Skip to main content

Advertisement

SpringerLink
Log in

Nutritional status, essential oil changes and water-use efficiency of rose geranium in response to arbuscular mycorrhizal fungi and water deficiency stress

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Stress induced by water deficit is considered to be a global problem and one of the most important factors limiting crop production in arid and semi-arid regions of the world. Application of certain microorganisms, including arbuscular mycorrhizal fungi (AMF), is considered to be an effective and sustainable strategy to mitigate the problem. A pot experiment was conducted in the field (from Feb. to Sep. in 2013–2014 in Isfahan, Iran) to assess the effectiveness of AMF inoculation on changes in biomass, essential oils, nutrient uptake and water-use efficiency of rose geranium (Pelargonium graveolens L.) experiencing stress induced by a deficit of water. The experiment was planned as a factorial experiment, using a completely randomized design, with two factors, including four AMF inoculation (non-mycorrhizal, Rhizophagus intraradices and Funneliformis mosseae inoculated, and the combination of both species) and three irrigation levels including well-watered (WW), moderate water deficiency (MWD) and severe water deficiency (SWD). The results indicated the occurrence of an adverse effect of water deficit on plant total biomass; however, AMF inoculation positively increased plant biomass compared to the non-inoculated ones under three irrigation levels. MWD condition resulted in higher essential oil (EO) content (12.4 %), water-use efficiency (WUE) (29.5 %) and glomalin-related soil proteins (GRSP) (19.1 %) in the plants compared to WW condition. Furthermore, all AMF inoculation improved EO content by at least 12 k%. The results also showed that severe water deficiency adversely affected the uptake of most nutrients by plants especially in non-inoculated plants. The results also revealed that, although EO production was under the control of irrigation regime, nutrient uptake was critically dependent on an association with mycorrhizae. Notwithstanding the fact that rose geranium can tolerate moderate drought stress, the high responsiveness of rose geranium to AMF under water deficiency stress confirms the key role of AMF in facilitating the production of this valuable crop in harsh environments. Dual infection of rose geranium with two AMF species could also synergistically affect biomass, essential oil content and mineral elements absorption.

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

  • Aliasgharzad N, Neyshabouri M, Salimi G (2006) Effects of arbuscular mycorrhizal fungi and Bradyrhizobium japonicum on drought stress of soybean. Biologia 61:324–328

    Article  Google Scholar 

  • Alloway BJ (2009) Soil factors associated with zinc deficiency in crops and humans. Environ Geochem Health 31:537–548

    Article  CAS  PubMed  Google Scholar 

  • Aroca R, del Mar AM, Vernieri P, Ruiz-Lozano JM (2008) Plant responses to drought stress and exogenous ABA application are modulated differently by mycorrhization in tomato and an ABA-deficient mutant (sitiens). Microb Ecol 56:704–719

    Article  CAS  PubMed  Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    Article  CAS  PubMed  Google Scholar 

  • Aslani Z, Hassani A, Rasouli-Sadaghiani M, Esmailpour B, Rohi Z (2014) Effects of arbuscular mycorrhizal (AM) fungi on essential oil content and nutrients uptake in basil under drought stress. J Med Plants By-Products 3:147–153

    Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381

    Article  Google Scholar 

  • Bagheri V, Shamshiri MH, Shirani H, Roosta H (2012) Nutrient uptake and distribution in mycorrhizal pistachio seedlings under drought stress. J Agric Sci Technol 14:1591–1604

    Google Scholar 

  • Bahreininejad B, Razmjoo J, Mirza M (2014) Effect of water stress on productivity and essential oil content and composition of Thymus carmanicus. J Essent Oil Bear Plants 17:717–725

    Article  CAS  Google Scholar 

  • Barman P, Singh SK, Patel VB, Nain L, Pandey A (2015) Cleopatra mandarin (Citrus reshni Hort. Ex tan.) modulate physiological mechanisms to tolerate drought stress due to arbuscular mycorrhizal fungi and mycorrhizal helper bacteria. Afr J Microbiol Res 9:1236–1246

    Article  Google Scholar 

  • Benhiba L, Fouad MO, Essahibi A, Ghoulam C, Qaddoury A (2015) Arbuscular mycorrhizal symbiosis enhanced growth and antioxidant metabolism in date palm subjected to long-term drought. Trees 29:1–9

    Article  Google Scholar 

  • British Pharmacopoeia (1980) H.M.S Office. 2. London.

  • Busse MD, Ellis J (1985) Vesicular-arbuscular mycorrhizal (Glomus fasciculatum) influence on soybean drought tolerance in high phosphorus soil. Can J Bot 63:2290–2294

    Article  Google Scholar 

  • Caravaca F, Alguacil MM, Hernández JA, Roldán A (2005) Involvement of antioxidant enzyme and nitrate reductase activities during water stress and recovery of mycorrhizal Myrtus communis and Phillyrea angustifolia plants. Plant Sci 169:191–197

    Article  CAS  Google Scholar 

  • Chapman HD, Pratt PF (1962) Methods of analysis for soils, plants and waters. Soil Sci 93:68

    Article  Google Scholar 

  • Diaz-Lopez L, Gimeno V, Simón I, Martínez V, Rodríguez-Ortega WM, García-Sánchez F (2012) Jatropha curcas Seedlings show a water conservation strategy under drought conditions based on decreasing leaf growth and stomatal conductance. Agric Water Manag 105:48–56

    Article  Google Scholar 

  • Eiasu BK, Steyn JM, Soundy P (2012) Physiomorphological response of rose-scented geranium (Pelargonium spp.) to irrigation frequency. South African J Bot 78:96–103

    Article  Google Scholar 

  • Entry JA, Rygiewicz PT, Watrud LS, Donnelly PK (2002) Influence of adverse soil conditions on the formation and function of arbuscular mycorrhizas. Adv Environ Res 7:123–138

    Article  CAS  Google Scholar 

  • Fereres E, Soriano MA (2007) Deficit irrigation for reducing agricultural water use. J Exp Bot 58:147–159

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Kuyper TW, Zou C, Zhang F, Hoffland E (2007) Mycorrhizal responsiveness of aerobic rice genotypes is negatively correlated with their zinc uptake when nonmycorrhizal. Plant Soil 290:283–291

    Article  CAS  Google Scholar 

  • George E (2000) Nutrient uptake. In: Kapulnick Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic Publishers, Netherlands, pp. 307–343

    Chapter  Google Scholar 

  • Gericke S, Kurmies B (1952) Die kolorimetrische Phosphorsäurebestimmung mit Ammonium-Vanadat-Molybdat und ihre Anwendung in der Pflanzenanalyse. Z Düngg Pflanzenernähr Bodenk 59:235–247

    CAS  Google Scholar 

  • Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A (2013) Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 117:106–114

    Article  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Graham JH, Syvertsen JP (1984) Influence of vesicular–arbuscular mycorrhiza on the hydraulic conductivity of roots of two citrus rootstocks. New Phytol 97:277–284

    Article  Google Scholar 

  • Green H, Larsen J, Olsson PA, Jensen DF, Jakobsen I (1999) Suppression of the biocontrol agent Trichoderma harzianum by mycelium of the arbuscular mycorrhizal fungus Glomus intraradices in root-free soil. Appl Environ Microbiol 65:1428–1434

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hijikata N, Murase M, Tani C, Ohtomo R, Osaki M, Ezawa T (2010) Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytol 186:285–289

    Article  CAS  PubMed  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299

    Article  CAS  PubMed  Google Scholar 

  • Jaleel CA, Gopi R, Sankar B, Gomathinayagam M, Panneerselvam R (2008) Differential responses in water use efficiency in two varieties of Catharanthus roseus under drought stress. C R Biol 331:42–47

    Article  PubMed  Google Scholar 

  • 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 129:329–334

    Article  CAS  Google Scholar 

  • Khalil SE, El-Noemani ASA (2015) Effect of bio-fertilizers on growth, yield, water relations, photosynthetic pigments and carbohydrates contents of Origanum vulgare L. Plants grown under water stress conditions. Am J Sustain Agric 9:60–73

    Google Scholar 

  • Koide RT, Peoples MS (2013) Behavior of Bradford-reactive substances is consistent with predictions for glomalin. Appl Soil Ecol 63:8–14

    Article  Google Scholar 

  • Li H, Xiang D, Wang C, Li X, Lou Y (2012) Effects of epigeic earthworm (Eisenia fetida) and arbuscular mycorrhizal fungus (Glomus intraradices) on enzyme activities of a sterilized soil–sand mixture and nutrient uptake by maize. Biol Fertil Soils 48:879–887

    Article  CAS  Google Scholar 

  • Manoharan PT, Shanmugaiah V, Balasubramanian N, Gomathinayagam S, Sharma MP, Muthuchelian K (2010) Influence of AM fungi on the growth and physiological status of Erythrina variegata Linn. Grown under different water stress conditions. Eur J Soil Biol 46:151–156

    Article  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    Article  CAS  Google Scholar 

  • Meng JJ, He XL (2011) Effects of AM fungi on growth and nutritional contents of Salvia miltiorrhiza Bge. Under drought stress. J Agr Univ Hebei 34:51–61

    CAS  Google Scholar 

  • Nichols KA, Wright SF (2004) Contributions of fungi to soil organic matter in agroecosystems. In: Magdoff F, Weil RR (eds) Soil organic matter in sustainable agriculture. CRC, Florida, pp. 179–198

    Google Scholar 

  • Nouraei S, Rahimmalek M, Saeidi G, Bahreininejad B (2016) Variation in seed oil content and fatty acid composition of globe artichoke under different irrigation regimes. J Am Oil Chem Soc 93:953–962

    Article  CAS  Google Scholar 

  • Novozamsky I, Eck R van, Van Schouwenburg JC, Walinga I (1974) Total nitrogen determination in plant material by means of the indophenol-blue method. Neth J Agric Sci 22:3–5.

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–IN18

    Article  Google Scholar 

  • Purin S, Rillig MC (2007) The arbuscular mycorrhizal fungal protein glomalin: limitations, progress, and a new hypothesis for its function. Pedobiologia 51:123–130

    Article  CAS  Google Scholar 

  • Raiesi F, Ghollarata M (2006) Interactions between phosphorus availability and an AM fungus (Glomus intraradices) and their effects on soil microbial respiration, biomass and enzyme activities in a calcareous soil. Pedobiologia 50:413–425

    Article  CAS  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Article  CAS  PubMed  Google Scholar 

  • Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, De Pascale S, Bonini P, Colla G (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hortic 30(196):91–108

    Article  Google Scholar 

  • Rydlová J, Jelínková M, Dušek K, Dušková E, Vosátka M, Püschel D (2015) Arbuscular mycorrhiza differentially affects synthesis of essential oils in coriander and dill. Mycorrhiza 26:123–131

    Article  PubMed  Google Scholar 

  • Saia S, Amato G, Frenda AS, Giambalvo D, Ruisi P (2014) Influence of arbuscular mycorrhizae on biomass production and nitrogen fixation of berseem clover plants subjected to water stress. PLoS One 9:e90738

    Article  PubMed  PubMed Central  Google Scholar 

  • Sbrana C, Avio L, Giovannetti M (2014) Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35:1535–1546

    Article  CAS  PubMed  Google Scholar 

  • Schaff BE, Skogley EO (1982) Diffusion of potassium, calcium, and magnesium in Bozeman silt loam as influenced by temperature and moisture. Soil Sci Soc Am J 46:521–524

    Article  CAS  Google Scholar 

  • Singh M, Singh UB, Ram M, Yadav A, Chanotiya CS (2013) Biomass yield, essential oil yield and quality of geranium (Pelargonium graveolens L. Her.) as influenced by intercropping with garlic (Allium sativum L.) under subtropical and temperate climate of India. Ind Crop Prod 46:234–237

    Article  CAS  Google Scholar 

  • Srivastava NK, Misra A, Sharma S (1997) Effect of Zn deficiency on net photosynthetic rate, 14C partitioning, and oil accumulation in leaves of peppermint. Photosynthetica 33:71–79

    Article  CAS  Google Scholar 

  • Subramanian KS, Santhanakrishnan P, Balasubramanian P (2006) Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci Hortic 107:245–253

    Article  Google Scholar 

  • Tian Y, Lei Y, Zheng Y, Cai Z (2013) Synergistic effect of colonization with arbuscular mycorrhizal fungi improves growth and drought tolerance of Plukenetia volubilis seedlings. Acta Physiol Plant 35:687–696

    Article  CAS  Google Scholar 

  • Wang S, Srivastava AK, Wu QS, Fokom R (2014) The effect of mycorrhizal inoculation on the rhizosphere properties of trifoliate orange (Poncirus trifoliata L. Raf.). Sci Hortic 170:137–142

    Article  Google Scholar 

  • Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107

    Article  CAS  Google Scholar 

  • Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425

    Article  CAS  PubMed  Google Scholar 

  • Wu QS, Xia RX, Zou YN (2008) Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress. Eur J Soil Biol 44:122–128

    Article  Google Scholar 

  • Wu F, Dong M, Liu Y, Ma X, An L, Young JP, Feng H (2011) Effects of long-term fertilization on AM fungal community structure and glomalin-related soil protein in the loess plateau of China. Plant Soil 342:233–247

    Article  CAS  Google Scholar 

  • Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87

    Article  CAS  Google Scholar 

  • Zarea MJ, Ghalavand A, Goltapeh EM, Rejali F, Zamaniyan M (2009) Effects of mixed cropping, earthworms (Pheretima sp.), and arbuscular mycorrhizal fungi (Glomus mosseae) on plant yield, mycorrhizal colonization rate, soil microbial biomass, and nitrogenase activity of free-living rhizosphere bacteria. Pedobiologia 52:223–235

    Article  CAS  Google Scholar 

  • 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 23:253–265

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Yao Q, Li J, Hu Y, Chen J (2014) Growth response and nutrient uptake of Eriobotrya japonica plants inoculated with three isolates of arbuscular mycorrhizal fungi under water stress condition. J Plant Nutr 37:690–703

    Article  CAS  Google Scholar 

  • Zhao R, Guo W, Bi N, Guo J, Wang L, Zhao J, Zhang J (2015) Arbuscular mycorrhizal fungi affect the growth, nutrient uptake and water status of maize (Zea mays L.) grown in two types of coal mine spoils under drought stress. Appl Soil Ecol 88:41–49

    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 

  • Zou YN, Srivastava AK, Wu QS, Huang YM (2014) Glomalin-related soil protein and water relations in mycorrhizal citrus (Citrus tangerina) during soil water deficit. Arch Agron Soil Sci 60:1103–1114

    Article  CAS  Google Scholar 

  • Zubek S, Rola K, Szewczyk A, Majewska ML, Turnau K (2015) Enhanced concentrations of elements and secondary metabolites in Viola tricolor L. Induced by arbuscular mycorrhizal fungi. Plant Soil 390:129–142

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge financial support from the Barij Essence Company (Kashan, Iran).

Author contributions

Rasekh Amiri: Conducting the experiment, analyzing the data and working on the manuscript draft. Ali Nikbakht: Leading the project, planning the experiment, providing the equipment for the experiment, working on the manuscript draft and finishing the final version. Nematollah Etemadi and Mohammad Reza Sabzalian: Assisting with the lab works and editing the final version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Horticulture, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran

    Rasekh Amiri, Ali Nikbakht & Nematollah Etemadi

  2. Department of Agronomy and Plant Breeding, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran

    Mohammad Reza Sabzalian

Authors
  1. Rasekh Amiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ali Nikbakht
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nematollah Etemadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohammad Reza Sabzalian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Rasekh Amiri or Ali Nikbakht.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amiri, R., Nikbakht, A., Etemadi, N. et al. Nutritional status, essential oil changes and water-use efficiency of rose geranium in response to arbuscular mycorrhizal fungi and water deficiency stress. Symbiosis 73, 15–25 (2017). https://doi.org/10.1007/s13199-016-0466-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-016-0466-z

Keywords

Search

Navigation