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.
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.
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.
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.
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.
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.
Doley, D. (1988). Fluoride-induced enhancement and inhibition of photosynthesis in four taxa of Pinus. New Phytologist, 110, 21–31.
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.
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.
Façanha, A. R., & de Meis, L. (1995). Inhibition of maize root H+-ATPase by fluoride and fluoroaluminate complexes. Plant Physiology, 108, 241–246.
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.
Fornasiero, R. B. (2003). Fluorides effects on Hypericum perforatum plants: first field observations. Plant Science, 165, 507–513.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Miller, G. W. (1993). The effect of fluoride on higher plants. Fluoride, 26, 3–22.
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.
Nilsson, T., & Braden, R. (1983). Kinetic study of the interaction between ribulosebisphosphate/carboxylase/oxigenase and inorganic fluoride. Biochemistry, 22, 1641–1645.
Ozsvath, D. L. (2009). Fluoride and environmental health: a review. Reviews in Environmental Science and Bio/Technology, 8, 59–79.
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.
Rennenberg, H., Herschbach, C., & Polle, A. (1996). Consequences of air pollution on shoot-root interactions. Journal of Plant Physiology, 148, 296–301.
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.
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.
Roháček, K. (2002). Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica, 40, 13–29.
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.
Saborit, J. M. D. (2009). Effects of air pollution on citrus. Tree and Forestry Science and Biotechnology, 1, 92–104.
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.
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.
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.
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.
Supharungsun, S., & Wainwright, M. (1982). Determination, distribution, and absorption of fluoride in atmospheric-polluted soils. Bulletin of Environmental Contamination and Toxicology, 28, 632–636.
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.
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.
Wei, L., & Miller, G. W. (1972). Effect of HF on the fine structure of mesophyll cells from Glycine max Merril. Fluoride, 5, 67–72.
Weinstein, L. H., & Davison, A. (2004). Fluoride in the environment. London: Cabi. 287p.
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.
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.
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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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