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Heavy Metal and Arsenic Resistance of the Halophyte Atriplex halimus L. Along a Gradient of Contamination in a French Mediterranean Spray Zone

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Abstract

Elements uptake, histological distributions as well as mycorrhizal and physiological statuses of Atriplex halimus were determined on trace metal and metalloid polluted soils from the surrounding spray zones of a former lead smelter in the South-East coast of Marseille (France). Analyses of heavy metal and arsenic distribution in soil and plant organs showed that A. halimus tolerance is largely due to exclusion mechanisms. No specific heavy metal concentration in leaf or root tissues was observed. However, accumulation of salts (NaCl, KCl, Mg and Ca salts) on leaf bladders and peripheral tissues of roots was observed and may compete with metal element absorption. Occurrence of endomycorrhizal structures was detected in roots and may contribute to lower element transfer from root into the aerial parts of plants. The non-destructive measurements of leaf epidermal chlorophylls, flavonols and phenols showed a healthy state of the A. halimus population on the metal and metalloid polluted sites. Considering the low metal bioaccumulation and translocation factors along with a reduced metal stress diagnosis, A. halimus appeared as a good candidate for phytostabilization of trace metals and metalloids and notably arsenic in contaminated soils of the Mediterranean spray zone. However, its invasive potential has to be determined before an intensive in situ use.

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References

  • Abbad, A., Cherkaoui, M., Wahid, N., El Hadrami, A., & Benchaabane, A. (2004). Variabilités phénotypique et génétique de trois populations naturelles d’Atriplex halimus. Comptes Rendus Biologies, 327, 371–380.

    Article  Google Scholar 

  • Abou Jaoudé, R., Pricop, A., Laffont-Schwob, I., Prudent, P., Rabier, J., Masotti, V., De Dato, G., & De Angelis, P. (2012). Evaluating the potential use of Tamarix gallica L. for phytoremediation practices in heavy-metal polluted soils. Geophysical Research Abstracts, 14, EGU2012–EGU12887.

    Google Scholar 

  • Affholder, M. C., Prudent, P., Masotti, V., Coulomb, B., Rabier, J., Nguyen-The, B., & Laffont-Schwob, I. (2013). Transfer of metals and metalloids from soil to shoots in wild rosemary (Rosmarinus officinalis L.) growing on a former lead smelter site: human exposure risk. Science of the Total Environment, 454–455, 219–229.

    Article  Google Scholar 

  • Affholder, M.C., Pricop, A.-D., Laffont-Schwob, I. Coulomb, B., Rabier, J., Borla, A., Demelas, C., & Prudent, P. (2014). As, Pb, Sb and Zn transfers from soil to root of wild rosemary: do native symbionts matter? Plant and Soil. doi:10.1007/s11104-014-2135-4.

  • Agati, G., Cerovic, Z. G., Pinelli, P., & Tattini, M. (2011). Light-induced accumulation of ortho-dihydroxylated flavonoids as non-destructively monitored by chlorophyll fluorescence excitation techniques. Environmental and Experimental Botany, 73, 3–9.

    Article  CAS  Google Scholar 

  • Aguilera, L. E., Gutierrez, J. R., & Moreno, R. J. (1998). Vesicular arbuscular mycorrhizae associated with saltbushes Atriplex spp. (Chenopodiaceae) in the Chilean arid zone. Revista Chilena de Historia Natural, 71, 291–302.

    Google Scholar 

  • Allen, M. F. (1983). Formation of arbuscular mycorrhizae in Atriplex gardneri, Chenopodiaceae: seasonal response in a cold desert. Mycologia, 75, 773–776.

    Article  Google Scholar 

  • Arnao, M. B., & Hernández-Ruiz, J. (2009). Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves. Journal of Pineal Research, 46(1), 58–63.

    Article  CAS  Google Scholar 

  • Asghari, H. R., Marschner, P., Smith, S. E., & Smith, F. A. (2005). Growth response of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels. Plant and Soil, 273, 245–256.

    Article  CAS  Google Scholar 

  • Baize, D. (1988). Guide des analyses courantes en pédologie. Paris: Institut de la Recherche Agronomique.

    Google Scholar 

  • Bajji, M., Kinet, J. M., & Lutts, S. (1998). Salt stress effects on roots and leaves of Atriplex halimus L. and their corresponding callus cultures. Plant Science, 137, 131–142.

    Article  CAS  Google Scholar 

  • Bajji, M., Kinet, J. M., & Lutts, S. (2002). Osmotic and ionic effects of NaCl on germination, early seedling growth, and ion content of Atriplex halimus (Chenopodiaceae). Canadian Journal of Botany, 80, 297–304.

    Article  CAS  Google Scholar 

  • Baker, A. J. M., & Brooks, R. R. (1989). Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery, 1, 81–126.

    CAS  Google Scholar 

  • Barrow, J. R., & Aaltonen, R. E. (2001). Evaluation of the internal colonization of Atriplex canescens (Pursh) Nutt. roots by dark septate fungi and the influence of host physiological activity. Mycorrhiza, 11, 199–205.

    Article  Google Scholar 

  • Becker, W., & Apel, K. (1993). Differences in gene expression between natural and artificially induced leaf senescence. Planta, 189, 74–79.

    Article  CAS  Google Scholar 

  • Bidel, L. P. R., Meyer, S., Goulas, Y., Cadot, Y., & Cerovic, Z. G. (2007). Responses of epidermal phenolic compounds to light acclimation: in vivo qualitative and quantitative assessment using chlorophyll fluorescence. Journal of Experimental Botany, 58, 1753–1760.

    Article  Google Scholar 

  • Cerovic, Z. G., Moise, N., Agati, G., Latouche, G., Ben Ghozlen, N., & Meyer, S. (2008). New portable optical sensors for the assessment of winegrape phenolic maturity based on berry fluorescence. Journal of Food Composition and Analysis, 21, 650–654.

    Article  CAS  Google Scholar 

  • 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 and Soil, 261, 209–217.

    Article  CAS  Google Scholar 

  • Clijsters, H., & Assche, F. (1985). Inhibition of photosynthesis by heavy metals. Photosynthesis Research, 7, 31–40.

    Article  CAS  Google Scholar 

  • Cotruvo, J. A. (2005). Water desalinization processes and associated health and environmental issues. Water Conditioning and Purification, 1, 13–17.

    Google Scholar 

  • Dietl, C., Reifenhäuser, W., & Peichl, L. (1997). Association of antimony with traffic occurrence in airborne dust, deposition and accumulation in standardized grass cultures. Science of the Total Environment, 205(2–3), 235–244.

    Article  CAS  Google Scholar 

  • El Omari, B., Fleck, I., Aranda, X., Abadía, A., Cano, A., Marino, B., & Arnao, C. (2003). Total antioxidant activity in Quercus ilex resprouts after fire. Plant Physiology and Biochemistry, 41, 41–47.

    Article  Google Scholar 

  • Filippi, O., & Aronson, J. (2010). Plantes invasives en région méditerranéenne: quelles restrictions d'utilisation préconiser pour les jardins et les espaces verts? Ecologia Mediterranea, 36, 31–54.

    Google Scholar 

  • Foster, S., Maher, W., Krikowa, F., Telford, K., & Ellwood, M. (2005). Observations on the measurement of total antimony and antimony species in algae, plant and animal tissues. Journal of Environmental Monitoring, 7, 1214–1219.

    Article  CAS  Google Scholar 

  • Institut national de l’information géographique et forestière (IGN). (1926, 1961) France & IGNF_PVA_1-0__1926-08-06__C3145-0351_1926_NP8_2050, scale 1: 9.916,IGNF_PVA_1-0__1961-03-25__C3245-0371_CDP1700_9055, scale 1: 8.975, 13008, Marseille 8e Arrondissement retrieved from http://geoportail.gouv.fr. Accessed 6 May 2013.

  • GPS visualizer. (2013). http://www.gpsvisualizer.com/. Accessed 10 May 2013.

  • Grigore, M.-N., & Toma, C. (2010). Salt secreting structures of halophytes. An integrative approach, Romanian Academic Press, Bucharest, 290 pp (in Romanian, extended summary in English). ISBN 978-973-27-1911-4.

  • He, X., Mouratov, S., & Steinberger, Y. (2002). Spatial distribution and colonization of arbuscular mycorrhizal fungi under the canopies of desert halophytes. Arid Land Research and Management, 16, 149–160.

    Article  Google Scholar 

  • Heywood, V., & Brunel, S. (2008). Code of conduct on horticulture and invasive alien plants. Council of Europe Convention on the Conservation of European Wildlife and Natural Habitats Standing Committee 28th meeting Strasbourg, 24–27 November 2008.

  • Hu, Y., & Schmidhalter, U. (2005). Drought and salinity: a comparison of their effects on mineral nutrition of plants. Journal of Plant Nutrition and Soil Science, 168, 541–549.

    Article  CAS  Google Scholar 

  • Johnson-Green, P. C., Kenkel, N. C., & Booth, T. (1995). Distribution and phenology of arbuscular-mycorrhizae along a salinity gradient at an inland salt pan. Canadian Journal of Botany, 73, 1318–1327.

    Article  Google Scholar 

  • Jumpponen, A. (2001). Dark septate endophytes—are they mycorrhizal? Mycorrhiza, 11, 207–211.

    Article  Google Scholar 

  • Kamaludeen, S. P. B., & Ramasamy, K. (2008). Rhizoremediation of metals: harnessing microbial communities. Indian Journal of Microbiology, 48, 80–88.

    Article  CAS  Google Scholar 

  • Kessler, J. J. (1990). Atriplex forage as a dry season supplementation feed for sheep in the Montane Plains of the Yemen Arab Republic. Journal of Arid Environments, 19, 225–234.

    Google Scholar 

  • Khavari-Nejad, R. A., Bujar, M., & Attaran, E. (2006). Evaluation of anthocyanin contents under salinity (NaCl) stress in Bellis perennis L. In M. A. Khan & D. J. Weber (Eds.), Ecophysiology of High Salinity Tolerant Plants, Series: Tasks for Vegetation Science (pp. 127–134). New York: Springer.

    Chapter  Google Scholar 

  • Kronzucker, H. J., & Britto, D. T. (2010). Sodium transport in plants: a critical review. New Phytologist, 189, 54–81.

    Article  Google Scholar 

  • Laffont-Schwob, I., Dumas, P. J., Pricop, A., Rabier, J., Miché, L., Affre, L., Masotti, V., Prudent, P., & Tatoni, T. (2011a). Insights on metal-tolerance and symbionts of the rare species Astragalus tragacantha aiming at phytostabilization of polluted soils and plant conservation. Ecologia Mediterranea, 37, 57–62.

    Google Scholar 

  • Laffont-Schwob, I., D’Enjoy-Weinkammerer, G., Pricop, A., Prudent, P., Masotti, V., & Rabier, J. (2011b). Evaluation of a potential candidate for heavy metal phytostabilization in polluted sites of the Mediterranean littoral (SE Marseille): endomycorrhizal status, fitness biomarkers and metal content of Atriplex halimus spontaneous populations. Ecological Questions, 14, 89–90.

    Google Scholar 

  • Lasalle, J.L. (2007). Présence de plomb et d’arsenic sur le littoral sud de Marseille: une etude de santé (juillet 2005). INVS report.

  • Le Houérou, H. N. (1992). The role of saltbushes (Atriplex spp.) in arid lands rehabilitation in the Mediterranean basin: a review. Agroforestry Systems, 18, 107–148.

    Article  Google Scholar 

  • Lefèvre, I., Marchal, G., Meerts, P., Corréal, E., & Lutts, S. (2009). Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environmental and Experimental Botany, 65, 142–152.

    Article  Google Scholar 

  • Lotmani, B., Fatarna, L., Berkani, A., Rabier, J., Prudent, P., & Laffont-Schwob, I. (2011). Selection of Algerian populations of the Mediterranean saltbush, Atriplex halimus, tolerant to high concentrations of lead, zinc, and copper for phytostabilization of heavy metal-contaminated soils. The European Journal of Plant Science and Biotechnology, 5, 20–26.

    Google Scholar 

  • Lutts, S., Lefèvre, I., Delpérée, C., Kivits, S., Dechamps, C., Robledo, A., & Correal, E. (2004). Heavy metal accumulation by the halophyte species Mediterranean saltbush. Journal of Environmental Quality, 33, 1271–1279.

    Article  CAS  Google Scholar 

  • Manousaki, E., & Kalogerakis, N. (2009). Phytoextraction of Pb and Cd by the Mediterranean saltbush (Atriplex halimus L.): metal uptake in relation to salinity. Environmental Science and Pollution Research, 16, 844–854.

    Article  CAS  Google Scholar 

  • Manousaki, E., & Kalogerakis, N. (2011). Halophytes present new opportunities in phytoremediation of heavy metals and saline soils. Industrial and Engineering Chemical Research, 50, 656–660.

    Article  CAS  Google Scholar 

  • Martinez, J. P., Lutts, S., Schanck, A., Bajji, M., & Kinet, J. M. (2004). Is osmotic adjustment required for water stress resistance in the Mediterranean shrub Atriplex halimus L.? Journal of Plant Physiology, 161, 1041–1051.

    Article  CAS  Google Scholar 

  • Mateos-Naranjo, E., Andrades-Moreno, L., Cambrollé, J., & Perez-Martin, A. (2013). Assessing the effect of copper on growth, copper accumulation and physiological responses of grazing species Atriplex halimus: ecotoxicological implications. Ecotoxicological and Environmental Safety, 90, 136–142.

    Article  CAS  Google Scholar 

  • McArthur, E.D., & Sanderson, C. (1984). Distribution, systematics and evolution of Chenopodiaceae: an overview. In A.R Tiedemann., E.D. McArthur, H.C. Stutz, R. Stevens, K.L. Johnson (Eds.), Proceedings of the symposium on the biology of Atriplex and related Chenopods (pp. 14-24). US Department of Agriculture, Forest Service, USA.

  • Mendez, M. O., & Maier, R. M. (2008). Phytoremediation of mine tailings in temperate and arid environments. Reviews in Environmental Science and Biotechnology, 7, 47–59.

    Article  CAS  Google Scholar 

  • Ortíz-Dorda, J., Martínez-Mora, C., Correal, E., Simón, B., & Cenis, J. L. (2005). Genetic structure of Atriplex halimus populations in the Mediterranean Basin. Annals of Botany, 95, 827–834.

    Article  Google Scholar 

  • Osmond, C. B., Björkman, O., & Anderson, D. J. (1980). Physiological processes in plant ecology: towards a synthesis with Atriplex. Berlin: Springer-Verlag.

    Book  Google Scholar 

  • Phillips, J. M., & Hayman, D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55, 159–161.

    Article  Google Scholar 

  • Pourrat, Y., & Dutuit, P. (1994). Etude précoce des effets morphologiques et physiologiques du rapport sodium/calcium in vitro sur une population d’Atriplex halimus. In AUPLEF—UREF (Ed.), Quel Avenir pour l’Amélioration des Plantes? (pp. 283–295). Paris: John Libbey Eurotext.

    Google Scholar 

  • Rabier, J., Laffont-Schwob, I., Notonier, R., Fogliani, B., & Bouraïma-Madjebi, S. (2008). Anatomical element localization by EDXS in Grevillea exul var. exul under Nickel stress. Environmental Pollution, 156, 1156–1163.

    Article  CAS  Google Scholar 

  • Sawalha, M. F., Peralta-Videa, J. R., Sanchez-Salcido, B., & Gardea-Torresdey, J. L. (2009). Sorption of hazardous metals from single and multi-element solutions by saltbush biomass in batch and continuous mode: interference of calcium and magnesium in batch mode. Journal of Environmental Management, 90, 1213–1218.

    Article  CAS  Google Scholar 

  • Skinner, H. C. W., & Jahren, A. H. (2003). Biomineralization. In H. F. Holland & K. K. Turekian (Eds.), Treatise on geochemistry 8 (pp. 117–184). New York: Elsevier.

    Google Scholar 

  • Sonjak, S., Udovic, M., Wraber, T., Likar, M., & Regvar, M. (2009). Diversity of halophytes and identification of arbuscular mycorrhizal fungi colonising their roots in an abandoned and sustained part of Secovlje saltern. Soil Biology & Biochemistry, 41, 1847–1856.

    Article  CAS  Google Scholar 

  • Testiati, E., Parinet, J., Massiani, C., Laffont-Schwob, I., Rabier, J., Pfeifer, H. R., Lenoble, V., Masotti, V., & Prudent, P. (2013). Trace metal and metalloid contamination levels in soils and in two native plant species of a former industrial site: evaluation of the phytostabilization potential. Journal of Hazardous Materials, 248–249, 131–141.

    Article  Google Scholar 

  • Thimann, K. V. (1980). Senescence in plants. Boca Raton: CRC Press.

    Google Scholar 

  • Triboit, F., Laffont-Schwob, I., Demory, F., Soulié-Märsche, I., Rabier, J., Despréaux, M., & Thiéry, A. (2010). Heavy metal lability in porewater of highway detention pond sediments in South-Eastern France in relation to submerged vegetation. Water, Air, & Soil Pollution, 209(1-4), 229–240.

    Article  CAS  Google Scholar 

  • Türkan, I., & Demiral, T. (2009). Recent developments in understanding salinity tolerance. Environmental and Experimental Botany, 67(1), 2–9.

    Article  Google Scholar 

  • Walker, D. J., Lutts, S., Sánchez-García, M., & Correal, E. (2014). Atriplex halimus L.: its biology and uses. Journal of Arid Environments, 100-101, 111–121.

    Article  Google Scholar 

  • Whipkey, C. E., Capo, R. C., Chadwick, O. A., & Stewart, B. W. (2000). The importance of sea spray to the cation budget of a coastal Hawaiian soil: a strontium isotope approach. Chemical Geology, 168, 37–48.

    Article  CAS  Google Scholar 

  • Yoon, J., Cao, X., Zhou, Q., & Ma, L. Q. (2006). Accumulation of Pb, Cu and Zn in native plants growing on a contaminated Florida site. Science of the Total Environment, 368, 456–464.

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank Thomas Devenoges, Soumia Djilalli and Cécile Evrard for their technical assistance of root preparation and endomycorrhizal colonization counting and Laurent Vassalo and Carine Demelas for their analytical assistance for trace and major element measurements. Many thanks to Alma Heckenroth, who conceived the map of the collection sites, and to Frédéric Médail for helpful discussion on the biogeographic distribution of A. halimus. The authors are grateful to Lidwine Le Mire Pécheux from the National Park of Calanques for helpful discussion on environment management. This study was funded by the French Research National Agency (ANR Marséco 2008 CESA 018) and supported by the National Innovative Cluster on Risks Management. This research has been made possible by participation in the EU COST Action FA 0901 favouring links between scientists of various countries on halophytes. Isabelle Laffont-Schwob is grateful to Tim Flowers and James Aronson that gave her the opportunity to participate to this COST Action.

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Authors and Affiliations

  1. Aix Marseille Université, CNRS, IRD, Avignon Université, Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale (IMBE), Campus Saint Charles, Case 4, 3, place Victor Hugo, 13331, Marseille cedex 03, France

    Jacques Rabier, Isabelle Laffont-Schwob, Anca Pricop, Ahlem Ellili, Gabriel D’Enjoy-Weinkammerer, Marie-Dominique Salducci & Véronique Masotti

  2. Aix Marseille Université, CNRS, Laboratoire de Chimie de l’Environnement, FRE 3416, Case 29, 3 place Victor Hugo, 13331, Marseille cedex 3, France

    Anca Pricop & Pascale Prudent

  3. Unité de Physiologie et Biochimie de la Tolérance au Sel des Plantes, Faculté des Sciences, Département de Biologie, Université de Tunis El Manar, 1060, Tunis, Tunisia

    Ahlem Ellili

  4. Laboratoire Protection des végétaux, Unité culture in vitro, Université A. Ibn Badis de Mostaganem, Mostaganem, Algeria

    Brahim Lotmani

  5. Aix Marseille Université, PRATIM, 3 place Victor Hugo, 13331, Marseille cedex 3, France

    Alain Tonetto

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  1. Jacques Rabier
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Correspondence to Isabelle Laffont-Schwob.

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Jacques Rabier and Isabelle Laffont-Schwob contributed equally to this work.

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Rabier, J., Laffont-Schwob, I., Pricop, A. et al. Heavy Metal and Arsenic Resistance of the Halophyte Atriplex halimus L. Along a Gradient of Contamination in a French Mediterranean Spray Zone. Water Air Soil Pollut 225, 1993 (2014). https://doi.org/10.1007/s11270-014-1993-y

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