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Traits Driving Tolerance to Atmospheric Fluoride Pollution in Tree Crops

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Abstract

Increased emissions of fluoride into the atmosphere contribute to reducing the sustainability of agricultural systems worldwide. In order to improve the understanding of the factors behind such phenomenon, varieties of citrus (Citrus spp.), Valencia sweet-orange, Ponkan mandarin, and Lisbon lemon and coffee (Coffea spp.), Obatã, Catuai, and Apoatã, were treated with fluoride nebulization. The trees were exposed to nebulization for 60 min inside a chamber by using medium (0.04 mol L−1) and high (0.16 mol L−1) doses of fluoridic acid (HF) during three nonconsecutive days in a single week, for a total of 26 days of exposure during the experiment. Sixty days after beginning nebulization, we evaluated leaf gas exchange, (ultra)structural organization, tree growth, and fluoride and nutrient concentrations in plant tissue. Photosynthesis and leaf dry mass of citrus and coffee varieties were affected differently by fluoride toxicity, and based on the tolerance index (relative leaf dry mass of control versus leaf dry mass of trees treated with 0.16 mol L−1 HF), the order of sensitivity for the varieties of each species was as follows: for citrus, lemon > mandarin > sweet-orange; and for coffee, Apoatã > Catuaí > Obatã. The ability of the trees to control fluoride absorption most likely explained this contrast in sensitivity among varieties because both photosynthesis and leaf growth were negatively correlated with leaf fluoride concentration. Although disorganization of the thylakoids, degeneration of vascular cells, and disruption of the middle lamella occurred in leaves of all varieties exposed to fluoride, the more severe damage was observed in those with greater sensitivity to the pollutant (i.e., lemon and Apoatã coffee). Taken together, these results provided insights into the factors that explain poor performance of citrus and coffee trees under fluoride pollution and also revealed the traits driving the tolerance of these crops such a limiting condition, which included a combination of the following: (i) reduced fluoride absorption, (ii) increased photosynthesis, and (iii) improved maintenance of the ultrastructural organization of leaves.

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References

  • Alloway, B. J., & Ayres, D. C. (1998). Chemical principles of environmental pollution. UK: Stanlet Thorns Publishers.

    Google Scholar 

  • Bataglia, O. C., Furlani, A. M. C., Teixiera, J. P. F., Furlani, P. R., & Gallo, J. R. (1983). Métodos de Análise Químicas de Plantas. Campinas: Instituto Agronômico. 48p.

    Google Scholar 

  • Bilger, W., Shreiber, U., & Bock, M. (1995). Determination of the quantum efficiency of photosystem II and non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia, 102, 425–432.

    Article  Google Scholar 

  • Bustamante, M., Oliva, M. A., Sant’anna-Santos, R., & Lopes, N. F. (1993). Sensibilidade da soja ao flúor. Brazilian Journal of Plant Physiology, 5, 151–157.

    CAS  Google Scholar 

  • Camargo, O.A., Moniz, A.C., Jorge, J.A., Valadares, J.M.A.S. (1986). Métodos de análise química, mineralógica e física do Instituto Agronômico de Campinas. Campinas: Instituto Agronômico, 94p. (IAC. Boletim Técnico, 106).

  • Coulter, C. T., Pack, M. R., & Ssulzbach, C. W. (1985). An evaluation of the dose–response relationship of fluoride injury to Gladiolus. Atmospheric Environment, 19, 1001–1007.

    Article  CAS  Google Scholar 

  • Cronin, S. J., Manoharan, V., Hedley, M. J., & Loganathan, P. (2001). Fluoride: a review of its fate, bioavailability, and risks of fluorosis in grazed-pasture systems in New Zealand. New Zealand Journal Agricultural Research, 43, 295–321.

    Article  Google Scholar 

  • Doley, D. (1988). Fluoride-induced enhancement and inhibition of photosynthesis in four taxa of Pinus. New Phytologist, 110, 21–31.

    Article  CAS  Google Scholar 

  • Doley, D., & Rossato, L. (2012). Modelling visible foliar injury effects on canopy photosynthesis and potential crop yield losses resulting from fluoride exposure. Journal Environmental Protection, 3, 979–988.

    Article  CAS  Google Scholar 

  • Domingues, R. R., Mesquita, G. L., Cantarella, H., & Mattos, D., Jr. (2011). Suscetibilidade do capim-colonião e de cultivares de milho ao flúor. Bragantia, 71, 729–736.

    Google Scholar 

  • Façanha, A. R., & de Meis, L. (1995). Inhibition of maize root H+-ATPase by fluoride and fluoroaluminate complexes. Plant Physiology, 108, 241–246.

    Article  Google Scholar 

  • Fares, S., Park, J.-H., Ormeno, E., Gentner, D. R., McKay, M., Loreto, F., Karlik, J., & Goldstein, A. H. (2010). Ozone uptake by citrus trees exposed to a range of ozone concentrations. Atmospheric Environment, 44, 3404–3412.

    Article  CAS  Google Scholar 

  • Fornasiero, R. B. (2003). Fluorides effects on Hypericum perforatum plants: first field observations. Plant Science, 165, 507–513.

    Article  CAS  Google Scholar 

  • Frankenberger Jr., W.T., Tabatabai, M.A., Adricano, D.C., Doner, H.E. (1996). Bromine, chlorine, and fluorine. p.833-867. In: Bingham, J.M. (Ed.). Methods of Soil Analysis. Part 3. Chemical Methods. Madison: Soil Science Society of America. 139 p. (SSSA Book Series, 5).

  • Garrec, J. P., & Chopin, S. (1982). Calcium accumulation in relation to fluoride pollution in plants. Fluoride, 15, 144–149.

    CAS  Google Scholar 

  • Hippler, F. W. R., Cipriano, D. O., Boaretto, R. M., Quaggio, J. A., Gaziola, S. A., Azevedo, R. A., & Mattos-Jr, D. (2016). Citrus rootstocks regulate the nutritional status and antioxidant system of trees under copper stress. Environmental and Experimental Botany, 130, 42–52.

    Article  CAS  Google Scholar 

  • Jadhav, S. V., Bringas, E., Yadav, G. D., Rathod, V. K., Ortiz, I., & Marathe, K. V. (2015). Arsenic and fluoride contaminated groundwaters: a review of current technologies for contaminants removal. Journal of Environmental Management, 162, 306–325.

    Article  CAS  Google Scholar 

  • Jha, S. K., Nayak, A. K., Sharma, Y. K., Mishra, V. K., & Sharma, D. K. (2008). Fluoride accumulation in soil and vegetation in the vicinity of Brick Fields. Bulletin of Environmental Contamination and Toxicology, 80, 369–373.

    Article  CAS  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. Biologia Plantarum, 55, 563–566.

    Article  CAS  Google Scholar 

  • Lopez-Climent, M. F., Arbona, V., Perez-Clemente, R. M., Zandalinas, P. S. I., & Gomez-Cadenas, A. G. (2014). Effect of cadmium and calcium treatments on phytochelatin and glutathione levels in citrus plants. Plant Biology, 16, 79–87.

    Article  CAS  Google Scholar 

  • Mesquita, G. L., Tanaka, F. A. O., Cantarella, H., & Mattos, D., Jr. (2011). Atmospheric absorption of fluoride by cultivated species. Leaf structural changes and plant growth. Water, Air, and Soil Pollution, 219, 143–156.

    Article  CAS  Google Scholar 

  • Mesquita, G. L., Machado, E. C., Machado, R., Cantarella, H., & Mattos, D., Jr. (2013). Fluoride exposure compromises gas exchange of plants. American Jounal of Plant Sciences, 4, 16–20.

    Article  Google Scholar 

  • Mesquita, G. L., Zambrosi, F. C. B., Tanaka, F. A. O., Boaretto, R. M., Quaggio, J. A., Ribeiro, R. V., & Mattos-Jr, D. (2016). Anatomical and physiological responses of citrus trees to varying boron availability are dependent on rootstock. Frontiers in Plant Science, 7, 224.

    Article  Google Scholar 

  • Miller, G. W. (1993). The effect of fluoride on higher plants. Fluoride, 26, 3–22.

    CAS  Google Scholar 

  • Momen, B., Anderson, P. D., Houpis, J. L. J., & Helms, J. A. (2002). Growth of ponderosa pine seedlings as affected by air pollution. Atmospheric Environment, 36, 1875–82.

    Article  CAS  Google Scholar 

  • Nilsson, T., & Braden, R. (1983). Kinetic study of the interaction between ribulosebisphosphate/carboxylase/oxigenase and inorganic fluoride. Biochemistry, 22, 1641–1645.

    Article  CAS  Google Scholar 

  • Ozsvath, D. L. (2009). Fluoride and environmental health: a review. Reviews in Environmental Science and Bio/Technology, 8, 59–79.

    Article  CAS  Google Scholar 

  • Parry, M. A. J., Schmidt, C. N. G., & Gutteridge, S. (1984). Inhibition of ribulose-P2 carboxylas/oxigenase by fluoride. Journal of Experimental Botany, 35, 161–198.

    Google Scholar 

  • Rennenberg, H., Herschbach, C., & Polle, A. (1996). Consequences of air pollution on shoot-root interactions. Journal of Plant Physiology, 148, 296–301.

    Article  CAS  Google Scholar 

  • Reynolds, E. S. (1963). The use of lead citrate at high pH an electron opaque stain in electron. The Journal of Cell Biology, 17, 208–212.

    Article  CAS  Google Scholar 

  • Ribeiro, R. V., Machado, E. C., Habermann, G., Santos, M. G., & Oliveira, R. F. (2012). Seasonal effects on the relationship between photosynthesis and leaf carbohydrates in orange trees. Functional Plant Biology, 39, 471–480.

    Article  CAS  Google Scholar 

  • Roháček, K. (2002). Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica, 40, 13–29.

    Article  Google Scholar 

  • Ruan, J., Ma, L., Shi, Y., & Han, W. (2004). The impact of pH and calcium on the uptake of fluoride by tea plants (Camellia sinensis L.). Annals of Botany, 93, 97–105.

    Article  CAS  Google Scholar 

  • Saborit, J. M. D. (2009). Effects of air pollution on citrus. Tree and Forestry Science and Biotechnology, 1, 92–104.

    Google Scholar 

  • Sant’anna-Santos, B. F., Silva, L. C., Azevedo, A. A., Araújo, J. M., Alves, E. F., Silva, E. A. M., & Aguiar, R. (2006). Effects of simulated acid rain on the foliar micromorphology and anatomy of three tropical species. Environmental and Experimental Botany, 58, 158–168.

    Article  Google Scholar 

  • Sant’Anna-Santos, B. F., Azevedo, A. A., Alves, T. G., Campos, N. V., Oliva, M. A., & Valente, V. M. M. (2014). Effects of emissions from an aluminum smelter in a tree tropical species sensitive to fluoride. Water, Air, and Soil Pollution, 225, 1817–1832.

    Article  Google Scholar 

  • Singh, M., & Verma, K. K. (2013). Influence of fluoride-contaminated irrigation water on physiological responses of popular seedlings (Populus deltoides L. Clones-S7C15). Fluoride, 46, 83–89.

    CAS  Google Scholar 

  • Soda, C., Bussotti, F., GrossoniI, P., Barnes, J., Mori, B., & Tani, C. (2000). Impacts of urban levels of ozone on Pinus halepensis foliage. Environmental and Experimental Botany, 44, 69–82.

    Article  CAS  Google Scholar 

  • Supharungsun, S., & Wainwright, M. (1982). Determination, distribution, and absorption of fluoride in atmospheric-polluted soils. Bulletin of Environmental Contamination and Toxicology, 28, 632–636.

    Article  CAS  Google Scholar 

  • van Raij, B., Andrade, J. C., Cantarella, H., & Quaggio, J. A. (2001). Análise química para avaliação da fertilidade de solos tropicais (p. 285). Campinas: Instituto Agronômico.

    Google Scholar 

  • Vike, E. (1999). Air-pollutant dispersal patterns and vegetation damage in the vicinity of three aluminum smelters in Norway. Science of the Total Environment, 236, 75–90.

    Article  CAS  Google Scholar 

  • Wei, L., & Miller, G. W. (1972). Effect of HF on the fine structure of mesophyll cells from Glycine max Merril. Fluoride, 5, 67–72.

    CAS  Google Scholar 

  • Weinstein, L. H., & Davison, A. (2004). Fluoride in the environment. London: Cabi. 287p.

    Google Scholar 

  • Woltz, S. S., Waters, W. E., & Leonard, D. C. (1971). Effects of fluorids on metabolism and visible injury in cut flowers crops an citrus. Fluoride of Official Quaterly Journal of International Society for Fluoride Research, 4, 30.

    CAS  Google Scholar 

  • Zambrosi, F. C. B., Mesquita, G. L., Tanaka, F. A. O., Quaggio, J. A., & Mattos-Jr, D. (2013). Phosphorus availability and rootstock affect copper-induced damage to the root ultra-structure of Citrus. Environmental and Experimental Botany, 95, 25–33.

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Acknowledgments

This research was possible with support from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Proc. 2008/52557-0 and 2008/09541-6). The authors also thank Dr. Oliveiro Guerreiro (Instituto Agronômico) for assisting on the selection of coffee varieties of interest for this study.

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Correspondence to Geisa Lima Mesquita.

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Mesquita, G.L., Mattos, D., Tanaka, F.A.O. et al. Traits Driving Tolerance to Atmospheric Fluoride Pollution in Tree Crops. Water Air Soil Pollut 227, 420 (2016). https://doi.org/10.1007/s11270-016-3115-5

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  • DOI: https://doi.org/10.1007/s11270-016-3115-5

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