Skip to main content

Advertisement

Log in

Arbuscular mycorrhizal symbiosis on serpentine soils: the effect of native fungal communities on different Knautia arvensis ecotypes

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

Abstract

Serpentine soils represent a unique environment that imposes multiple stresses on vegetation (low Ca/Mg ratios, macronutrient deficiencies, elevated heavy metal concentrations and drought). Under these conditions, a substantial role of arbuscular mycorrhizal (AM) symbiosis can be anticipated due to its importance for plant nutrition and stress alleviation. We tested whether serpentine and non-serpentine populations of Knautia arvensis (Dipsacaceae) differ in the benefits derived from native AM fungal communities. Four serpentine and four non-serpentine populations were characterised in terms of mycorrhizal colonisation and soil characteristics. The serpentine populations showed significantly lower mycorrhizal colonisation than their non-serpentine counterparts. The mycorrhizal colonisation positively correlated with soil pH, Ca and K concentrations and Ca/Mg ratio. Seedlings from each population were then grown for 3 months in their sterilised native substrates, either uninoculated or reinoculated with native AM fungi. Two serpentine and two non-serpentine populations responded positively to mycorrhizal inoculation, while no significant change in plant growth was observed in the remaining populations. Contrary to our hypothesis, serpentine populations of K. arvensis did not show higher mycorrhizal growth dependence than non-serpentine populations when grown in their native soils and inoculated with native AM fungi.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AM:

Arbuscular mycorrhiza, arbuscular mycorrhizal

CEC:

Cation exchange capacity

DMF:

Dimethylformamide

DW:

Dry weight

MGD:

Mycorrhizal growth dependence

NS:

Non-serpentine

PCA:

Principal component analysis

S:

Serpentine

SEM:

Standard error of the mean

References

  • Abbott LK, Robson AD (1985) The effect of soil pH on the formation of VA mycorrhizas by 2 species of Glomus. Aust J Soil Res 23:253–261

    Article  Google Scholar 

  • Allsopp N, Stock WD (1993) Mycorrhizas and seedling growth of slow-growing sclerophylls from nutrient-poor environments. Acta Oecol 14:577–587

    Google Scholar 

  • Amir H, Perrier N, Rigault F, Jaffre T (2007) Relationships between Ni-hyperaccumulation and mycorrhizal status of different endemic plant species from New Caledonian ultramafic soils. Plant Soil 293:23–35

    Article  CAS  Google Scholar 

  • Amir H, Jasper DA, Abbott LK (2008) Tolerance and induction of tolerance to Ni of arbuscular mycorrhizal fungi from New Caledonian ultramafic soils. Mycorrhiza 19:1–6

    Article  PubMed  CAS  Google Scholar 

  • Azcón R, Barea JM (1992) The effect of vesicular-arbuscular mycorrhizae in decreasing Ca acquisition by alfalfa plants in calcareous soils. Biol Fertil Soils 13:155–159

    Google Scholar 

  • Boulet FM, Lambers H (2005) Characterisation of arbuscular mycorrhizal fungi colonisation in cluster roots of Hakea verrucosa F. Muell (Proteaceae), and its effect on growth and nutrient acquisition in ultramafic soil. Plant Soil 269:357–367

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Castelli JP, Casper BB (2003) Intraspecific AM fungal variation contributes to plant-fungal feedback in a serpentine grassland. Ecology 84:323–336

    Article  Google Scholar 

  • Chiarucci A, Maccherini S, Bonini I, De Dominicis V (1999) Effects of nutrient addition on community productivity and structure of serpentine vegetation. Plant Biol 1:121–126

    Article  CAS  Google Scholar 

  • Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902

    Article  CAS  Google Scholar 

  • Doherty JH, Ji BM, Casper BB (2008) Testing nickel tolerance of Sorghastrum nutans and its associated soil microbial community from serpentine and prairie soils. Environ Pollut 151:593–598

    Article  PubMed  CAS  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 

  • Goncalves SC, Martins-Loucao MA, Freitas H (2001) Arbuscular mycorrhizas of Festuca brigantina, an endemic serpentinophyte from Portugal. S Afr J Sci 97:571–572

    CAS  Google Scholar 

  • Gustafson DJ, Casper BB (2004) Nutrient addition affects AM fungal performance and expression of plant/fungal feedback in three serpentine grasses. Plant Soil 259:9–17

    Article  CAS  Google Scholar 

  • Hepper CM, Oshea J (1984) Vesicular-arbuscular mycorrhizal infection in lettuce (Lactuca sativa) in relation to calcium supply. Plant Soil 82:61–68

    Article  CAS  Google Scholar 

  • Hetrick BAD (1991) Mycorrhizas and root architecture. Experientia 47:355–362

    Article  Google Scholar 

  • Hopkins NA (1987) Mycorrhizae in a California serpentine grassland community. Can J Bot 65:484–487

    Article  Google Scholar 

  • Jarstfer AG, Farmer-Koppenol P, Sylvia DM (1998) Tissue magnesium and calcium affect arbuscular mycorrhiza development and fungal reproduction. Mycorrhiza 7:237–242

    Article  CAS  Google Scholar 

  • Jenny H (1980) The soil resource: origin and behavior. Springer, New York

    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 

  • Johnston WR, Proctor J (1981) Growth of serpentine and non-serpentine races of Festuca rubra in solutions simulating the chemical conditions in a toxic serpentine soil. J Ecol 69:855–869

    Article  CAS  Google Scholar 

  • Jun DJ, Allen EB (1991) Physiological responses of 6 wheatgrass cultivars to mycorrhizae. J Range Manag 44:336–341

    Article  Google Scholar 

  • Kaplan Z (1998) Relict serpentine populations of Knautia arvensis s.l. (Dipsacaceae) in the Czech Republic and an adjacent area of Germany. Preslia 70:21–31

    Google Scholar 

  • Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508

    PubMed  CAS  Google Scholar 

  • Koide RT, Mooney HA (1987) Spatial variation in inoculum potential of vesicular arbuscular mycorrhizal fungi caused by formation of gopher mounds. New Phytol 107:173–182

    Article  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 103:963–974

    Article  PubMed  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 

  • Kothari SK, Marschner H, Romheld V (1990) Direct and indirect effects of VA mycorrhizal fungi and rhizosphere microorganisms on acquisition of mineral nutrients by maize (Zea mays L.) in a calcareous soil. New Phytol 116:637–645

    Article  CAS  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 

  • Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153

    Article  CAS  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  • Liu A, Hamel C, Hamilton RI, Smith DL (2000) Mycorrhizae formation and nutrient uptake of new corn (Zea mays L.) hybrids with extreme canopy and leaf architecture as influenced by soil N and P levels. Plant Soil 221:157–166

    Article  CAS  Google Scholar 

  • Liu A, Hamel C, Elmi A, Costa C, Ma B, Smith DL (2002) Concentrations of K, Ca and Mg in maize colonized by arbuscular mycorrhizal fungi under field conditions. Can J Soil Sci 82:271–278

    Article  CAS  Google Scholar 

  • Malcová R, Gryndler M, Vosátka M (2002) Magnesium ions alleviate the negative effect of manganese on Glomus claroideum BEG23. Mycorrhiza 12:125–129

    Article  PubMed  Google Scholar 

  • Marschner H (2002) Mineral nutrition in higher plants. Academic, London

    Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonisation of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • O'Dell RE, James JJ, Richards JH (2006) Congeneric serpentine and nonserpentine shrubs differ more in leaf Ca:Mg than in tolerance of low N, low P, or heavy metals. Plant Soil 280:49–64

    Article  Google Scholar 

  • Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. 2. Chemical and microbiological properties, 2nd edn. American Society of Agronomy, Madison, pp 403–430

    Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochem Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Proctor J (1971) Plant ecology of serpentine. II. Plant response to serpentine soils. J Ecol 59:397–410

    Article  Google Scholar 

  • Proctor J, Woodell SRJ (1975) The ecology of serpentine soils. Adv Ecol Res 9:255–365

    Article  Google Scholar 

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

    Article  PubMed  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 

  • Schechter SP, Bruns TD (2008) Serpentine and non-serpentine ecotypes of Collinsia sparsiflora associate with distinct arbuscular mycorrhizal fungal assemblages. Mol Ecol 17:3198–3210

    Article  PubMed  CAS  Google Scholar 

  • Schüssler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London

    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 

  • Sudová R, Rydlová J, Münzbergová Z, Suda J (2010) Ploidy-specific interactions of three host plants with arbuscular mycorrhizal fungi: Does genome copy number matter? Am J Bot 97:1798–1807

    Article  PubMed  Google Scholar 

  • Turnau K, Mesjasz-Przybylowicz J (2003) Arbuscular mycorrhiza of Berkheya coddii and other Ni-hyperaccumulating members of Asteraceae from ultramafic soils in South Africa. Mycorrhiza 13:185–190

    Article  PubMed  Google Scholar 

  • van Aarle IM, Olsson PA, Söderström B (2002) Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytol 155:173–182

    Article  Google Scholar 

  • Vivas A, Biró B, Németh T, Barea JM, Azcón R (2006) Nickel-tolerant Brevibacillus brevis and arbuscular mycorrhizal fungus can reduce metal acquisition and nickel toxicity effects in plant growing in nickel supplemented soil. Soil Biol Biochem 38:2694–2704

    Article  CAS  Google Scholar 

  • Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363

    Article  PubMed  CAS  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and chlorophyll b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    CAS  Google Scholar 

Download references

Acknowledgements

Financial support of the Grant Agency of the Academy of Sciences of the Czech Republic (project KJB600050812 to R.S.) and the Grant Agency of Charles University (project 13409 to P.D.) is gratefully acknowledged. Additional support was provided by the Academy of Sciences of the Czech Republic within the institutional research programme (AV0Z 60050516) and by the Ministry of Education, Youth and Sports of the Czech Republic (project MSM0021620828). The authors are grateful to M. Albrechtová and her team from the Analytical Laboratory of the Institute of Botany AS CR for the chemical analyses of plant biomass and soils. Sincere thanks are due to F. Kolář and M. Štech for providing information on K. arvensis localities and to P. Trávníček and Z. Sýkorová for their kind advice on the ordination analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Radka Sudová.

Additional information

Responsible Editor: Erik J. Joner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Doubková, P., Suda, J. & Sudová, R. Arbuscular mycorrhizal symbiosis on serpentine soils: the effect of native fungal communities on different Knautia arvensis ecotypes. Plant Soil 345, 325–338 (2011). https://doi.org/10.1007/s11104-011-0785-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-011-0785-z

Keywords

Navigation