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Changes in mesophyll element distribution and phytometabolite contents involved in fluoride tolerance of the arid gypsum-tolerant plant species Atractylis serratuloides Sieber ex Cass. (Asteraceae)

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Abstract

Atractylis serratuloides is an abundant native spiny species that grows in the surroundings of superphosphate factories in Tunisia. This plant species is adapted to arid environments and tolerates a high level of fluoride pollution in soils. The aim of this study was to better understand the physiological mechanisms of fluoride tolerance of this species, comparing the fluoride-contaminated sites of Gabes and Skhira with the reference site of Smara. Results demonstrated the involvement of leaf element and phytometabolite balances in the in situ response of A. serrulatoides to fluoride. Calcium, sulphur and magnesium were differently distributed between the sites of Gabes and Smara in all plant organs. No specific tissue fluorine accumulation in root, stem and leaf, even in the most contaminated site at Gabes, was detected by EDAX mapping. Lower anthocyan and flavonol levels but enhanced nitrogen balance index were found in A. serrulatoides leaves from Gabes compared to the two other sites. A. serratuloides appeared as a fluoride excluder and its tolerance involved calcium interactions with fluoride. Moreover, an occurrence of dark septate endophytes and arbuscular mycorhizal fungi in root systems of A. serratuloides was reported for the first time, and these symbioses were present but low at all sites. We suggest the use of this plant species for fluoride-polluted soil stabilization.

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References

  • Affholder MC, 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 exposition risk. Sci Total Environ 454–455:219–229

    Article  Google Scholar 

  • Agati G, Cerovic ZG, Pinelli P, Tattini M (2011) Light-induced accumulation of ortho-dihydroxylated flavonoids as non-destructively monitored by chlorophyll fluorescence excitation techniques. Environ Exp Bot 73:3–9

    Article  CAS  Google Scholar 

  • Álvarez-Ayuso E, Giménez A, Ballesteros JC (2011) Fluoride accumulation by plants grown in acid soils amended with flue gas desulphurisation gypsum. J Hazard Mater 192:1659–1666

    Article  Google Scholar 

  • Asthir B, Basra AS, Batta SK (1998) Fluoride-induced alteration of carbon and nitrogen metabolism in developing wheat grains. Biol Plant 41:287–292

    Article  CAS  Google Scholar 

  • Baker AJM (1981) Accumulators and excluders: strategies in the response of plants to trace metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Barbier O, Arreola-Mendoza L, Del Razo LM (2010) Molecular mechanisms of fluoride toxicity. Chem Biol Interact 188:319–333

    Article  CAS  Google Scholar 

  • Ben Abdallah F, Elloumi N, Mezghani I, Boukhris M, Garrec J-P (2006) Survival strategies of pomegranate and almond trees in a fluoride polluted area. C R Biologies 329:200–207

    Article  CAS  Google Scholar 

  • Benaradj A, Boucherit H, Hasnaoui O, Mederbal K, Sehli A (2013) Rehabilitation of the steppe Lygeum spartum in the region of Naama (western Algeria). Energy Procedia 36:349–357

    Article  Google Scholar 

  • Blanke V, Renker C, Wagner M, Füllner K, Held M, Kuhn AJ, Buscot F (2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytol 166:981–992

    Article  CAS  Google Scholar 

  • Boukhris A, Laffont-Schwob I, Mezghani I, Kadri E, Lefi P, Pricop A, Tatoni T, Chaieb M (2015) Screening biological traits and fluoride contents of native vegetations in arid environments to select efficiently fluoride-tolerant native plant species for in-situ phytoremediation. Chemosphere 119:217–223

    Article  CAS  Google Scholar 

  • Braen SN, Weinstein LH (1985) Uptake of fluoride and aluminium by plants grown in contaminated soils. Water Air Soil Pollut 24:215–223

    Article  CAS  Google Scholar 

  • Branquinho C, Serrano HC, Pinto MJ, Martins-Loução MA (2007) Revisiting the plant hyperaccumulation criteria to rare plants and earth abundant elements. Environ Pollut 146:437–443

    Article  CAS  Google Scholar 

  • Brougham KM, Roberts SR, Davison AW, Port GR (2013) The impact of aluminium smelter shut-down on the concentration of fluoride in vegetation and soils. Environ Pollut 178:89–96

    Article  CAS  Google Scholar 

  • Cerovic ZG, 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. J Food Compos Anal 21:650–654

    Article  CAS  Google Scholar 

  • Chaieb M, Floret C, Le Floc’h E, Pontanier R (1992) Life history strategies and water resource allocation in five pasture species of the Tunisian arid zone. Arid Land Res Manag 6(1):1–10

    Google Scholar 

  • Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9

    Article  CAS  Google Scholar 

  • Choi DS, Kayama M, Jin HO, Lee CH, Izuta T, Koike T (2006) Growth and photosynthetic responses of two pine species (Pinus koraiensis and Pinus rigida) in a polluted industrial region in Korea. Environ Pollut 139:421–432

    Article  CAS  Google Scholar 

  • Cruz C, Correia P, Ramos A, Carvalho L, Bago A, Martins Loução MA (2008) Arbuscular mycorrhiza in physiological and morphological adaptations of Mediterranean plants, In: Varma A, editor. Mycorrhiza—State of the Art, Genetics and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure and Systematics. Springer, 733–752. DOI:10.1007/978-3-540-78826-3-34

  • Davison AW, Weinstein LH (2006) Some problems relating to fluorides in the environment: effects on plants and animals, in fluorine and the environment, atmospheric chemistry, emissions and lithosphere, Elsevier, Tressaud ed. Vol 1, p251-298

  • Delgado-Baquerizo M, Maestre FT, Gallardo A, Bowker MA, Wallenstein MD, Quero JL, Ochoa V, Gozalo B, García-Gómez M, Soliveres S, García-Palacios P, Berdugo M, Valencia E, Escolar C, Arredondo T, Barraza-Zepeda C, Bran D, Carreira JA, Chaieb M, Conceição AA, Derak M, Eldridge DJ, Escudero A, Espinosa CI, Gaitán J, Gatica MG, Gómez-González S, Guzman E, Gutiérrez J,R, Florentino A, Hepper E, Hernández RM, Huber-Sannwald E, MJankju M, Liu J, Mau RL, Miriti M, Monerris J, Naseri K, Noumi Z, Polo V, Prina A, Pucheta E, Ramírez E, Ramírez-Collantes DA, Romão R, Tighe M, Torres D, Torres-Díaz C, Ungar ED, Val J, Wamiti W, Wang D, Zaady E (2013) Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502:672–676

    Article  CAS  Google Scholar 

  • Façanha AR, Okorokova-Façanha AL (2002) Inhibition of phosphate uptake in corn roots by aluminum-fluoride complexes. Plant Physiol 129:1763–1772

    Article  Google Scholar 

  • Fornasiero RB (2001) Phytotoxic effects of fluorides. Plant Sci 161:979–985

    Article  CAS  Google Scholar 

  • Guerrero-Campo J, Alberto F, Hodgson J, García-Ruiz JM, Montserrat-Martí G (1999) Plant community patterns in a gypsum area of NE Spain. I. Interactions with topographic factors and soil erosion. J Arid Environ 41:401–410

    Article  Google Scholar 

  • Jauffret S, Visser M (2003) Assigning life-history traits to plant species to better qualify arid land degradation in Presaharian Tunisia. J Arid Environ 5:1–28

    Article  Google Scholar 

  • Koblar A, Tavčar G, Ponikvar-Svet M (2011) Effects of airborne fluoride on soil and vegetation. J Fluor Chem 132:755–759

    Article  CAS  Google Scholar 

  • Labidi S, Calonne M, Ben Jeddi F, Debiane D, Rezgui S, Laruelle F, Tisserant B, Grandmougin-Ferjani A, Sahraoui AL (2011) Calcareous impact on arbuscular mycorrhizal fungus development and on lipid peroxidation in monoxenic roots. Phytochemistry 72:2335–2341

    Article  CAS  Google Scholar 

  • Lamprecht WO, Powell RD (1977) The effect of hydrogen fluoride on two pigments in coleus. Econ Bot 31:148–152

    Article  CAS  Google Scholar 

  • LAS INRA (2014) Laboratoire d’analyses des sols d’Arras. Méthodes applicables aux sols. http://www6.lille.inra.fr/las/Methodes-d-analyse/Sols

  • Le Houérou H-N (1995) Bioclimatologie et biogéographie des steppes arides du Nord de l'Afrique : diversité biologique, développement durable et désertisation. In : Le Houérou H.-N. (ed.). Bioclimatologie et biogéographie des steppes arides du Nord de l’Afrique : diversité biologique, développement durable et désertisation. Montpellier : CIHEAM, p. 1–39 6

  • Leung HM, Ye ZH, Wong MH (2007) Survival strategies of plants associated with arbuscular mycorrhizal fungi on toxic mine tailings. Chemosphere 66:905–915

    Article  CAS  Google Scholar 

  • Leung HM, Wu FY, Cheung KC, Ye ZH, Wong MH (2010) Synergistic effects of arbuscular mycorrhizal fungi and phosphate rock on heavy metal uptake and accumulation by an arsenic hyperaccumulator. J Hazard Mater 181:497–507

    Article  CAS  Google Scholar 

  • Leusteck T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120:637–643

    Article  Google Scholar 

  • Li C, Zheng Y, Zhou J, Xu J, Ni D (2011) Changes of leaf antioxidant system, photosynthesis and ultrastructure in tea plant under the stress of fluorine. Biol Plant 55:563–566

    Article  CAS  Google Scholar 

  • Loganathan P, Hedley MJ, Wallace GC, Roberts AHC (2001) Fluoride accumulation in pasture forages and soils following long-term applications of phosphorus fertilisers. Environ Pollut 115:275–282

    Article  CAS  Google Scholar 

  • Mezghani I, Elloumi N, Ben Abdallah F, Chaieb M, Boukhris M (2005) Fluoride accumulation by vegetation in the vicinity of a phosphate fertiliser plant. Fluoride 38:69–75

    CAS  Google Scholar 

  • Mtimet A (2001). Soils of Tunisia, In: P. Zdruli, P. Steduto, C. Lacirignola, L. Montanarella (Eds.), Soil resources of southern and eastern Mediterranean countries. CIHEAM, Bari, pp. 243–262

  • Nakata PA, McConn MM (2000) Isolation of Medicago trunculata mutants defective in calcium oxalate formation. Plant Physiol 124:1097–1104

    Article  CAS  Google Scholar 

  • Navarro T, El Oualidi J, Taleb MS, Pascual V, Cabezudo B (2009) Dispersal traits and dispersal patterns in an oro-Mediterranean thorn cushion plant formation of the eastern High Atlas, Morocco. Flora 204(9):658–672

    Article  Google Scholar 

  • Özbek B, Dadali G (2007) Thin-layer drying characteristics and modelling of mint leaves undergoing microwave treatment. J Food Eng 83:541–549

    Article  Google Scholar 

  • Palacio S, Johnson D, Escudero A, Montserrat-Martí G (2012) Root colonisation by AM fungi differs between gypsum specialist and non-specialist plants: links to the gypsophile behaviour. J Arid Environ 76:128–132

    Article  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular arbuscular fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Pouget M (1968) Contribution à l’étude des croûtes et encroûtements gypseux de nappe dans le sud tunisien. Cah ORSTOM, Sér Pédologie 6:309–365

    CAS  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. Environ Pollut 156:1156–1163

    Article  CAS  Google Scholar 

  • Rabier J, Laffont-Schwob I, Pricop A, Ellili A, D’enjoy-Weinkammerer G, Salducci MD, Prudent P, Lotmani B, Tonetto A, Masotti V (2014) 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. doi:10.1007/s11270-014-1993-y

    Google Scholar 

  • Renker C, Blanke V, Buscot F (2005) Diversity of arbuscular mycorrhizal fungi in grassland spontaneously developed on area polluted by a fertilizer plant. Environ Pollut 135(2):255–66

    Article  CAS  Google Scholar 

  • Rodríguez AR, Mora JL, Arbelo C, Bordon J (2005) Plant succession and soil degradation in desertified areas (Fuerteventura, Canary Islands, Spain). Catena 59:117–131

    Article  Google Scholar 

  • Ronel M, Néeman G, Lev-Yadun S (2010) Spiny east Mediterranean plant species flower later and in a drier season than non-spiny species. Flora 205:276–281

    Article  Google Scholar 

  • Rouis MJ, Bensalah A (1990) Phosphogypsum management in Tunisia: environmental problems and required solutions. In: Proceedings of the Third International Symposium on Phosphogypsum, Orlando, FL, FIPR Pub. No. 01-060-083; 1, 87–105

  • Rutherford PM, Dudas MJ, Samek RA (1994) Environmental impacts of phosphogysum. Sci Total Environ 149:1–38

    Article  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  CAS  Google Scholar 

  • Singh J, Singh P, Singh A (2014) Fluoride ions vs removal. A Study, Arabian Journal of Chemistry, Technologies. doi:10.1016/j.arabjc.2014.06.005

    Google Scholar 

  • Slimani H, Aidoud A, Rozé F (2010) 30 years of protection and monitoring of a steppic rangeland undergoing desertification. J Arid Environ 74:685–691

    Article  Google Scholar 

  • Soysal Y (2004) Microwave drying characteristics of parsley. Biosyst Eng 89(2):167–173

    Article  Google Scholar 

  • Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999

    Article  CAS  Google Scholar 

  • Tayibi H, Choura M, López FA, Alguacil FJ, López-Delgado A (2009) Environmental impact and management of phosphogypsum. J Environ Manag 90:2377–2386

    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. J Hazard Mater 248–249:131–141

    Article  Google Scholar 

  • Treshow M, Anderson FK (1989) Plant stress from air pollution. Wiley, Chichester, p 283

    Google Scholar 

  • Trotta A, Falaschi P, Cornara L, Minganti V, Fusconi A, Drava G, Berta G (2006) Arbuscular mycorrhizae increase the arsenic translocation factor in the as hyperaccumulating fern Pteris vittata L. Chemosphere 65:74–81

    Article  CAS  Google Scholar 

  • Türkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67:2–9

    Article  Google Scholar 

  • Valdez-Jiménez L, Soria Fregozo C, Miranda Beltrán ML, Gutiérrez Coronado O, Pérez Vega MI (2011) Effects of the fluoride on the central nervous system. Neurologia 26(5):297–300

    Article  Google Scholar 

  • Wainwright M, Supharungsun S (1984) Release by fungi of F from insoluble fluorides. Trans Br Mycol Soc 82(2):289–292

    Article  CAS  Google Scholar 

  • Weinstein LH, Davison AW (2004) Fluorides in the environment. CABI Publishing, Cambridge

    Google Scholar 

  • White PJ, Broadley RM (2003) Calcium in plants. Rev Ann Bot 92:487–511

    Article  CAS  Google Scholar 

  • Wu FY, Bi YL, Leung HM, Ye ZH, Lin XG, Wong MH (2010) 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 213–218

  • Zahran MA (2010) Climate vegetation. Afro-Asian Mediterranean and Red Sea coastal lands. Plant and Vegetation. London New York: Springer Dordrecht Heidelberg, 344

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Acknowledgments

This study was partly funded by the Action Intégrée Franco-Tunisienne of the French Ministère des Affaires Etrangères et Européennes and the Tunisian Ministère de l’Enseignement Supérieur, de la Recherche Scientifique. The authors thank Imed Mezghani for his help in harvesting and sampling in the field, and thanks are also due to Oceane Beaufort for helping with root staining in the laboratory. The authors are grateful to Laurent Vassalo for his efficient help in TOC and TKN analyses in a high-performance time. Also, the authors thank the Groupe Chimique Tunisien, in particular the Direction Centrale de la Recherche, for its assistance and logistical support in carrying out this study. Lastly, the authors would like to thank Michael Paul for revising the English of this text.

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Correspondence to Isabelle Laffont-Schwob.

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Boukhris, A., Laffont-Schwob, I., Rabier, J. et al. Changes in mesophyll element distribution and phytometabolite contents involved in fluoride tolerance of the arid gypsum-tolerant plant species Atractylis serratuloides Sieber ex Cass. (Asteraceae). Environ Sci Pollut Res 22, 7918–7929 (2015). https://doi.org/10.1007/s11356-014-3957-6

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