Fluoride Action Network

Abstract

Fluoride (F) is considered one of the most phytotoxic pollutants, even when present in low concentrations. When dispersed in the air, F can be transported to about 100 km from the polluting source, reaching plants, animals and humans and causing serious damage. Nevertheless, studies are still scarce on the effect of fluoride in Cerrado species integrating morphological, anatomical and physiological responses. Therefore, this study aimed to investigate the effect of simulated rainfall containing potassium fluoride (KF) on Hancornia speciosa leaves and roots, to determine its bioaccumulator potential. Young plants at approximately 45 days of emergence were treated daily with simulated KF rain at four concentrations (0, 4, 8 and 12 mg L-1), and four replicates. The experiment was carried out for 40 days, in completely randomized design. After KF exposure, visual, morphological and chlorophyll a fluorescence analyses were performed, alongside fluoride accumulation assessments in roots and shoots. Hancornia speciosa did not present any visual, anatomical and physiological symptoms in response to fluoride; however, it showed an accumulation of phenolic compounds in mesophyll root and leaf cells in all treatments. Physiological characteristic preservation and fluoride accumulation in roots and leaves allow us to suggest that Hancornia speciosa displays tolerance potential at the investigated doses.


References

  1. Agalakova N, Gusev PG (2012) Fluoride induces oxidative stress and ATP depletion in the rat erythrocytes in vitro. Environ Toxicol Pharmacol 34:334–337. https://doi.org/10.1016/j.etap.2012.05.006

    CAS  Article  PubMed  Google Scholar

  2. Almeida GQ, Chaves LJ, Vieira MC, Ganga RMD (2019) Agronomic evaluation of a Hancornia speciosa Gomes germplasm collection from the Brazilian Cerrado. Crop Breed Appl Biotechnol 19:8–14. https://doi.org/10.1590/1984-70332019v19n1a02

    Article  Google Scholar

  3. Alves ES, Moura BB, Vaz Pedroso AN, Tresmondi F, Machado SR (2016) Cellular markers indicative of ozone stress on bioindicator plants growing in a tropical environment. Ecol Indic 67:417–424. https://doi.org/10.1016/j.ecolind.2016.03.011

    CAS  Article  Google Scholar

  4. Baker NR, Rosenqvst E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55(403):1607–1621. https://doi.org/10.1093/jxb/erh196

    CAS  Article  PubMed  Google Scholar

  5. Banerjee A, Roychoudhury A (2019) Fluorine: a biohazardous agent for plants and phytoremediation strategies for its removal from the environment. Biol Plant 63:104–112. https://doi.org/10.32615/bp.2019.013

    CAS  Article  Google Scholar

  6. Baunthiyal M, Sharma V (2014) Response of three semi-arid plant species to fluoride; consequences for chlorophyll florescence. Int J Phytoremediation 16(4):397–414. https://doi.org/10.1080/15226514.2013.783790

    CAS  Article  PubMed  Google Scholar

  7. Ben Abdallah F, Elloumi N, Mezghani I, Boukhris M, Garrec JP (2006) Survival strategies of pomegranate and almond trees in a fluoride polluted area. Comptes Rendus Biol 329:200–207. https://doi.org/10.1016/j.crvi.2005.12.003

    CAS  Article  Google Scholar

  8. Bhatnagar A, Kumar E, Silanpaa M (2011) Fluoride removal from water by adsorption- a review. Chem Eng J 171:811–840. https://doi.org/10.1016/j.cej.2011.05.028

    CAS  Article  Google Scholar

  9. Calzone A, Podda A, Lorenzini G, Maserti BE, Carrari E, Deleanu E, Hoshika Y, Haworth M, Nali C, Badea O, Pellegrini E, Fares S, Paoletti E (2019) Cross-talk between physiological and biochemical adjustments by Punica granatum cv. Dente di cavallo mitigates the effects of salinity and ozone stress. Sci Total Environ 656:589–597. https://doi.org/10.1016/j.scitotenv.2018.11.402

    CAS  Article  PubMed  Google Scholar

  10. Cardoso LM, Reis BL, Oliveira DS, Pinheiro-Sant´ana HM (2014) Mangaba (Hancornia speciosa Gomes) from the Brazilian Cerrado: nutritional value, carotenoids and antioxidant vitamins. Fruits 69(2):89–99. https://doi.org/10.1051/fruits/2013105

    CAS  Article  Google Scholar

  11. Divan Junior AM, Oliva MA, Martinez CA, Cambraia J (2007) Effects of fluoride emissions on two tropical grasses: Chloris gavana and Panicum maximum, cv. Colonião. Ecotoxicol Environ Saf 67:247–253. https://doi.org/10.1016/j.ecoenv.2006.06.002

    CAS  Article  PubMed  Google Scholar

  12. Farhangi-Abriz S, Torabian S (2017) Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress. Ecotoxicol Environ Saf 137:64–70. https://doi.org/10.1016/j.ecoenv.2016.11.029

    CAS  Article  PubMed  Google Scholar

  13. Fawell J, Bailey K, Chilton J, Dahi E, Fewtrell L, Magara Y (2006) Fluoride in drinking water, WHO, IWA publishing, pp 1–144

  14. Fornasiero RB (2001) Phytotoxic effects of fluorides. Plant Sci 161:979–985. https://doi.org/10.1016/S0168-9452(01)00499-X

    CAS  Article  Google Scholar

  15. Fortes C, Duarte AP, Matsuoka S, Hoffmann HP, Lavorenti NA (2003) Fluoride toxicity in corn cultivars in an area near a ceramic industry, Araras (SP). Bragantia 62:275–281. https://doi.org/10.1590/S0006-87052003000200013

    CAS  Article  Google Scholar

  16. Franzaring J, Hrenn H, Schumm C, Klumpp A, Fangmeier A (2006) Environmental monitoring of fluoride emissions using precipitation, dust, plant and soil samples. Environ Pollut Barking 144(1):158–165. https://doi.org/10.1016/j.envpol.2005.12.033

    CAS  Article  Google Scholar

  17. Gao HJ, Zhao Q, Zhang XC, Wan XC, Mao JD (2014) Localization of fluoride and aluminum in subcellular fractions of tea leaves and roots. J Agric Food Chem 62:2313–2319. https://doi.org/10.1021/jf4038437

    CAS  Article  PubMed  Google Scholar

  18. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92. https://doi.org/10.1016/S0304-4165(89)80016-9

    CAS  Article  Google Scholar

  19. Ghassemi-Golezani K, Farhangi-Abriz S (2019) Biochar alleviates fluoride toxicity and oxidative stress in safflower (Carthamus tinctorius L.) seedlings. Chemosphere 223:406–415. https://doi.org/10.1016/j.chemosphere.2019.02.087

    CAS  Article  PubMed  Google Scholar

  20. Gritsan NP, Miller GM, Schumatkov GG (1995) Correlation between heavy metals and fluoride in soil, air and plants in relation to environmental damages. Fluoride 28:180–188

    CAS  Google Scholar

  21. Günthardt-Goerg MS, Vollenweider P (2007) Linking stress with macroscopic and microscopic leaf response in trees: new diagnostic perspectives. Environ Pollut 147:467–488. https://doi.org/10.1016/j.envpol.2006.08.033

    CAS  Article  PubMed  Google Scholar

  22. Jha SK, Nayak AK, Sharma YK (2009) Fluoride toxicity effects in onion (Allium cepa L.) grown in contaminated soils. Chemosphere 76:353–356. https://doi.org/10.1016/j.chemosphere.2009.03.044

    CAS  Article  PubMed  Google Scholar

  23. Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Co, New York, p 523

    Google Scholar

  24. Karnovsky MJA (1965) Formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27(2):137–138

    Google Scholar

  25. Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromo thymoquinone. Biochim Biophys Acta 376:105–115. https://doi.org/10.1016/0005-2728(75)90209-1

    CAS  Article  PubMed  Google Scholar

  26. Krause GH, Weis E (1991) Chorophyll fluorescence and photosyntheses: the basics. Ann Rev Plant Biol 42:313–349. https://doi.org/10.1146/annurev.pp.42.060191.001525

    CAS  Article  Google Scholar

  27. Kumari S, Khan S (2018) Effect of Fe3O4 NPs application on fluoride (F) accumulation efficiency of Prosopis juliflora. Ecotoxicol Environ Saf 166:419–426. https://doi.org/10.1016/j.ecoenv.2018.09.103

    CAS  Article  PubMed  Google Scholar

  28. Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43(3):379–393. https://doi.org/10.1007/s11099-005-0062-6

    CAS  Article  Google Scholar

  29. Liu Y, Cao D, Ma L, Jin X, Yang P, Ye F, Liu P, Gong Z, Wei C (2018) TMT-based quantitative proteomics analysis reveals the response of tea plant (Camellia sinensis) to fluoride. J Proteomics 176:71–81. https://doi.org/10.1016/j.jprot.2018.02.001

    CAS  Article  PubMed  Google Scholar

  30. Louback E, Pereira TAR, Souza RS, Oliveira JA, Silva LC (2016) Vegetation damage in the vicinity of an aluminum smelter in Brazil. Ecol Indic 64:193–203. https://doi.org/10.1016/j.ecolind.2016.02.044

    CAS  Article  Google Scholar

  31. Maxwell K, Johnson G (2000) Chlorophyll fluorescence a practical guide. J Exp Bot 51:659–668. https://doi.org/10.1093/jexbot/51.345.659

    CAS  Article  PubMed  PubMed Central  Google Scholar

  32. Mesquita GL, Ossamu Tanaka FA, Cantarella H, Mattos D (2011) Atmospheric absorption fluoride by cultivated species: leaf structural changes and plant growth. Water Air Soil Pollut 219(1):143–156. https://doi.org/10.1007/s11270-010-0694-4

    CAS  Article  Google Scholar

  33. Müller A, Österlund H, Marsalek J, Viklander M (2020) The pollution conveyed by urban runoff: a review of sources. Sci Total Environ 709:136125. https://doi.org/10.1016/j.scitotenv.2019.136125

    CAS  Article  PubMed  Google Scholar

  34. O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue. Protoplasma 59:368–373. https://doi.org/10.1007/BF01248568

    CAS  Article  Google Scholar

  35. Panda D (2015) Fluoride toxicity stress: physiological and biochemical consequences on plants. Int J Bioresour Environ Agric Sci 1:70–84

    Google Scholar

  36. Peng C-Y, Xu X-F, Ren Y-F, Niu H-L, Yang Y-Q, Hou R-Y, Wan X-C, Cai H-M (2020) Fluoride absorption, transportation and tolerance mechanism in Camellia sinensis, and its bioavailability and health risk assessment: a systematic review. J Sci Food Agric. https://doi.org/10.1002/jsfa.10640

    Article  PubMed  Google Scholar

  37. Rahman ZU, Khan B, Ahmada I, Mian IA, Saeed A, Afaq A, Khan A, Smith P, Mianh AA (2018) A review of groundwater fluoride contamination in Pakistan and an assessment of the risk of fluorosis. Fluoride 51(2):171–181

    CAS  Google Scholar

  38. Rodrigues AA, Vasconcelos-Filho SC, Mendes GC, Rehn LS, Rodrigues DA, Rodrigues CL, Müller C (2017) Fluoride in simulated rain affects the morphoanatomy and physiology of Eugenia dysenterica (Mart.) DC. Ecol Indic 82:189–195. https://doi.org/10.1016/j.ecolind.2017.07.005

    CAS  Article  Google Scholar

  39. Rodrigues DA, Vasconcelos-Filhos SC, Rodrigues AA, Müller C, Farnese FS, Costa AC, Teles EMG, Rodrigues CL (2018) Byrsonima basiloba as a bioindicator of simulated air pollutants: morphoanatomical and physiological changes in response to potassium fluoride. Ecol Indic 89:301–308. https://doi.org/10.1016/j.ecolind.2018.02.019

    CAS  Article  Google Scholar

  40. Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916. https://doi.org/10.1104/pp.15.01935

    CAS  Article  PubMed  PubMed Central  Google Scholar

  41. Saini P, Khan S, Baunthiyal M, Sharma V (2012) Organ-wise accumulation of fluoride in Prosopis juliflora and its potential for phytoremediation of fluoride contaminated soil. Chemosphere 89:633–635. https://doi.org/10.1016/j.chemosphere.2012.05.034

    CAS  Article  PubMed  Google Scholar

  42. Sales CRG, Marchiori PER, Machado RS, Fontenele AV, Machado EC, Silveira JAG, Ribeiro RV (2013) Photosynthetic and antioxidant responses to drought during the sugarcane ripening. Photosynthetica 53(4):547–554. https://doi.org/10.1007/s11099-015-0146-x

    CAS  Article  Google Scholar

  43. Sant’Anna-Santos BF, Azevedo AA, Alves TG, Campos NV, Oliva MA, Valente VMM (2014) Effects of emissions from an aluminium smelter in a tree tropical species sensitive to fluoride. Water Air Soil Pollut 225:1817. https://doi.org/10.1007/s11270-013-1817-

    Article  Google Scholar

  44. Santos APM, Segura-Muñoz SI, Nadal M, Schuhmacher M, Domingo JL, Martinez CA, Magasso Takayanagui AM (2015) Traffic-related air pollution biomonitoring with Tradescantia pallida (Rose) Hunt. cv. Purpurea. Boom in Brazil. Environ Monit Assess. https://doi.org/10.1007/s10661-014-4234-3

    Article  PubMed  Google Scholar

  45. Santos PS, Freitas LS, Santana JGS, Muniz EN, Rabani ARC, Silva AVC (2017) Genetic diversity and the quality of Mangabeira tree fruits (Hancornia speciosa Gomes – Apocynaceae), a native species from Brazil. Sci Hortic 226:372–378. https://doi.org/10.1016/j.scienta.2017.09.008

    Article  Google Scholar

  46. Santos-Díaz MS, Zamora-Pedraza C (2010) Fluoride removal from water by plant species that are tolerant and highly tolerant to hydrogen fluoride. Fluoride 43(2):150–156

    Google Scholar

  47. Scandalios JG (1993) Oxygen stress and superoxide dismutases. Plant Physiol 101:7–12. https://doi.org/10.1104/pp.101.1.7

    CAS  Article  PubMed  PubMed Central  Google Scholar

  48. Singh-Rawal P, Jajoo A, Bharti S (2010) Fluoride affects distribution of absorbed excitation energy more in favour of photosystem 1. Plant Biol 54:556–560. https://doi.org/10.1007/s10535-010-0099-7

    CAS  Article  Google Scholar

  49. Singh G, Kumari B, Sinam G, Kriti K, Kumar N, Mallick S (2018) Fluoride distribution and contamination in the water, soil and plants continuum and its remedial technologies, an Indian perspective– a review. Environ Pollut 239:95–108. https://doi.org/10.1016/j.envpol.2018.04.002

    CAS  Article  PubMed  Google Scholar

  50. Smith FA, Hodge HC (1979) Airborne fluorides and man: part I. Crit Rev Environ Control 8:293–371

    Article  Google Scholar

  51. Tropicos (2020) Missouri botanical garden. Tropicos.org. https://legacy.tropicos.org/Name/1800808?tab=specimens&langid=12. Accessed 08 Feb 2020

  52. Vaughn K, Duke SO (1984) Function of polyphenol oxidase in higher plants. Phys Plant 60:106–112. https://doi.org/10.1111/j.1399-3054.1984.tb04258

    CAS  Article  Google Scholar

  53. Walna B, Kuzyca I, Bednorz E, Kolendowicz L (2014) Fluoride pollution from atmospheric precipitation and its relation to air circulation and weather patterns (Wielkopolski National Park, Poland). Environ Monit Avaliar 185:5497–5514. https://doi.org/10.1007/s10661-012-2962-9

    CAS  Article  Google Scholar

  54. Weinstein LH (1977) Fluoride and plant life. J Occup Med 19:49–78. https://doi.org/10.1097/00043764-197701000-00005

    CAS  Article  PubMed  Google Scholar

  55. Weinstein LH, Davison A (2004) Fluorides in the environment: effects on plants and animals. CABI Publishing, Oxford, p 287. https://doi.org/10.1079/9780851996837.0000

    Google Scholar

  56. Wen D, Zhang F, Zhang E, Wang C, Han S, Zheng Y (2013) Arsenic, fluoride and iodine in groundwater of China. J Geochem Explor 135:1–21. https://doi.org/10.1016/j.gexplo.2013.10.012

    CAS  Article  Google Scholar

  57. Zouari M, Elloumi N, Bellassoued K, Ben Ahmed C, Krayem M, Delmail D, Elfeki A, Ben Abdallah F, Labrousse P (2017) Enzymatic antioxidant responses and mineral status in roots and leaves of olive plants subject to fluoride stress. S Afr J Bot 111:44–49. https://doi.org/10.1016/j.sajb.2017.03.039

    CAS  Article  Google Scholar

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Acknowledgements

The authors would like to thank the Goiano Federal Institute of Education, Science and Technology (IFGoiano-RV) for financial support. DA Rodrigues (n. 1524842/2015) and C Müller (n. 88887.352933/2019-00) are grateful to the Coordination for the Improvement of Higher Education Personnel (CAPES), and AA Rodrigues to the National Council for Scientific and Technological Development (CNPq-PDJ; n. 151023/2018-2) for fellowships.