Abstract
In order to improve knowledge about the role of arbuscular mycorrhizal fungi (AMF) in the tolerance to heavy metals in ultramafic soils, the present study investigated the influence of two Glomus etunicatum isolates from New Caledonian ultramafic maquis (shrubland), on nickel tolerance of a model plant species Sorghum vulgare, and of two ultramafic endemic plant species, Alphitonia neocaledonica and Cloezia artensis. In a first step, plants were grown in a greenhouse, on sand with defined concentrations of Ni, to appreciate the effects of the two isolates on the alleviation of Ni toxicity in controlled conditions. In a second step, the influence of the AMF on A. neocaledonica and C. artensis plants grown in a New Caledonian ultramafic soil rich in extractable nickel was investigated. Ni reduced mycorrhizal colonization and sporulation of the fungal isolates, but the symbionts increased plant growth and adaptation of endemic plant species to ultramafic conditions. One of the two G. etunicatum isolates showed a stronger positive effect on plant biomass and phosphorus uptake, and a greater reduction in toxicity symptoms and Ni concentration in roots and shoots. The symbionts seemed to act as a barrier to the absorption of Ni by the plant and reduced root-to-shoot Ni translocation. Results indicate the potential of selected native AMF isolates from ultramafic areas for ecological restoration of such degraded ecosystems.
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Ahiabor DC, Hirata H (1995) Influence of growth stage on the association between some tropical legumes and two variant species of Glomus in an Andosol. Soil Sci Plant Nutr 40:481–496
Alexander E, Coleman R, Keeler-Wolfe T, Harrison S (2007) Serpentine geoecology of Northern North America. Geology, soils, and vegetation. Oxford University Press, New York
Amir H, Ducousso M (2010) Les bactéries et les champignons du sol sur roches ultramafiques. In: L’Huillier L, Jaffré T, Wulf A (eds) Mines et environnement en Nouvelle-Calédonie: les milieux sur substrats ultramafiques et leur restauration. IAC Ed Noumea, New Caledonia, pp 129–145
Amir H, Pineau R, Violette Z (1997) Premiers résultats sur les endomycorhizes des plantes de maquis miniers de Nouvelle-Calédonie. In : Jaffré T, Reeves RD, Becquer T (eds) Écologie des milieux sur roches ultramafiques et sur sols métallifères. Edition ORSTOM, Documents Scientifiques et Techniques III2, Noumea, pp 79–85
Amir H, Perrier N, Rigault F, Jaffré T (2007) Relationships between Ni-hyperaccumulation and mycorrhizal status of different endemic plant species from New Caledonian ultramafic soils. Plant Soil 293:23–35
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
Andrade SAL, Gratao PL, Silveira APD, Schiavinato MA, Azevedo RA, Mazzafera P (2009) Zn uptake, physiological response and stress attenuation in mycorrhizal jack bean growing in soil with increasing Zn concentrations. Chemosphere 75:1363–1370
Andrade SAL, Gratao PL, Azevedo RA, Silveira APD, Schiavinato MA, Mazzafera P (2010) Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. Environ Exp Bot 68:198–207
Arriagada C, Pereira G, Garcia-Romera I, Ocampo JA (2010) Improved zinc tolerance in Eucalyptus globulus inoculated with Glomus deserticola and Trametes versicolor or Coriolopsis rigida. Soil Biol Biochem 42:118–124
Audet P, Charest C (2007) Dynamics of arbuscular mycorrhizal symbiosis in heavy metal phytoremediation: meta-analytical and conceptual perspectives. Environ Pollut 147:609–614
Boulet FM, Lambers H (2005) Characterisation of arbuscular mycorrhizal fungi colonization 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
Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides, Portland
Carvalho LM, Cacador I, Martins-Loucao MA (2006) Arbuscular mycorrhizal fungi enhancer root cadmium and copper accumulation in the roots of the salt marsh plant Aster tripolium L. Plant Soil 285:161–169
Chen BD, Zhu YG, Duan J, Xiao XY, Smith SE (2007) Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environ Pollut 147:374–380
Christie P, Li X, Chen B (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil 261:209–217
Doherty JH, Baoming JI, Gasper BB (2008) Testing nickel tolerance of Sorghastrum nutans and its associated soil microbial community from serpentine and prairie soils. Environ Pollut 151:593–598
Ezawa T, Smith SE, Smith FA (2002) P metabolism and transport in AM fungi. Plant Soil 244:221–230
Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122
Guo Y, George E, Marschner H (1996) Contribution of an arbuscular mycorrhizal fungus to the uptake of cadmium and nickel in bean and maize plants. Plant Soil 184:195–205
Hewitt EJ (1952) Sand and water culture methods used in the study of plant nutrition. Commonwealth Agricultural Bureau Technical communication, No. 22. Maidstone, Kent, UK: Commonwealth Bureau of Horticulture and Plantation Crops, East Malling
Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochem 68:139–146
Jaffré T (1980) Étude écologique du peuplement végétal des sols dérivés de roches ultrabasiques en Nouvelle Calédonie. Travaux et documents de l'ORSTOM 124, Noumea
Jaffré T (1993) The relationship between ecological diversity and floristic diversity in New Caledonia. Biodiv Lett 1:82–87
Jaffré T, L’Huillier L (2010) Conditions de milieu des terrains miniers. In: L’Huillier L, Jaffré T, Wulf A (eds) Mines et environnement en Nouvelle-Calédonie: les milieux sur substrats ultramafiques et leur restauration. IAC Ed, Noumea, New Caledonia, pp 33–44
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 33:351–357
Jourand P, Ducousso M, Loulergue-Majorel C, Hannibal L, Santoni S, Prin Y, Lebrun M (2010a) Ultramafic soils from New Caledonia structure Pisolithus albus in ecotypes. FEMS Microbiol Ecol 72:238–249
Jourand P, Ducousso M, Reid R, Majorel C, Richert C, Riss J, Lebrun M (2010b) Nickel-tolerant ectomycorrhizal Pisolithus albus ultramafic ecotype isolated from nickel mines in New Caledonia strongly enhance growth of a host plant at toxic nickel concentrations. Tree Physiol 30:1311–1319
Kaldorf M, Kuhn AJ, Schöder WH, Hildebrandt U, Bothe H (1999) Selective element deposit in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728
Khan AG, Kuek C, Chauhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197–207
Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505
Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984
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
Leung HM, Ye ZH, Wong MH (2007) Survival strategies of plants associated with arbuscular mycorrhizal fungi on toxic mine tailings. Chemosphere 66:905–915
Liao JP, Lin XG, Cao ZH, Shi YQ, Wong MH (2003) Interactions between arbuscular mycorrhizae and heavy metals under sand culture experiment. Chemosphere 50:847–853
Lin AJ, Zhang XH, Wong MH, Ye ZH, Lou LQ, Wang YS, Zhu YG (2007) Increase of multi-metal tolerance of three leguminous plants by arbuscular mycorrhizal fungi colonization. Environ Geochem Health 29:473–481
Luçon S, Marion F, Niel JF, Pelletier B (1997) Réhabilitation des sites miniers sur roches ultramafiques en Nouvelle-Calédonie. In : Jaffré T, Reeves RD, Becquer T (eds) Écologie des milieux sur roches ultramafiques et sur sols métallifères. Edition ORSTOM, Documents Scientifiques et Techniques III2, Noumea, pp 297–303
Majorel C, Hannibal L, Soupe M, Carriconde F, Ducousso M, Lebrun M, Jourand P (2012) Tracking nickel-adaptive biomarkers in Pisolithus albus from New Caledonia using a transcriptomic approach. Mol Ecol 21:2208–2223
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London
Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102
Orlowska E, Mesjasz-Przybylowicz J, Przybylowicz W, Turnau K (2008) Nuclear microprobe studies of elemental distribution in mycorrhizal and non-mycorrhizal roots of Ni-hyperaccumulator Berkheya coddii. X-Ray Spectrom 37:129–132
Orlowska E, Przybylowicz W, Orlowski D, Turnau K, Mesjasz-Przybylowicz J (2011) The effect of mycorrhiza on the growth and elemental composition of Ni-hyperaccumulating plant Berkheya coddii Roessler. Environ Poll 159:3730–3738
Orlowska E, Godzik B, Turnau K (2012) Effect of different arbuscular mycorrhizal fungal isolates on growth and arsenic accumulation in plantago lanceolata L. Environ poll 168:121–130
Perrier N, Amir H, Colin F (2006) Occurrence of mycorrhizal symbioses in the metal-rich lateritic soils of the Koniambo Massif, New Caledonia. Mycorrhiza 16:449–458
Redon PO, Béguiristain T, Leyval C (2009) Differential effects of AM fungal isolates on Medicago trunculata growth and metal uptake in a multimetallic (Cd, Zn, Pb) contaminated agricultural soil. Mycorrhiza 19:187–195
Schübler A, Walker C (2010) The Glomeromycota. A species list with new families and new genera. Edinburgh & Kew, UK: The Royal Botanic Garden; Munich, Germany: Botanische Staatssammlung Munich; Oregon, USA: Oregon State University. URL: http://www.amf-phylogeny.com. ISBN-13: 978–1466388048; ISBN-10: 1466388048
Smith SE, Read DJ (2008) Mycorrhizal symbiosis (third edition). Academic, New York
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystems scales. Annu Rev Plant Biol 62:227–250
Sudova R, Doubkova P, Vosatka M (2008) Mycorrhizal association of Agrostis capillaris and Glomus intraradices under heavy metal stress: combination of plant clones and fungal isolates from contaminated substrates. Appl Soil Ecol 40:19–29
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, Paris, pp 217–221
Weissenhorn I, Leyval C, Belgy G, Berthelin J (1995) Arbuscular mycorrhizal contribution to heavy metal uptake by maize (Zea mays L.) in pot culture with contaminated soil. Mycorrhiza 5:245–251
Wu FY, Be YL, Leung HM, Ye ZH, Lin XG, Wong MH (2009) Accumulation of As, Pb, Zn, Cd and Cu and arbuscular mycorrhizal status in populations of Cynodon dactylon grown on metal-contaminated soils. Appl Soil Ecol 44:213–218
Zhang XH, Zhu Y-G, Chen BD, Lin AJ, Smith SE, Smith FA (2005) Arbuscular mycorrhizal fungi contribute to resistance of upland rice to combined metal contamination of soil. J Plant Nutr 28:2065–2077
Zhang XH, Lin AJ, Gao YL, Reid RJ, Wong MH, Zhu YG (2009) Arbscular mycorrhizal colonization increases copper binding capacity of root cell walls of Oryza sativa L. and reduces copper uptake. Soil Biol Biochem 41:930–935
Acknowledgments
This study was funded by two projects of “Agence Nationale de la Recherche Scientifique”: “ANR ECCO” and “ANR Ultrabio” and also by BioTop project CNRT “Nickel et son Environnement”. We want to thank Valérie Médevielle, Armelle Renard, Cindy Pupier, and Xavier Cuniberti for their contribution to the technical support of the study.
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Amir, H., Lagrange, A., Hassaïne, N. et al. Arbuscular mycorrhizal fungi from New Caledonian ultramafic soils improve tolerance to nickel of endemic plant species. Mycorrhiza 23, 585–595 (2013). https://doi.org/10.1007/s00572-013-0499-6
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DOI: https://doi.org/10.1007/s00572-013-0499-6