Advertisement

Plant and Soil

, Volume 345, Issue 1–2, pp 325–338 | Cite as

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

  • Pavla Doubková
  • Jan Suda
  • Radka Sudová
Regular Article

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.

Keywords

Arbuscular mycorrhizal fungi Ca/Mg ratio Edaphic stress Nickel Mycorrhizal colonisation Ploidy level Serpentine 

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

Notes

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.

References

  1. 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 23:253–261CrossRefGoogle Scholar
  2. Allsopp N, Stock WD (1993) Mycorrhizas and seedling growth of slow-growing sclerophylls from nutrient-poor environments. Acta Oecol 14:577–587Google Scholar
  3. 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 293:23–35CrossRefGoogle Scholar
  4. Amir H, Jasper DA, Abbott LK (2008) Tolerance and induction of tolerance to Ni of arbuscular mycorrhizal fungi from New Caledonian ultramafic soils. Mycorrhiza 19:1–6PubMedCrossRefGoogle Scholar
  5. Azcón R, Barea JM (1992) The effect of vesicular-arbuscular mycorrhizae in decreasing Ca acquisition by alfalfa plants in calcareous soils. Biol Fertil Soils 13:155–159Google Scholar
  6. 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 269:357–367CrossRefGoogle Scholar
  7. Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266CrossRefGoogle Scholar
  8. Castelli JP, Casper BB (2003) Intraspecific AM fungal variation contributes to plant-fungal feedback in a serpentine grassland. Ecology 84:323–336CrossRefGoogle Scholar
  9. Chiarucci A, Maccherini S, Bonini I, De Dominicis V (1999) Effects of nutrient addition on community productivity and structure of serpentine vegetation. Plant Biol 1:121–126CrossRefGoogle Scholar
  10. Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902CrossRefGoogle Scholar
  11. 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 151:593–598PubMedCrossRefGoogle Scholar
  12. 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 330:393–405CrossRefGoogle Scholar
  13. Goncalves SC, Martins-Loucao MA, Freitas H (2001) Arbuscular mycorrhizas of Festuca brigantina, an endemic serpentinophyte from Portugal. S Afr J Sci 97:571–572Google Scholar
  14. Gustafson DJ, Casper BB (2004) Nutrient addition affects AM fungal performance and expression of plant/fungal feedback in three serpentine grasses. Plant Soil 259:9–17CrossRefGoogle Scholar
  15. Hepper CM, Oshea J (1984) Vesicular-arbuscular mycorrhizal infection in lettuce (Lactuca sativa) in relation to calcium supply. Plant Soil 82:61–68CrossRefGoogle Scholar
  16. Hetrick BAD (1991) Mycorrhizas and root architecture. Experientia 47:355–362CrossRefGoogle Scholar
  17. Hopkins NA (1987) Mycorrhizae in a California serpentine grassland community. Can J Bot 65:484–487CrossRefGoogle Scholar
  18. Jarstfer AG, Farmer-Koppenol P, Sylvia DM (1998) Tissue magnesium and calcium affect arbuscular mycorrhiza development and fungal reproduction. Mycorrhiza 7:237–242CrossRefGoogle Scholar
  19. Jenny H (1980) The soil resource: origin and behavior. Springer, New YorkGoogle Scholar
  20. Ji BM, Bentivenga SP, Casper BB (2010) Evidence for ecological matching of whole AM fungal communities to the local plant-soil environment. Ecology 91:3037–3046PubMedCrossRefGoogle Scholar
  21. 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 69:855–869CrossRefGoogle Scholar
  22. Jun DJ, Allen EB (1991) Physiological responses of 6 wheatgrass cultivars to mycorrhizae. J Range Manag 44:336–341CrossRefGoogle Scholar
  23. Kaplan Z (1998) Relict serpentine populations of Knautia arvensis s.l. (Dipsacaceae) in the Czech Republic and an adjacent area of Germany. Preslia 70:21–31Google Scholar
  24. 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 83:495–508PubMedGoogle Scholar
  25. Koide RT, Mooney HA (1987) Spatial variation in inoculum potential of vesicular arbuscular mycorrhizal fungi caused by formation of gopher mounds. New Phytol 107:173–182CrossRefGoogle Scholar
  26. 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 103:963–974PubMedCrossRefGoogle Scholar
  27. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505CrossRefGoogle Scholar
  28. 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 116:637–645CrossRefGoogle Scholar
  29. 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 57:21–28PubMedCrossRefGoogle Scholar
  30. Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153CrossRefGoogle Scholar
  31. Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428CrossRefGoogle Scholar
  32. 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 221:157–166CrossRefGoogle Scholar
  33. 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 82:271–278CrossRefGoogle Scholar
  34. Malcová R, Gryndler M, Vosátka M (2002) Magnesium ions alleviate the negative effect of manganese on Glomus claroideum BEG23. Mycorrhiza 12:125–129PubMedCrossRefGoogle Scholar
  35. Marschner H (2002) Mineral nutrition in higher plants. Academic, LondonGoogle Scholar
  36. 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 115:495–501CrossRefGoogle Scholar
  37. 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 280:49–64CrossRefGoogle Scholar
  38. 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 403–430Google Scholar
  39. 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 975:384–394CrossRefGoogle Scholar
  40. Proctor J (1971) Plant ecology of serpentine. II. Plant response to serpentine soils. J Ecol 59:397–410CrossRefGoogle Scholar
  41. Proctor J, Woodell SRJ (1975) The ecology of serpentine soils. Adv Ecol Res 9:255–365CrossRefGoogle Scholar
  42. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53PubMedCrossRefGoogle Scholar
  43. Sambatti JBM, Rice KJ (2007) Functional ecology of ecotypic differentiation in the Californian serpentine sunflower (Helianthus exilis). New Phytol 175:107–119PubMedCrossRefGoogle Scholar
  44. Schechter SP, Bruns TD (2008) Serpentine and non-serpentine ecotypes of Collinsia sparsiflora associate with distinct arbuscular mycorrhizal fungal assemblages. Mol Ecol 17:3198–3210PubMedCrossRefGoogle Scholar
  45. Schüssler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  46. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  47. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20PubMedCrossRefGoogle Scholar
  48. 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 326:3–20CrossRefGoogle Scholar
  49. Štěpánek J (1997) Knautia L. – chrastavec. In: Slavík B (ed) Květena České republiky 6 [Flora of the Czech Republic 6]. Academia, Prague, pp 543–554Google Scholar
  50. 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 97:1798–1807PubMedCrossRefGoogle Scholar
  51. 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 13:185–190PubMedCrossRefGoogle Scholar
  52. 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 155:173–182CrossRefGoogle Scholar
  53. 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 38:2694–2704CrossRefGoogle Scholar
  54. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363PubMedCrossRefGoogle Scholar
  55. 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 144:307–313Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Institute of BotanyAcademy of Sciences of the Czech RepublicPrůhoniceCzech Republic
  2. 2.Department of Experimental Plant Biology, Faculty of ScienceCharles University in PraguePrague 2Czech Republic
  3. 3.Department of Botany, Faculty of ScienceCharles University in PraguePrague 2Czech Republic

Personalised recommendations