Skip to main content

Advertisement

SpringerLink
Log in

Arbuscular mycorrhizal symbiosis alleviates drought stress imposed on Knautia arvensis plants in serpentine soil

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and Aims

Plants growing on serpentine bedrock have to cope with the unique soil chemistry and often also low water-holding capacity. As plant-soil interactions are substantially modified by arbuscular mycorrhizal (AM) symbiosis, we hypothesise that drought tolerance of serpentine plants is enhanced by AM fungi (AMF).

Methods

We conducted a pot experiment combining four levels of drought stress and three AMF inoculation treatments, using serpentine Knautia arvensis (Dipsacaceae) plants as a model.

Results

AMF inoculation improved plant growth and increased phosphorus uptake. The diminishing water supply caused a gradual decrease in plant growth, accompanied by increasing concentrations of drought stress markers (proline, abscisic acid) in root tissues. Mycorrhizal growth dependence and phosphorus uptake benefit increased with drought intensity, and the alleviating effect of AMF on plant drought stress was also indicated by lower proline accumulation.

Conclusions

We documented the role of AM symbiosis in plant drought tolerance under serpentine conditions. However, the potential of AMF to alleviate drought stress was limited beyond a certain threshold, as indicated by a steep decline in mycorrhizal growth dependence and phosphorus uptake benefit and a concomitant rise in proline concentrations in the roots of mycorrhizal plants at the highest drought intensity.

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
Fig. 4

Similar content being viewed by others

References

  • Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269

    Article  PubMed  Google Scholar 

  • Anacker B, Rajakaruna N, Ackerly D, Harrison S, Keeley J, Vasey M (2011) Ecological strategies in California chaparral: interacting effects of soils, climate, and fire on specific leaf area. Plant Ecol Divers 4:179–188

    Article  Google Scholar 

  • Aroca R, Bago A, Sutka M, Paz JA, Cano C, Amodeo G, Ruiz-Lozano JM (2009) Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and nonstressed mycelium. Mol Plant Microbe Interact 22:1169–1178

    Article  PubMed  CAS  Google Scholar 

  • Asch F (2000) Determination of abscisic acid by indirect enzyme linked immuno sorbent assay (ELISA). Technical report. Laboratory for Agrohydrology and Bioclimatology, Department of Agricultural Sciences, The Royal Veterinary and Agricultural University, Taastrup

    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 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bolandnazar S, Aliasgarzad N, Neishabury MR, Chaparzadeh N (2007) Mycorrhizal colonization improves onion (Allium cepa L.) yield and water use efficiency under water deficit condition. Sci Hortic 114:11–15

    Article  Google Scholar 

  • Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol S 36:243–266

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Coleman R, Jove C (1992) Geological origin of serpentinites. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept Ltd, Andover, pp 1–18

  • Danneberg G, Latus Z, Zimmer W, Hundeshagen B, Schneiderpoetsch H, Bothe H (1993) Influence of vesicular-arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L.). J Plant Physiol 141:33–39

    Article  CAS  Google Scholar 

  • Davies FT, Olalde-Portugal V, Aguilera-Gomez L, Alvarado MJ, Ferrera-Cerrato RC, Boutton TW (2002) Alleviation of drought stress of Chile ancho pepper (Capsicum annuum L. cv. San Luis) with arbuscular mycorrhiza indigenous to Mexico. Sci Hortic 92:347–359

    Article  Google Scholar 

  • Davoodian N, Bosworth J, Rajakaruna N (2012) Mycorrhizal colonization of Hypericum perforatum L. (Hypericaceae) from serpentine and granite outcrops on the Deer Isles, Maine. Northeast Nat 19:517–526

    Article  Google Scholar 

  • Doubková P, Suda J, Sudová R (2011) Arbuscular mycorrhizal symbiosis on serpentine soils: the effect of native fungal communities on different Knautia arvensis ecotypes. Plant Soil 345:325–338

    Article  Google Scholar 

  • Doubková P, Suda J, Sudová R (2012) The symbiosis with arbuscular mycorrhizal fungi contributes to plant tolerance to serpentine edaphic stress. Soil Biol Biochem 44:56–64

    Article  Google Scholar 

  • Duan XG, Neuman DS, Reiber JM, Green CD, Saxton AM, Augé RM (1996) Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J Exp Bot 47:1541–1550

    Article  CAS  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 

  • Fan QJ, Liu JH (2011) Colonization with arbuscular mycorrhizal fungus affects growth, drought tolerance and expression of stress-responsive genes in Poncirus trifoliata. Acta Physiol Plant 33:1533–1542

    Article  Google Scholar 

  • Fitzsimons MS, Miller RM (2010) Serpentine soil has little influence on the root-associated microbial community composition of the serpentine tolerant grass species Avenula sulcata. Plant Soil 330:393–405

    Article  CAS  Google Scholar 

  • Gerdemann JW, Nicolson TH (1962) Endogone spores in cultivated soils. Nature 195:308–309

    Article  Google Scholar 

  • Goicoechea N, Antolín MC, Sánchez-Díaz M (1997) Gas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfalfa subjected to drought. Physiol Plantarum 100:989–997

    Article  CAS  Google Scholar 

  • Huang Z, Zou ZR, He CX, He ZQ, Zhang ZB, Li JM (2011) Physiological and photosynthetic responses of melon (Cucumis melo L.) seedlings to three Glomus species under water deficit. Plant Soil 339:391–399

    Article  CAS  Google Scholar 

  • Hughes R, Bachmann K, Smirnoff N, Macnair MR (2001) The role of drought tolerance in serpentine tolerance in the Mimulus guttatus Fischer ex DC. complex. S Afr J Sci 97:581–586

    Google Scholar 

  • Jansa J, Smith FA, Smith FE (2008) Are there benefits of simultaneous colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789

    Article  PubMed  CAS  Google Scholar 

  • Ji BM, Bentivenga SP, Casper BB (2010) Evidence for ecological matching of whole AM fungal communities to the local plant-soil environment. Ecology 91:3037–3046

    Article  PubMed  Google Scholar 

  • Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    Article  PubMed  CAS  Google Scholar 

  • Kishor PKB, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    CAS  Google Scholar 

  • Kolář F, Štech M, Trávníček P, Rauchová J, Urfus T, Vít P, Kubešová M, Suda J (2009) Towards resolving the Knautia arvensis agg. (Dipsacaceae) puzzle: primary and secondary contact zones and ploidy segregation at landscape and microgeographic scales. Ann Bot-London 103:963–974

    Article  Google Scholar 

  • Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA-mycorrhizas. Mycol Res 92:486–505

    Article  Google Scholar 

  • Krüger M, Stockinger H, Krüger C, Schüssler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223

    Article  PubMed  Google Scholar 

  • Lagrange A, Ducousso M, Jourand P, Majorel C, Amir H (2011) New insights into the mycorrhizal status of Cyperaceae from ultramafic soils in New Caledonia. Can J Microbiol 57:21–28

    Article  PubMed  CAS  Google Scholar 

  • Lee BR, Muneer S, Avice JC, Jung WJ, Kim TH (2012) Mycorrhizal colonisation and P-supplement effects on N uptake and N assimilation in perennial ryegrass under well-watered and drought-stressed conditions. Mycorrhiza 22:525–534

    Google Scholar 

  • Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD (2012) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197:617–630

    Google Scholar 

  • Ludwig-Müller J (2010) Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: Physiology and function. Springer, pp. 169–190

  • 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 

  • Marulanda A, Azcón R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plantarum 119:526–533

    Article  CAS  Google Scholar 

  • Marulanda A, Porcel R, Barea JM, Azcón R (2007) Drought tolerance and antioxidant activities in lavender plants colonized by native drought-tolerant or drought-sensitive Glomus species. Microb Ecol 54:543–552

    Article  PubMed  CAS  Google Scholar 

  • O’Dell R, Rajakaruna N (2011) Intraspecific variation, adaptation, and evolution. In: Harrison S, Rajakaruna N (eds) Serpentine: Evolution and ecology in a model system. UC Press, California, pp 97–137

    Google Scholar 

  • Rajakaruna N, Bradfield GE, Bohm BA, Whitton J (2003) Adaptive differentiation in response to water stress by edaphic races of Lasthenia californica (Asteraceae). Int J Plant Sci 164:371–376

    Article  Google Scholar 

  • Römheld V, Kirkby EA (2010) Research on potassium in agriculture: needs and prospects. Plant Soil 335:155–180

    Article  Google Scholar 

  • Ruiz-Lozano JM, Azcón R, Gómez M (1995) Effects of arbuscular-mycorrhizal Glomus species on drought tolerance: Physiological and nutritional plant responses. Appl Environ Microb 61:456–460

    CAS  Google Scholar 

  • Sambatti JBM, Rice KJ (2007) Functional ecology of ecotypic differentiation in the Californian serpentine sunflower (Helianthus exilis). New Phytol 175:107–119

    Article  PubMed  CAS  Google Scholar 

  • Sauter A, Davies WJ, Hartung W (2001) The long-distance abscisic acid signal in the droughted plant: the fate of the hormone on its way from root to shoot. J Exp Bot 52:1991–1997

    Article  PubMed  CAS  Google Scholar 

  • Schreiner RP, Bethlenfalvay GJ (1997) Plant and soil response to single and mixed species of arbuscular mycorrhizal fungi under fungicide stress. Appl Soil Ecol 7:93–102

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Academic, Cambridge

    Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20

    Article  CAS  Google Scholar 

  • Štěpánek J (1997) Knautia L. – chrastavec. In: Slavík B (ed) Květena České republiky 6 [Flora of the Czech Republic 6]. Academia, Prague, pp 543–554

    Google Scholar 

  • Subramanian KS, Charest C (1999) Acquisition of N by external hyphae of an arbuscular mycorrhizal fungus and its impact on physiological responses in maize under drought-stressed and well-watered conditions. Mycorrhiza 9:69–75

    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 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Paris, Dijon, pp 217–221

    Google Scholar 

  • Wu QS, Xia RX, Zou YN, Wang GY (2007a) Osmotic solute responses of mycorrhizal citrus (Poncirus trifoliata) seedlings to drought stress. Acta Physiol Plant 29:543–549

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN, Xia RX, Wang MY (2007b) Five Glomus species affect water relations of Citrus tangerine during drought stress. Bot Stud 48:147–154

    Google Scholar 

  • Wu CA, Lowry DB, Nutter LI, Willis JH (2010) Natural variation for drought-response traits in the Mimulus guttatus species complex. Oecologia 162:23–33

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The financial support of the Grant Agency of the Academy of Sciences of the Czech Republic (project KJB600050812) and the Grant Agency of Charles University in Prague (project 271011) is gratefully acknowledged. Additionally, this study was also supported by a long-term research development project no. RVO 67985939 (Academy of Sciences of the Czech Republic), by Charles University in Prague (project SVV 265203/2012), and by the Ministry of Agriculture of the Czech Republic (0002700604). The authors would also like to thank M. Albrechtová and her team at the Analytical laboratory of the Institute of Botany AS CR for their chemical analyses of plant biomass and soils, as well as T. Hájek (Institute of Botany AS CR, Třeboň) for the provision of and advice regarding the LI-COR, portable photosynthesis system. Thanks are also due to Prof. F. Asch and his team from the Institute for Plant Production and Agroecology in the Tropics and Subtropics at University of Hohenheim for providing the conjugate for ABA analysis. The advices of Z. Sýkorová and P. Kohout on AMF molecular determination, the support of members of the DNA laboratory of the Institute of Botany AS CR as well as the valuable comments of the editor and reviewers of the previous version of the manuscript are greatly appreciated.

Author information

Authors and Affiliations

  1. Institute of Botany, Academy of Sciences of the Czech Republic, CZ-252 43, Průhonice, Czech Republic

    Pavla Doubková & Radka Sudová

  2. Department of Experimental Plant Biology, Faculty of Science, Charles University in Prague, CZ-128 44, Prague 2, Czech Republic

    Pavla Doubková

  3. Crop Research Institute, CZ-161 06, Prague 6, Czech Republic

    Eva Vlasáková

Authors
  1. Pavla Doubková
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eva Vlasáková
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Radka Sudová
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pavla Doubková.

Additional information

Responsible Editor: Tatsuhiro Ezawa.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 480 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Doubková, P., Vlasáková, E. & Sudová, R. Arbuscular mycorrhizal symbiosis alleviates drought stress imposed on Knautia arvensis plants in serpentine soil. Plant Soil 370, 149–161 (2013). https://doi.org/10.1007/s11104-013-1610-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1610-7

Keywords

Search

Navigation