Rhizophagus irregularis. AMF inoculation significantly stimulated EO synthesis in both plant species. EO synthesis (total EO and several individual constituents) was increased in dill in all mycorrhizal treatments (containing native and/or inoculated AMF) compared to non-mycorrhizal plants. In contrast, EO concentrations in coriander (total EO and most constituents) were increased only in the treatment combining both inoculated and native AMF. A clear positive effect of AMF on EO synthesis was found for both aromatic plants, which was, however, specific for each plant species and modified by the pool of AMF present in the soil.


Aromatic plants Dill Coriander Essential oils Arbuscular mycorrhiza Growth responses 



The authors are grateful to Pavla Doubková for valuable comments on the text of the manuscript and to Marie Albrechtová and Hana Strusková from the Analytical Laboratories of the Institute of Botany AS CR who performed soil chemical analyses and determined the content of phosphorus in plant biomass. Financial support for this study was provided by the Ministry of Education, Youth and Sports of the Czech Republic (grant 1M0571), by the long-term research development project RVO 67985939 and grant no. ED0007/01/01 Centre of the Region Haná for Biotechnological and Agricultural Research.


  1. Allen MF, Moore TS, Christensen M (1980) Phytohormone changes in Bouteloua gracilis infected by vesicular-arbuscular mycorrhizae.1. Cytokinin increases in the host plant. Can J Bot 58:371–374CrossRefGoogle Scholar
  2. Allen MF, Moore TS, Christensen M (1982) Phytohormone changes in Bouteloua gracilis infected by vesicular arbuscular mycorrhizae. 2. Altered levels of gibberellin-like substances and abscisic acid in the host plant and abscisic-acid in the host plant. Can J Bot 60:468–471CrossRefGoogle Scholar
  3. Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  4. Avio L, Pellegrino E, Bonari E, Giovannetti M (2006) Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytol 172:347–357CrossRefPubMedGoogle Scholar
  5. Bakkali F, Averbeck S, Averbeck D, Waomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475CrossRefPubMedGoogle Scholar
  6. Bassole IHN, Juliani HR (2012) Essential oils in combination and their antimicrobial properties. Molecules 17:3989–4006CrossRefPubMedGoogle Scholar
  7. Bennet AE, Bever JD (2009) Trade-offs between arbuscular mycorrhizal fungal competive ability and host growth promotion. Oecologia 160:807–816CrossRefGoogle Scholar
  8. Binet MN, van Tuinen D, Depretre N, Koszela N, Chambon C, Gianinazzi S (2011) Arbuscular mycorrhizal fungi associated with Artemisia umbelliformis Lam, an endangered aromatic species in Southern French Alps, influence plant P and essential oil contents. Mycorrhiza 21:523–535CrossRefPubMedGoogle Scholar
  9. Burni T, Hussain F, Sharif M (2013) Effect of arbuscular mycorrhizal fungi on essential oils of two pharmaceutically important Mentha species in marginal soils. Pakistan J Bot 45:293–296Google Scholar
  10. Chaudhary V, Kapoor R, Bhatnagar AK (2008) Effectiveness of two arbuscular mycorrhizal fungi on concentrations of essential oil and artemisinin in three accessions of Artemisia annua L. Appl Soil Ecol 40:174–181CrossRefGoogle Scholar
  11. Copetta A, Lingua G, Berta G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mycorrhiza 16:485–494CrossRefPubMedGoogle Scholar
  12. de Novais CB, Borges WL, Jesus ED, Saggin OJ, Siqueira JO (2014) Inter- and intraspecific functional variability of tropical arbuscular mycorrhizal fungi isolates colonizing corn plants. Appl Soil Ecol 76:78–86CrossRefGoogle Scholar
  13. Dugassa GD, vonAlten H, Schonbeck F (1996) Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant Soil 185:173–182CrossRefGoogle Scholar
  14. Farahani HA, Lebaschi MH, Hamidi A (2008) Effect of arbuscular mycorrhizal fungi, phosphorus and water stress on quantity and quality characteristics of coriander. Adv Nat Appl Sci 2:55–59Google Scholar
  15. Fitter AH, Helgason T, Hodge A (2011) Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implication for sustainable agriculture. Fungal Biol Rev 25:68–72CrossRefGoogle Scholar
  16. Geneva MP, Stancheva IV, Boychinova MM, Mincheva NH, Yonova PA (2010) Effects of foliar fertilization and arbuscular mycorrhizal colonization on Salvia officinalis L. growth, antioxidant capacity, and essential oil composition. J Sci Food Agr 90:696–702Google Scholar
  17. Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244CrossRefGoogle Scholar
  18. Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  19. Grassmann J (2005) Terpenoids as plant antioxidants. Vitam Horm 72:505–535CrossRefPubMedGoogle Scholar
  20. 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. Bioresource Technol 81:77–79CrossRefGoogle Scholar
  21. Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344CrossRefGoogle Scholar
  22. Janoušková M, Krak K, Wagg C, Štorchová H, Caklová P, Vosátka M (2013) Effects of inoculum additions in the presence of a preestablished arbuscular mycorrhizal fungal community. Appl Environ Microb 79:6507–6515CrossRefGoogle Scholar
  23. Kapoor R, Giri B, Mukerji KG (2002a) Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in dill (Anethum graveolens L.) and carum (Trachyspermum ammi (Linn.) Sprague). World J Microb Biot 18:459–463CrossRefGoogle Scholar
  24. Kapoor R, Giri B, Mukerji KG (2002b) Mycorrhization of coriander (Coriandrum sativum L.) to enhance the concentration and quality of essential oil. J Sci Food Agr 82:339–342CrossRefGoogle Scholar
  25. Kapoor R, Giri B, Mukerji KG (2004) Improved growth and essential oil yield and quality in Foeniculum vulgare mill on mycorrhizal inoculation supplemented with P-fertilizer. Bioresource Technol 93:307–311CrossRefGoogle Scholar
  26. Kapoor R, Chaudhary V, Bhatnagar AK (2007) Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza 17:581–587CrossRefPubMedGoogle Scholar
  27. Karagiannidis N, Thomidis T, Lazari D, Panou-Filotheou E, Karagiannidou C (2011) Effect of three Greek arbuscular mycorrhizal fungi in improving the growth, nutrient concentration, and production of essential oils of oregano and mint plants. Sci Hortic 129:329–334CrossRefGoogle Scholar
  28. Khaosaad T, Vierheilig H, Nell M, Zitterl-Eglseer K, Novak J (2006) Arbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16:443–446CrossRefPubMedGoogle Scholar
  29. Koch AM, Antunes PM, Barto EK, Cipollini D, Mummey DL, Klironomos JN (2011) The effects of arbuscular mycorrhizal (AM) fungal and garlic mustard introductions on native AM fungal diversity. Biol Invasions 13:1627–1639CrossRefGoogle Scholar
  30. Kon KV, Rai MK (2012) Plant essential oils and their constituents in coping with multidrug-resistant bacteria (vol 10, pg 775, 2012). Expert Rev Anti-Infe 10:1070–1070Google Scholar
  31. Kopáček J, Hejzlar J (1995) Semi-micro determination of total phosphorus in soils, sediments, and organic materials—a simplified perchloric-acid digestion procedure. Commun Soil Sci Plan 26:1935–1946CrossRefGoogle Scholar
  32. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505CrossRefGoogle Scholar
  33. Lange BM, Mahmoud SS, Wildung MR, Turner GW, Davis EM, Lange I, Baker RC, Boydston RA, Croteau RB (2011) Improving peppermint essential oil yield and composition by metabolic engineering. Proc Natl Acad Sci U S A 108:16944–16949PubMedCentralCrossRefPubMedGoogle Scholar
  34. Loomis WD, Corteau L (1972) Essential oil biosynthesis. Recent Adv Phytochem 6:147–185CrossRefGoogle Scholar
  35. Lücker J, Bouwmeester HJ, Aharoni A (2007) Metabolic engineering of terpenoid biosynthesis in plants. In: Verpoorte R, Alfermann AW, Johnson TS (eds) Applications of plant metabolic engineering. Springer, Berlin, pp 219–236CrossRefGoogle Scholar
  36. Maes L, Inze D, Goossens A (2008) Functional specialization of the TRANSPARENT TESTA GLABRA1 network allows differential hormonal control of laminal and marginal trichome initiation in Arabidopsis rosette leaves. Plant Physiol 148:1453–1464PubMedCentralCrossRefPubMedGoogle Scholar
  37. Maes L, Van Nieuwerburgh FCW, Zhang YS, Reed DW, Pollier J, Casteele SRFV, Inze D, Covello PS, Deforce DLD, Goossens A (2011) Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants. New Phytol 189:176–189CrossRefPubMedGoogle Scholar
  38. Mandal S, Evelin H, Girl B, Singh VP, Kapoor R (2013) Arbuscular mycorrhiza enhances the production of stevioside and rebaudioside-A in Stevia rebaudiana via nutritional and non-nutritional mechanisms. Appl Soil Ecol 72:187–194CrossRefGoogle Scholar
  39. Mandal S, Upadhyay S, Wajid S, Ram M, Jain DC, Singh VP, Abdin MZ, Kapoor R (2015) Arbuscular mycorrhiza increase artemisinin accumulation in Artemisia annua by higher expression of key biosynthesis genes via enhanced jasmonic acid levels. Mycorrhiza 25:345–357Google Scholar
  40. Morone-Fortunato I, Avato P (2008) Plant development and synthesis of essential oils in micropropagated and mycorrhiza inoculated plants of Origanum vulgare L. ssp hirtum (Link) Ietswaart. Plant Cell Tissue Organ Cult 93:139–149CrossRefGoogle Scholar
  41. Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364CrossRefGoogle Scholar
  42. Nell M, Votsch M, Vierheilig H, Steinkellner S, Zitterl-Eglseer K, Franz C, Novak J (2009) Effect of phosphorus uptake on growth and secondary metabolites of garden sage (Salvia officinalis L.). J Sci Food Agr 89:1090–1096CrossRefGoogle Scholar
  43. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. P Roy Soc B-Biol Sci 276:4237–4245CrossRefGoogle Scholar
  44. Püschel D, Rydlová J, Sudová R, Gryndler M, Vosátka M (2011) The potential of mycorrhizal inoculation and organic amendment to increase yields of Galega orientalis and Helianthus tuberosus in a spoil-bank substrate. J Plant Nutr Soil Sci 174:664–672CrossRefGoogle Scholar
  45. Püschel D, Rydlová J, Vosátka M (2014) Can mycorrhizal inoculation stimulate the growth and flowering of peat-grown ornamental plants under standard or reduced watering? Appl Soil Ecol 80:93–99CrossRefGoogle Scholar
  46. Rapparini F, Llusia J, Penuelas J (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol 10:108–122CrossRefPubMedGoogle Scholar
  47. Rasouli-Sadaghiani M, Hassani A, Barin M, Danesh YR, Sefidkon F (2010) Effects of arbuscular mycorrhizal (AM) fungi on growth, essential oil production and nutrient uptake in basil. J Medicinal Plants Res 4:2222–2228Google Scholar
  48. Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annu Rev Entomol 57:405–424CrossRefPubMedGoogle Scholar
  49. Sbrana C, Avio L, Giovannetti M (2014) Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35:1535–1546CrossRefPubMedGoogle Scholar
  50. Schroeder V, Gange AC, Stead AD (2012) Underground networking: the potential for improving yield and quality of pot-grown herbs with mycorrhizas. J Sci Food Agr 92:203–206CrossRefGoogle Scholar
  51. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  52. Sudová R, Pánková H, Rydlová J, Münzbergová Z, Suda J (2014) Intraspecific ploidy variation: a hidden, minor player in plant-soil-mycorrhizal fungi interactions. Am J Bot 101:26–33CrossRefPubMedGoogle Scholar
  53. Toussaint JP (2007) Investigating physiological changes in the aerial parts of AM plants: what do we know and where should we be heading? Mycorrhiza 17:349–353CrossRefPubMedGoogle Scholar
  54. Toussaint JP, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297CrossRefPubMedGoogle Scholar
  55. Zeng Y, Guo LP, Chen BD, Hao ZP, Wang JY, Huang LQ, Yang G, Cui XM, Yang L, Wu ZX, Chen ML, Zhang Y (2013) Arbuscular mycorrhizal symbiosis and active ingredients of medicinal plants: current research status and prospectives. Mycorrhiza 23:253–265CrossRefPubMedGoogle Scholar
  56. Zubek S, Mielcarek S, Turnau K (2012) Hypericin and pseudohypericin concentrations of a valuable medicinal plant Hypericum perforatum L. are enhanced by arbuscular mycorrhizal fungi. Mycorrhiza 22:149–156PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jana Rydlová
    • 1
  • Marcela Jelínková
    • 2
  • Karel Dušek
    • 2
  • Elena Dušková
    • 2
  • Miroslav Vosátka
    • 1
  • David Püschel
    • 1
  1. 1.Institute of BotanyAcademy of Sciences of the Czech RepublicPrůhoniceCzech Republic
  2. 2.Crop Research InstituteOlomouc - HoliceCzech Republic

Personalised recommendations