Understanding calcium functionality by examining growth characteristics and structural aspects in calcium-deficient grapevine
de Bang, T. C., Husted, S., Laursen, K. H., Persson, D. P. & Schjoerring, J. K. The molecular-physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants. New Phytol. 229, 2446–2469 (2021).PubMed
 Google Scholar 
 White, P. J. & Brown, P. H. Plant nutrition for sustainable development and global health. Ann. Bot. 105, 1073–1080 (2010).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Hirschi, K. D. The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol. 136, 2438–2444 (2004).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Hepler, P. K. Calcium: A central regulator of plant growth and development. Plant Cell 17, 2142–2155 (2005).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Marschner, H. Mineral Nutrition of Higher Plants (Academic Press, 2011).
 Google Scholar 
 Jones, R. J. W. & Lunt, O. R. The function of calcium in plants. Bot. Rev. 33, 407–426 (1967).CAS 
 Google Scholar 
 White, P. J. & Broadley, M. R. Calcium in plants. Ann. Bot. 92, 487–511 (2003).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Spehar, C. R. & Galwey, N. W. Screening soya beans [Glycine max (L.) Merill] for calcium efficiency by root growth in low-Ca nutrient solution. Euphytica 94, 113–117 (1997).
 Google Scholar 
 Schulte-Baukloh, C. & Fromm, J. The effect of calcium starvation on assimilate partitioning and mineral distribution of the phloem. J. Exp. Bot. 44, 1703–1707 (1993).CAS 
 Google Scholar 
 Duan, S. et al. Differential regulation of enzyme activities and physio-anatomical aspects of calcium nutrition in grapevine. Sci. Hortic. 272, 109423 (2020).CAS 
 Google Scholar 
 Bondada, B. & Syvertsen, J. P. Leaf chlorophyll, net gas exchange, and chloroplast ultrastructure in citrus leaves of different nitrogen status. Tree Physiol. 23, 553–559 (2003).CAS 
 PubMed 
 Google Scholar 
 Wind, C., Arend, M. & Fromm, J. Potassium-dependent cambial growth in poplar. Plant Biol. 6, 30–37 (2004).CAS 
 PubMed 
 Google Scholar 
 Kirkby, E. A. & Pilbeam, D. J. Calcium as a plant nutrient. Plant Cell Environ. 7, 397–405 (1984).CAS 
 Google Scholar 
 Song, W.-P., Chen, W., Yi, J.-W., Wang, H.-C. & Huang, X.-M. Ca distribution pattern in Litchi fruit and pedicel and impact of Ca channel inhibitor, La3+. Front. Plant Sci. 8, 2228. https://doi.org/10.3389/fpls.2017.02228 (2018).Article 
 PubMed 
 PubMed Central 
 Google Scholar 
 Conn, S. & Gilliham, M. Comparative physiology of elemental distributions in plants. Ann. Bot. 105, 1081–1102 (2010).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Broadley, M. R. et al. Variation in the shoot calcium content of angiosperms. J. Exp. Bot. 54, 1431–1446 (2003).CAS 
 PubMed 
 Google Scholar 
 Shikanai, Y. et al. Arabidopsis thaliana PRL1 is involved in low-calcium tolerance. Soil Sci. Plant Nutr. 61, 951–956 (2015).CAS 
 Google Scholar 
 Burstrom, H. G. Calcium and plant growth. Biol. Rev. 43, 287–316 (1968).CAS 
 Google Scholar 
 Hecht-Buchholz, Ch. Calcium deficiency and plant ultrastructure. Commun. Soil Sci. Plant Anal. 10, 67–81 (1979).CAS 
 Google Scholar 
 Fink, S. D. The micromorphological distribution of bound calcium in needles of Norway spruce [Picea abies (L.) Karst.]. New Phytol. 119, 33–40 (1991).CAS 
 PubMed 
 Google Scholar 
 Skok, J. Effect of the form of the available nitrogen on the calcium deficiency symptoms in the bean plant. Plant Physiol. 16, 145–157 (1941).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 de Aguiar Santiago, F. L., Santiago, F. E. M., Filho, J. F. L. & Ratke, R. F. Plant growth and symptomatology of macronutrient deficiencies in cowpea plants. Comun. Sci. 9, 503–508 (2018).
 Google Scholar 
 Gao, H., Wu, X., Zorrilla, C., Vega, S. E. & Palta, J. P. Fractionating of calcium in tuber and leaf tissues explains the calcium deficiency symptoms in potato plant overexpressing CAX1. Front. Plant Sci. 10, 1793. https://doi.org/10.3389/fpls.2019.01793 (2020).Article 
 PubMed 
 PubMed Central 
 Google Scholar 
 Chapman, H. D. Calcium. In Diagnostic Criteria for Plants and Soil (ed. Chapman, H. D.) 65–93 (University of California Press, 1966).
 Google Scholar 
 Bondada, B., Harbertson, E., Shrestha, P. M. & Keller, M. Temporal extension of ripening beyond its physiological limits imposes physical and osmotic challenges perturbing metabolism in grape (Vitis vinifera L.) berries. Sci. Hortic. 219, 135–143 (2017).CAS 
 Google Scholar 
 Robertson, D. Modulating plant calcium for better nutrition and stress tolerance. ISRN Bot. 2013, 952043 (2013).
 Google Scholar 
 Martins, T. V., Evans, M. J., Woolfenden, H. C. & Morris, R. J. Towards the physics of calcium signaling in plants. Plants 2, 541–588 (2013).CAS 
 PubMed 
 Google Scholar 
 Gupta, B. L. & Hall, T. A. Electron probe X-ray analysis of calcium. Ann. N.Y. Acad. Sci. 307, 28–51 (1978).CAS 
 ADS 
 Google Scholar 
 Ramalho, J. C., Rebelo, M. C., Santos, M. E., Antunes, M. L. & Nunes, M. A. Effects of calcium deficiency on Coffea arabica. Nutrient changes and correlation of calcium levels with some photosynthetic parameters. Plant Soil 172, 87–96 (1995).
 Google Scholar 
 Liu, Y., Riaz, M., Yan, L., Zeng, Y. & Cuncang, J. Boron and calcium deficiency disturbing the growth of trifoliate rootstock seedlings (Poncirus trifoliate L.) by changing root architecture and cell wall. Plant Physiol. Biochem. 144, 345–354 (2019).CAS 
 PubMed 
 Google Scholar 
 Bondada, B., Oosterhuis, D. M., Wullschleger, S. D., Kim, K. S. & Harris, W. H. Anatomical considerations related to photosynthesis in cotton (Gossypium hirsutum L.) leaves, bracts, and the capsule wall. J. Exp. Bot. 270, 111–118 (1994).
 Google Scholar 
 Bondada, B. & Syvertsen, J. P. Concurrent changes in net CO2 assimilation and chloroplast ultrastructure in nitrogen deficient citrus leaves. Environ. Exp. Bot. 54, 41–48 (2005).CAS 
 Google Scholar 
 Atkinson, C. J., Mansfield, T. A., Kean, A. M. & Davies, W. J. Control of stomatal aperture by calcium in isolated epidermal tissue and whole leaves of Commelina communis L. New Phytol. 111, 9–17 (1989).CAS 
 Google Scholar 
 Martinez, H. E. P. et al. Leaf and stem anatomy of cherry tomato under calcium and magnesium deficiencies. Braz. Arch. Biol. Technol. 63, e20180670 (2020).CAS 
 Google Scholar 
 Bondada, B. Anomalies in structure, growth characteristics, and nutritional composition as induced by 2, 4-D drift phytotoxicity in grapevine (Vitis vinifera L.) leaves and clusters. J. Am. Soc. Hortic. Sci. 136, 165–176 (2011).CAS 
 Google Scholar 
 Bondada, B. Micromorpho-anatomical examination of 2, 4-D phytotoxicity in grapevine (Vitis vinifera L.) leaves. J. Plant Growth Regul. 30, 185–198 (2011).CAS 
 Google Scholar 
 Finger, A. T., de Bastos, A. A., Ferrarese-Filho, O. & Lucio, F. M. L. Role of calcium on phenolic compounds and enzymes related to lignification in soybean (Glycine max L.) root growth. Plant Growth Regul. 49, 69–76 (2006).
 Google Scholar 
 Davis, D. E. Some effects of calcium deficiency on the anatomy of Pinus taeda. Am. J. Bot. 36, 276–282 (1949).CAS 
 Google Scholar 
 Nightingale, G. T., Addoms, R. M., Robbins, W. R. & Schemerhorn, L. G. Effect of calcium deficiency on nitrate absorption and on metabolism in tomato. Plant Physiol. 6, 605–630 (1931).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Day, D. Some chemical aspects of calcium deficiency effects on Pisum sativum. Plant Physiol. 10, 811–816 (1935).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Lautner, S. & Fromm, J. Calcium-dependent physiological processes in trees. Plant Biol. 12, 268–274 (2010).CAS 
 PubMed 
 Google Scholar 
 Fromm, J. Wood formation in trees in relation to calcium and potassium nutrition. Tree Physiol. 30, 1140–1147 (2010).CAS 
 PubMed 
 Google Scholar 
 Bondada, B. Technical Advance: Novel, simple, fast, and safe approaches to visualizing fine cellular structures in free-hand sections of stem, leaf, and fruit using optical microscopy. Curr. Bot. 3, 11–22 (2012).
 Google Scholar 
 Venning, F. D. The influence of major mineral nutrient deficiencies on growth and tissue differentiation in the hypocotyl of marglobe tomato. Phytomorphology 3, 315–326 (1953).CAS 
 Google Scholar 
 Garrison, R. The growth and development of internodes in Helianthus. Bot. Gaz. 134, 246–255 (1973).
 Google Scholar 
 Sai, J. & Johnson, C. H. Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell 14, 1279–1291 (2002).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Van Dingenen, J., Blomme, J., Gonzalez, N. & Inzé, D. Plants grow with a little help from their organelle friends. J. Exp. Bot. 67, 6267–6281 (2016).PubMed 
 Google Scholar 
 Bondada, B. & Oosterhuis, D. M. Morphometric analysis of chloroplasts of cotton leaf and fruiting organs. Biol. Plant. 47, 281–284 (2003).
 Google Scholar 
 Hall, J. D., Barr, R., Al-Abbas, A. H. & Crane, F. L. The Ultrastructure of chloroplasts in mineral-deficient maize leaves. Plant Physiol. 50, 404–409 (1972).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Larcher, W., Lütz, C., Nagele, M. & Bodner, M. Photosynthetic functioning and ultrastructure of chloroplasts in stem tissue of Fagus sylvatica. J. Plant Physiol. 132, 731–737 (1988).CAS 
 Google Scholar 
 Pfanz, H., Aschan, G., Langenfeld-Heyser, R., Wittmann, C. & Loose, M. Ecology and ecophysiology of tree stems: Corticular and wood photosynthesis. Naturwissenschaften 89, 147–162 (2002).CAS 
 PubMed 
 ADS 
 Google Scholar 
 Day, D. Some effects of calcium deficiency on Pisum sativum. Plant Physiol. 4, 493–506 (1929).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 Rangnekar, P. Effect of calcium deficiency in the carbon metabolisms in photosynthesis and respiration in tomato leaf. Plant Soil 42, 565–583 (1975).CAS 
 Google Scholar 
 Rorison, I. H. & Robinson, D. Calcium as an environmental variable. Plant Cell Environ. 7, 381–390 (1984).CAS 
 Google Scholar 
 Epstein, E. Mineral Nutrition of Plants. Principles and Perspectives (Wiley, 1972).
 Google Scholar 
 Adhikari, T., Sarkar, D., Mashayekhi, H. & Xing, B. Growth and enzymatic activity of maize (Zea mays L.) plant: Solution culture test for copper dioxide nano particles. J. Plant Nutr. 39, 99–115 (2016).CAS 
 Google Scholar 
 Wu, X. et al. Boron deficiency in trifoliate orange induces changes in pectin composition and architecture of components in root cell walls. Front. Plant Sci. 8, 1882. https://doi.org/10.3389/fpls.2017.01882 (2017).Article 
 PubMed 
 PubMed Central 
 Google Scholar 
 Lloret, P. G. & Casero, P. J. Lateral root initiation. In Plant Roots: The Hidden Half (eds Waisel, Y. et al.) 198–241 (Marcel Dekker Inc, 2002).
 Google Scholar 
 Lynch, J. P. & Brown, K. M. Topsoil foraging: An architectural adaptation of plants to low phosphorus availability. Plant Soil 237, 225–237 (2001).CAS 
 Google Scholar 
 Mazen, A. M. A., Zhang, D. & Franceschi, V. R. Calcium oxalate formation in Lemna minor L.: Physiological and ultrastructural aspects of high capacity calcium sequestration. New Phytol. 161, 435–448 (2003).
 Google Scholar 
 Xie, Z. S., Forney, C. F., Xu, W. P. & Wang, S. P. Effects of root restriction on ultrastructural variation of phloem and phloem parenchyma cells in grape berry. Hortic. Sci. 44, 1334–1339 (2009).
 Google Scholar 
 Franceschi, V. R. Calcium oxalate formation is a rapid and reversible process in Lemna minor L. Protoplasma 148, 130–139 (1989).
 Google Scholar 
 Volk, G. M., Lynch-Holm, V. J., Kostman, T. A., Goss, L. J. & Francesch, V. R. The Role of druse and raphide calcium oxalate crystals in tissue calcium regulation in Pistia stratiotes leaves. Plant Biol. 4, 34–45 (2002).CAS 
 Google Scholar 
 Cherel, I., Lefoulon, C., Boeglin, M. & Sentenac, H. Molecular mechanisms involved in plant adaptation to low K(+) availability. J. Exp. Bot. 65, 833–848 (2014).CAS 
 PubMed 
 Google Scholar 
 Poni, S. & Intrieri, C. Grapevine photosynthesis: effects linked to light radiation and leaf age. Adv. Hortic. Sci. 15, 5–15 (2001).
 Google Scholar 
 Zhu, L., Wang, S., Yang, T., Zhang, C. & Xu, W. Vine growth and nitrogen metabolism of ‘Fujiminori’ grapevines in response to root restriction. Sci. Hortic. 107, 143–149 (2006).
 Google Scholar 
 Schichnes, D., Nemson, J., Sohlberg, L. & Ruzin, S. E. Microwave protocols for paraffin microtechnique and in situ localization in plants. Microsc. Microanal. 4, 491–496 (1998).CAS 
 PubMed 
 ADS 
Google Scholar More
 