Advertisement

Plant and Soil

, Volume 293, Issue 1–2, pp 23–35 | Cite as

Relationships between Ni-hyperaccumulation and mycorrhizal status of different endemic plant species from New Caledonian ultramafic soils

  • H. Amir
  • N. Perrier
  • F. Rigault
  • T. Jaffré
Regular Article

Abstract

For a long time, Ni-hyperaccumulating plants have been considered to be non-mycorrhizal species. However, two recent publications have reported arbuscular mycorrhizal fungi (AMF) colonisation in Ni-hyperaccumulators. In this work, 9 endemic Ni-accumulators of unknown mycorrhizal status, from New Caledonia, were studied. All were mycorrhizal, but some were poorly colonised by the symbiots. Only AMF were observed. We analysed the relationships between Ni-hyperaccumulation ability and AMF colonisation of the plants. The roots of the three strongest hyperaccumulators, namely Sebertia acuminata, Psychotria douarrei and Phyllanthus favieri, were characterised by a lower mycorrhizal colonisation than the others. Mycorrhizal density varied with the level of Ni concentration in soil and plant. Root-colonisation by AMF was negatively correlated with leaf Ni content and with extractable-Ni concentration in soil. The roots of Ni-hyperaccumulators and the soils collected under these plants clearly inhibited germination of AMF spores. Hence, it appears that mycorrhizal colonisation is inhibited above a certain threshold of Ni concentration in soil and plant and becomes either absent or very low. However AMF isolated from the roots of strong Ni-hyperaccumulators have developed a very high level of Ni-tolerance and are then able to colonize at least parts of their roots.

Keywords

Arbuscular mycorrhizae AMF spore germination Nickel Ni-hyperaccumulating plants Ultramafic soils 

References

  1. Amir H, Pineau R (2003) Relationships between extractable Ni, Co and other metals and microbiological characteristics of different ultramafic soils from New Caledonia. Aust J Soil Res 41:1–14CrossRefGoogle Scholar
  2. Amir H, Pineau R, Violette Z (1997) Premiers résultats sur les endomycorhizes des plantes de maquis miniers. In: Jaffré T, Reeves RD, Becquer T (eds) The ecology of ultramafic and metalliferous areas. ORSTOM Edition, Noumea, pp 79–85Google Scholar
  3. Baker AJM (1981) Accumulators and excluders strategies in the response of plants to heavy metals. J Plant Nutr. 3:643–654Google Scholar
  4. Bathia N, Walsh KB, Orlic I, Siegele R, Ashwath N, Baker AJM (2004) Studies on spatial distribution of nickel in leaves and stems of the metal hyperaccumulator Stackhousia tryonii using nuclear microprobe (micro-PIXE) and EDXS techniques. Func Plant Biol 31:1061–1074CrossRefGoogle Scholar
  5. Boyd RS, Jaffré T (2001) Phytoenrichment of soil Ni content by Sebertia acuminata in New Caledonia and the concept of elemental allelopathy. South Afr J Sci 97:535–538Google Scholar
  6. Boyd RS, Jaffré T, Odom JW (1999) Variation of nickel content in the nickel-hyperaccumulating shrub Psychotria douarrei (Rubiaceae) from New Caledonia. Biotropica 31:403–410CrossRefGoogle Scholar
  7. Boyd RS, Shaw JJ, Martens SN (1994) Nickel hyperaccumulation defends Streptanthus polygaloides (Brassicaceae) against pathogens. Am J Bot 81:294–300CrossRefGoogle Scholar
  8. Brooks RR (1987) Serpentine and its vegetation. A multidisciplinary approach. Dioscorides Press, Portland, OregonGoogle Scholar
  9. Coles KE, David JC, Fisher PJ, Lappin-Scott HM, Macnair MR (2001) Solubilisation of zinc compounds by fungi associated with the hyperaccumulator Thlaspi caerulescens. Bot J Scot 51:237–247CrossRefGoogle Scholar
  10. Gildon A, Tinker PB (1981) A heavy metal-tolerant strain of a mycorrhizal fungus. Trans Brit Mycol Soc 77:648–649CrossRefGoogle Scholar
  11. Heggo A, Angle JS (1990) Effects of vesicular-arbuscular mycorrhizal fungi on heavy metal uptake by soybeans. Soil Biol Biochem 22:865–869CrossRefGoogle Scholar
  12. Hilderbrandt M, Kaldorf M, Bothe H (1999) The zinc violet and its colonisation by arbuscular mycorrhizal fungi. J Plant Physiol 154:709–717Google Scholar
  13. Jaffré T (1980) Etude écologique du peuplement végétal des sols dérivés de roches ultrabasiques en Nouvelle-Calédonie. ORSTOM Press, ParisGoogle Scholar
  14. Jaffré T, Brooks RR, Reeves RD (1976) Sebertia acuminata: a nickel accumulating plant from New Caledonia. Science 193:573–580CrossRefGoogle Scholar
  15. Jaffré T, Veillon JM (1991) Etude floristique et structurale de deux forêts denses humides sur roches ultrabasiques en Nouvelle-Calédonie. Bull Mus Natn Hist Nat 12:243–273Google Scholar
  16. Jhee EM, Boyd RS, Eubanks MD (2005) Nickel hyperaccumulation as an elemental defense of Streptanthus polygaloides (Brassicaceae): influence of herbivore feeding mode. New Phytol 168:331–344PubMedCrossRefGoogle Scholar
  17. Joner EJ, Leyval C (2001) Time-course of heavy metal uptake in maize and clover as affected by root density and different mycorrhizal inoculation regimes. Biol Fertil Soils 33:351–357CrossRefGoogle Scholar
  18. Kersten WJ, Brooks RR, Reeves RD, Jaffré T (1980) Nature of nickel complexes in Psychotria douarrei and other nickel-accumulating plants. Phyochemistry 19:1963–1965CrossRefGoogle Scholar
  19. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA Mycorrhizas. Mycol Res 92:486–505CrossRefGoogle Scholar
  20. Krämer U, Cotter Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638CrossRefGoogle Scholar
  21. Lee J, Reeves RD, Brooks RR, Jaffré T (1977) Isolation and identification of a citrato-complex of nickel from nickel-accumulating plants. Phytochemistry 16:1503–1505CrossRefGoogle Scholar
  22. Leyval C, Singh BA, Joner EJ (1995) Occurrence and infectivity of arbuscular mycorrhizal fungi in some Norwegian soils influenced by heavy metals and soil properties. Wat Air Soil Pol 84:203–216CrossRefGoogle Scholar
  23. Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonisation and function, physiological, ecological and applied aspects. Mycorrhiza 7:139–153CrossRefGoogle Scholar
  24. 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
  25. Ouerdane L, Mari S, Czernic P, Lebrun M, Lobinski R (2006) Speciation of non-covalent nickel species in plant tissue extracts by electrospray Q-TOFMS/MS after their isolation by 2D size exclusion-hydrophilic interaction LC (SEC-HILIC) monitored by ICP-MS. J Anal Atom Spectr 21:676–683CrossRefGoogle Scholar
  26. Pawlowska TE, Chaney RL, Chin M, Charvat I (2000) Effects of metal phytoextraction practices on the indigenous community of arbuscular mycorrizal fungi at a metal contaminated landfill. Appl Environ Microbiol 66:2526–2530PubMedCrossRefGoogle Scholar
  27. Perrier N, Amir H, Colin F (2006) Occurrence of mycorrizal symbioses in the metal-rich lateritic soils of the Koniambo Massif, New Caledonia. Mycorrhiza, 57:572–582Google Scholar
  28. Perrier N, Colin F, Jaffré T, Ambrosi JP, Rose J, Bottero JY (2004) Nickel speciation in Sebertia acuminata, a plant growing on a lateritic soil of New Caledonia. C R Geosciences 336:567–577CrossRefGoogle Scholar
  29. Reeves RD (1992) The hyperaccumulation of nickel by serpentine plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 253–277Google Scholar
  30. Sagner S, Kneer R, Wanner G, Cosson J-P, Deus-Neumann B, Zenk MH (1998) Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry 47:339–347PubMedCrossRefGoogle Scholar
  31. Schlegel HG, Cosson JP, Baker AJM (1991) Nickel-hyperaccumulating plants provide a niche for nickel-resistant bacteria. Bot Acta 104:18–25Google Scholar
  32. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Second edn. Academic Press, San Diego, LondonGoogle Scholar
  33. Tomsett EB, Thurman DA (1988) Molecular biology of metal tolerances in plants. Plant Cell Environ 11:383–394CrossRefGoogle Scholar
  34. Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization 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 Edition, Paris, pp 217–221Google Scholar
  35. 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
  36. Verkleij JAC (1990) In: Shaw AJ Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, FLGoogle Scholar
  37. Vivas A, Barea JM, Azcon R (2005) Interactive effect of Brevibacillus brevis and Glomus mossae, both isolated from Cd contaminated soil, on plant growth, physiological mycorrhizal fungal characteristics and soil enzymatic activities in Cd polluted soil. Environ Pollut 134:257–266PubMedCrossRefGoogle Scholar
  38. Vogel-Mikus K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242PubMedCrossRefGoogle Scholar
  39. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363PubMedCrossRefGoogle Scholar
  40. Weissenhorn I, Glashoff A, Leyval C, Berthelin J (1994) Differential tolerance to Cd and Zn of arbuscular mycorrhizal (AM) fungal spores from heavy-metal polluted soils. Plant Soil 167:189–196CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Unité “Mécanismes Adaptatifs et Biomolécules des plantes endémiques de Mélanésie”Université de la Nouvelle-CalédonieNoumeaNew Caledonia
  2. 2.UMR 161, Institut de Recherche pour le DéveloppementNoumeaNew Caledonia
  3. 3.Laboratoire de Botanique et d’Ecologie AppliquéesInstitut de Recherche pour le Développement, Centre de NouméaNoumeaNew Caledonia

Personalised recommendations