Exogenous calcium reduces boron toxicity by regulating efficient antioxidant system and boron forms in trifoliate rootstock

References

• Aebi, H. 1983. Catalase in Bergmeyer HU. (ed) Methods of enzymatic analyses Verlag nodulation of neuronal excitibality by NO. Trends in Neurosciences 25:510–517.
   Google Scholar
• Ardic, M., A. H. Sekmen, S. O. Tokur, F. Zdemir, and I. Turkan. 2009. Antioxidant responses of chickpea plants subjected to boron toxicity. Plant Biology (Stuttgart, Germany) 11 (3):328–38. doi: https://doi.org/10.1111/j.1438-8677.2008.00132.x.
   PubMed Web of Science ®Google Scholar
• Ayvaz, M., M. Avci, C. Yamaner, M. Koyuncu, A. Guven, and K. Fagerstedt. 2013. Does excess boron affect the malondialdehyde levels of potato cultivars? EurAsian Journal of Biosciences 7:47–53. doi: https://doi.org/10.5053/ejobios.2013.7.0.6.
   Google Scholar
• Beauchamp, C., and I. Fridovich. 1971. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44 (1):276–87. doi: https://doi.org/10.1016/0003-2697(71)90370-8.
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248–54. doi: https://doi.org/10.1006/abio.1976.9999.
   PubMed Web of Science ®Google Scholar
• Brown, P. H., and H. Hu. 1996. Phloem mobility of boron is species dependent: Evidence for phloem mobility in sorbitol-rich species. Annals of Botany 77 (5):497–506. doi: https://doi.org/10.1006/anbo.1996.0060.
   Web of Science ®Google Scholar
• Cai, K., D. Gao, S. Luo, R. Zeng, J. Yang, and X. Zhu. 2008. Physiological and cytological mechanisms of silicon-induced resistance in rice against blast disease. Physiologia Plantarum 134 (2):324–33. doi: https://doi.org/10.1111/j.1399-3054.2008.01140.x.
   PubMed Web of Science ®Google Scholar
• Carpena, R. O., E. Esteban, M. J. Sarro, J. Peñalosa, A. Gárate, J. J. Lucena, and P. Zornoza. 2000. Boron and calcium distribution in nitrogen-fixing pea plants. Plant Science 151 (2):163–70. doi: https://doi.org/10.1016/s0168-9452(99)00210-1.
   PubMed Web of Science ®Google Scholar
• Cartwright, B., B. A. Zarcinas, and I. A. Spouncer. 1986. Boron toxicity in South Australian barley crops. Australian Journal of Agricultural Research 37 (4):351–9. doi: https://doi.org/10.1071/AR9860351.
   Google Scholar
• Cervilla, L. M., B. Blasco, J. Rıos, L. Romero, and J. Ruiz. 2007. Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Annals of Botany 100 (4):747–56. doi: https://doi.org/10.1093/aob/mcm156.
   PubMed Web of Science ®Google Scholar
• Chen, L. S., S. Han, Y. P. Qi, and L. T. Yang. 2012. Boron stresses and tolerance in citrus. African Journal of Biotechnology 11 (22):5961–9.
   Google Scholar
• Choi, E. Y., A. Mcneill, D. Coventry, and J. Stangoulis. 2006. Whole plant response of crop and weed species to high subsoil boron. Australian Journal of Agricultural Research 57 (7):761–70. doi: https://doi.org/10.1071/AR04302.
   Google Scholar
• Dannel, F., H. Pfeffer, and V. Römheld. 1999. Distribution within the plant or compartmentation does not contribute substantially to the detoxification of excess boron in sunflower (helianthus annuus). Functional Plant Biology 26 (2):95–9. doi: https://doi.org/10.1071/PP98110.
   Google Scholar
• Du, C. W., Y. Wang, X. U. Fang, and H. Wang. 2002a. Study on boron forms and their relationship in rape cultivars with different boron efficiency. Journal of Plant Nutrition and Fertilizers 8 (1):105–9.
   Google Scholar
• Du, C. W., Y. H. Wang, F. S. Xu, Y. H. Yang, and H. Y. Wang. 2002b. Study on the physiological mechanism of boron utilization efficiency in rape cultivars. Journal of Plant Nutrition 25 (2):231–44. doi: https://doi.org/10.1081/PLN-100108832.
   Web of Science ®Google Scholar
• Fang, K., W. Zhang, Y. Xing, Q. Zhang, L. Yang, Q. Cao, and L. Qin. 2016. Boron toxicity causes multiple effects on Malus domestica pollen tube growth. Frontiers in Plant Science 7:208. doi: https://doi.org/10.3389/fpls.2016.00208.
   PubMed Web of Science ®Google Scholar
• Forner-Giner, M. A., A. Alcaide, E. Primo-Millo, and J. B. Forner. 2003. Performance of ‘Navelina’ orange on 14 rootstocks in Northern Valencia (Spain). Scientia Horticulturae 98 (3):223–32. doi: https://doi.org/10.1016/S0304-4238(02)00227-3.
   Web of Science ®Google Scholar
• Guimarães, F. V. A., C. F. de Lacerda, E. C. Marques, M. R. A. de Miranda, C. E. B. de Abreu, J. T. Prisco, and E. Gomes-Filho. 2011. Calcium can moderate changes on membrane structure and lipid composition in cowpea plants under salt stress. Plant Growth Regulation 65 (1):55–63. doi: https://doi.org/10.1007/s10725-011-9574-1.
   Web of Science ®Google Scholar
• Guo, P., Y.-P. Qi, L.-T. Yang, X. Ye, H.-X. Jiang, J.-H. Huang, and L.-S. Chen. 2014. cDNA-AFLP analysis reveals the adaptive responses of citrus to long-term boron-toxicity. BMC Plant Biology 14 (1):284. doi: https://doi.org/10.1186/s12870-014-0284-5.
   PubMedGoogle Scholar
• Heath, R. L., and L. Packer. 1968. Photoperoxidation in isolated chloroplasts I Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125 (1):189–98. doi: https://doi.org/10.1016/0003-9861(68)90654-1.
   PubMed Web of Science ®Google Scholar
• Hoagland, D. R., and D. I. Arnon. 1950. The water-culture method for growing plants without soil. Circular. California Agricultural Experiment Station 347:1–32.
   Google Scholar
• Hu, H., and P. H. Brown. 1994. Localization of boron in cell walls of squash and tobacco and its association with pectin (evidence for a structural role of boron in the cell wall). Plant Physiology 105 (2):681–9. doi: https://doi.org/10.1104/pp.105.2.681.
   PubMed Web of Science ®Google Scholar
• Huang, J. H., Z. J. Cai, S. X. Wen, P. Guo, X. Ye, G. Z. Lin, and L. S. Chen. 2014. Effects of boron toxicity on root and leaf anatomy in two citrus species differing in boron tolerance. Trees 28 (6):1653–66. doi: https://doi.org/10.1007/s00468-014-1075-1.
   Web of Science ®Google Scholar
• Huang, C., and R. D. Graham. 1990. Resistance of wheat genotypes to boron toxicity is expressed at the cellular level. Plant and Soil 126 (2):295–300. doi: https://doi.org/10.1007/BF00012832.
   Google Scholar
• Huang, J.-H., X.-J. Lin, L.-Y. Zhang, X.-D. Wang, G.-C. Fan, and L.-S. Chen. 2019. MicroRNA sequencing revealed Citrus adaptation to long-term boron toxicity through modulation of root development by miR319 and miR171. International Journal of Molecular Sciences 20 (6):1422. doi: https://doi.org/10.3390/ijms20061422.
   PubMed Web of Science ®Google Scholar
• Karabal, E., Y. Meral, and A. Ö. Hüseyin. 2003. Antioxidant responses of tolerant and sensitive barley cultivars to boron toxicity. Plant Science 164 (6):925–33. doi: https://doi.org/10.1016/S0168-9452(03)00067-0.
   Web of Science ®Google Scholar
• Kumar, K.,. K. A. Mosa, S. Chhikara, C. Musante, J. C. White, and O. P. Dhankher. 2014. Two rice plasma membrane intrinsic proteins, OsPIP2;4 and OsPIP2;7, are involved in transport and providing tolerance to boron toxicity. Planta 239 (1):187–98. doi: https://doi.org/10.1007/s00425-013-1969-y.
   PubMed Web of Science ®Google Scholar
• Lei, Y., R. Muhammad, X. W. Wu, C. Q. Du, Y. L. Liu, and C. C. Jiang. 2018. Ameliorative effects of boron on aluminum induced variations of cell wall cellulose and pectin components in trifoliate orange (Poncirus trifoliate (L.) Raf.) rootstock. Environmental Pollution (Barking, Essex: 1987) 240:764–74. doi: https://doi.org/10.1016/j.envpol.2018.05.022.
   PubMedGoogle Scholar
• Lu, X. P., C. C. Jiang, X. C. Dong, X. W. Wu, and L. Yan. 2017. Leaf photosynthetic characteristics of citrus rootstocks with different boron efficiency. Journal of Plant Nutrition and Fertilizers 23 (2):476–83.
   Google Scholar
• Matoh, T. 1997. Boron in plant cell walls. Plant and Soil 193 (2):59–70. doi: https://doi.org/10.1023/A:1004207824251.
   Web of Science ®Google Scholar
• Mosa, K. A., K. Kumar, S. Chhikara, C. Musante, J. C. White, and O. P. Dhankher. 2016. Enhanced boron tolerance in plants mediated by bidirectional transport through plasma membrane intrinsic proteins. Scientific Reports 6:21640. doi: https://doi.org/10.1038/srep21640.
   PubMedGoogle Scholar
• Nable, R. O. 1988. Resistance to boron toxicity amongst several barley and wheat cultivars: A preliminary examination of the resistance mechanism. Plant and Soil 112 (1):45–52. doi: https://doi.org/10.1007/BF02181751.
   Web of Science ®Google Scholar
• Nable, R. O., G. S. Bañuelos, and J. G. Paull. 1997. Boron toxicity. Plant and Soil 193 (2):181–98. doi: https://doi.org/10.1023/A:1004272227886.
   Web of Science ®Google Scholar
• Nakano, Y., and K. Asada. 1981. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22:867–80.
   Web of Science ®Google Scholar
• Nali, C., A. Francini, E. Pellegrini, S. Loppi, and G. Lorenzini. 2015. Visible injury CO2 assimilation and PSII photochemistry of eucaliptus plants in response to boron stress. In Plants pollutants and remediation, 1–11. Netherlands: Springer.
   Google Scholar
• Pallotta, M., T. Schnurbusch, J. Hayes, A. Hay, U. Baumann, J. Paull, P. Langridge, and T. Sutton. 2014. Molecular basis of adaptation to high soil boron in wheat landraces and elite cultivars. Nature 514 (7520):88–91. doi: https://doi.org/10.1038/nature13538.
   PubMed Web of Science ®Google Scholar
• Pang, Y., L. Li, F. Ren, P. Lu, P. Wei, J. Cai, L. Xin, J. Zhang, J. Chen, and X. Wang. 2010. Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in arabidopsis. Journal of Genetics and Genomics = Yi Chuan Xue Bao 37 (6):389–97. doi: https://doi.org/10.1016/S1673-8527(09)60057-6.
   PubMed Web of Science ®Google Scholar
• Papadakis, I. E., K. N. Dimassi, I. N. Therios, I. E. Papadakis, K. N. Dimassi, and I. N. Therios. 2003. Response of two citrus genotypes to six boron concentrations: Concentration and distribution of nutrients total absorption and nutrient use efficiency. Australian Journal of Agricultural Research 54 (6):571–80. doi: https://doi.org/10.1071/AR02163.
   Google Scholar
• Peng, G., Q. Yiping, Y. Lintong, Y. Xin, H. Jinghao, and C. Lisong. 2016. Long-term boron-excess-induced alterations of gene profiles in roots of two citrus species differing in boron-tolerance revealed by cDNA-AFLP. Frontiers in Plant Science 7:898.
   PubMedGoogle Scholar
• Piñero, M. C., M. Pérez-Jiménez, J. López-Marín, and F. M. D. Amor. 2017. Amelioration of boron toxicity in sweet pepper as affected by calcium management under an elevated CO2 concentration. Environmental Science and Pollution Research International 24 (11):10893–9. doi: https://doi.org/10.1007/s11356-017-8742-x.
   PubMed Web of Science ®Google Scholar
• Rámila, C. D. P., S. A. Contreras, C. Di Domenico, M. A. Molina-Montenegro, A. Vega, M. Handford, C. A. Bonilla, and G. E. Pizarro. 2016. Boron stress response and accumulation potential of the extremely tolerant species Puccinellia frigida. Journal of Hazardous Materials 317:476–84. doi: https://doi.org/10.1016/j.jhazmat.2016.05.086.
   PubMed Web of Science ®Google Scholar
• Ramón, A. M., R. O. Carpenaruiz, A. Gárate, and M. L. V. Beusichem. 1990. The effects of short-term deficiency of boron on potassium calcium and magnesium distribution in leaves and roots of tomato (Lycopersicon esculentum) plants. Plant Nutrition - Physiology and Applications Proceedings of the Eleventh International Plant Nutrition Colloquium. Wageningen, Netherlands, 287–90.
   Google Scholar
• Reid, R. 2007. Identification of boron transporter genes likely to be responsible for tolerance to boron toxicity in wheat and barley. Plant & Cell Physiology 48 (12):1673–8. doi: https://doi.org/10.1093/pcp/pcm159.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Serrano, M., M. C. Romero-Puertas, A. N. A. Zabalza, F. J. Corpas, M. Gomez, L. A. DEL Rio, and L. M. Sandalio. 2006. Cadmium effect on oxidative metabolism of pea (Pisum sativum l.) rootsimaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant, Cell and Environment 29 (8):1532–44. doi: https://doi.org/10.1111/j.1365-3040.2006.01531.x.
   PubMed Web of Science ®Google Scholar
• Sang, W., Z. R. Huang, L. T. Yang, P. Guo, X. Ye, and L. S. Chen. 2017. Effects of high toxic boron concentration on protein profiles in roots of two citrus species differing in boron-tolerance revealed by a 2-DE based MS approach. Frontiers in Plant Science 8:180. doi: https://doi.org/10.3389/fpls.2017.00180.
   PubMedGoogle Scholar
• Shah, A., X. Wu, A. Ullah, S. Fahad, R. Muhammad, L. Yan, and C. Jiang. 2017. Deficiency and toxicity of boron: Alterations in growth, oxidative damage and uptake by citrange orange plants. Ecotoxicology and Environmental Safety 145 (6):575–82. doi: https://doi.org/10.1016/j.ecoenv.2017.08.003.
   PubMedGoogle Scholar
• Shuang, H., T. Ning, J. Huanxin, Y. Lintong, L. Yan, and C. Jiang. 2009. CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to boron stress. Plant Science 176:143–153.
   Web of Science ®Google Scholar
• Siddiqui, M. H., M. H. Al-Whaibi, A. M. Sakran, H. M. Ali, M. O. Basalah, M. Faisal, A. Alatar, and A. A. Al-Amri. 2013. Calcium-induced amelioration of boron toxicity in radish. Journal of Plant Growth Regulation 32 (1):61–71. doi: https://doi.org/10.1007/s00344-012-9276-6.
   Web of Science ®Google Scholar
• Sutton, T., U. Baumann, J. Hayes, N. C. Collins, B.-J. Shi, T. Schnurbusch, A. Hay, G. Mayo, M. Pallotta, M. Tester, et al. 2007. Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science (New York, NY) 318 (5855):1446–9. doi: https://doi.org/10.1126/science.1146853.
   Google Scholar
• Takano, J., K. Noguchi, M. Yasumori, M. Kobayashi, Z. Gajdos, K. Miwa, H. Hayashi, T. Yoneyama, and T. Fujiwara. 2002. Arabidopsis boron transporter for xylem loading. Nature 420 (6913):337–400.
   PubMed Web of Science ®Google Scholar
• Tanaka, M., and T. Fujiwara. 2008. Physiological roles and transport mechanisms of boron: Perspectives from plants. Pflugers Archiv: European Journal of Physiology 456 (4):671–7. doi: https://doi.org/10.1007/s00424-007-0370-8.
   PubMed Web of Science ®Google Scholar
• Tombuloglu, H., N. Semizoglu, S. Sakcali, and G. Kekec. 2012. Boron induced expression of some stress-related genes in tomato. Chemosphere 86 (5):433–8. doi: https://doi.org/10.1016/j.chemosphere.2011.09.035.
   PubMed Web of Science ®Google Scholar
• Turan, M. A., S. Taban, G. B. Kayin, and N. Taban. 2018. Effect of boron application on calcium and boron concentrations in cell wall of durum (Triticum durum) and bread (Triticum aestivum) wheat. Journal of Plant Nutrition 41 (11):1351–7. doi: https://doi.org/10.1080/01904167.2018.1450424.
   Web of Science ®Google Scholar
• Turan, M. A., N. Taban, and S. Taban. 2009. Effect of calcium on the alleviation of boron toxicity and localization of boron and calcium in cell wall of wheat. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 37 (2):99–103.
   Web of Science ®Google Scholar
• Wang, B. L., L. Shi, Y. X. Li, and W. H. Zhang. 2010. Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231 (6):1301–9. doi: https://doi.org/10.1007/s00425-010-1134-9.
   PubMedGoogle Scholar
• Wang, H. Y., Y. H. Wang, C. W. Du, F. S. Xu, and Y. H. Yang. 2003. Effects of boron and calcium supply on calcium fractionation in plants and suspension cells of rape cultivars with different boron efficiency. Journal of Plant Nutrition 26 (4):789–806. doi: https://doi.org/10.1081/PLN-120018565.
   Web of Science ®Google Scholar
• Warington, K. 1923. The effect of boric acid and borax on the broad bean and certain other plants. Annals of Botany os-37 (4):629–72. doi: https://doi.org/10.1093/oxfordjournals.aob.a089871.
   Google Scholar
• White, P. J., and M. R. Broadley. 2003. Calcium in plants. Annals of Botany 92 (4):487–511. doi: https://doi.org/10.1093/aob/mcg164.
   PubMed Web of Science ®Google Scholar
• Xu, F. S. 2002. Study on the physiological mechanism of boron utilization efficiency in rape cultivars. Journal of Plant Nutrition 25 (2):231–244.
   Google Scholar
• Yamauchi, T., T. Hara, and Y. Sonoda. 1986. Effects of boron deficiency and calcium supply on the calcium metabolism in tomato plant. Plant and Soil 93 (2):223–30. doi: https://doi.org/10.1007/BF02374224.
   Web of Science ®Google Scholar