Protoplasma

, Volume 247, Issue 3–4, pp 215–231

Calcium storage in plants and the implications for calcium biofortification

  • Maclin Dayod
  • Stephen Donald Tyerman
  • Roger Allen Leigh
  • Matthew Gilliham
Review Article

Abstract

Calcium (Ca) is an essential nutrient for plants and animals, with key structural and signalling roles, and its deficiency in plants can result in poor biotic and abiotic stress tolerance, reduced crop quality and yield. Likewise, low Ca intake in humans has been linked to various diseases (e.g. rickets, osteoporosis, hypertension and colorectal cancer) which can threaten quality of life and have major economic costs. Biofortification of various food crops with Ca has been suggested as a good method to enhance human intake of Ca and is advocated as an economically and environmentally advantageous strategy. Efforts to enhance Ca content of crops via transgenic means have had promising results. Overall Ca content of transgenic plants has been increased but in some cases adverse affects on plant function have been observed. This suggests that a better understanding of how Ca ions (Ca2+) are stored and transported through plants is required to maximise the effectiveness of future approaches.

Keywords

Apoplasm Apoplast Biofortification Bioavailability Calcium CAX Osteoporosis 

Abbreviations

At

Arabidopsis thaliana

Arabidopsis

Arabidopsis thaliana

Ca

Calcium

Ca2+

Calcium ion(s)

[x]

Concentration of x

CDC2a

Cell division cycle 2a gene promoter

CMV

Cauliflower mosaic virus

EDTA

Ethylenediaminetetraacetic acid

ER

Endoplasmic reticulum

PM

Plasma membrane

RDI

Recommended daily intake

References

  1. Adams P, Ho LC (1993) Effects of environment on the uptake and distribution of calcium in tomato and on the incidence of blossom-end rot. Plant Soil 154:127–132CrossRefGoogle Scholar
  2. AIHW (2010) Australian Institute of Health and Welfare. Available at: http://www.aihw.gov.au/. Accessed 18 May 2010
  3. Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffman T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057PubMedCrossRefGoogle Scholar
  4. Alleva K, Niemietz CM, Maurel C, Parisi M, Tyerman SD, Amodeo G (2006) Plasma membrane of Beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations. J Exp Bot 57:609–621Google Scholar
  5. Bachrach LK (2001) Acquisition of optimal bane mass in childhood and adolescence. Trends Endocrinol Metab 12:22–28PubMedCrossRefGoogle Scholar
  6. Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach, 2nd edn. Wiley, New YorkGoogle Scholar
  7. Barber SA, Ozanne PG (1970) Autoradiographic evidence for differential effect of 4 plant species in altering calcium content of rhizosphere soil. Soil Sci Soc Am Proc 34:635–637CrossRefGoogle Scholar
  8. Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Harper JF, Axelsen KB (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132:618–628PubMedCrossRefGoogle Scholar
  9. Baxter I, Hosmani PS, Rus A, Lahner B, Borevitz JO, Muthukumar B, Mickelbart MV, Schreiber L, Franke RB, Salt DE (2009) Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet 5:e1000492PubMedCrossRefGoogle Scholar
  10. Benson J, Geary B, Hopkins B, Jolley V, Miller J (2009) Effect of Ca on pink rot infection in potato. Phytopathol 99:S180–S180CrossRefGoogle Scholar
  11. Bhatia V (2008) Dietary calcium intake - a critical reappraisal. Indian J Med Res 127:269–273PubMedGoogle Scholar
  12. Biggs AR (1999) Effects of calcium salts on apple bitter rot caused by two Colletotrichum spp. Plant Dis 83:1001–1005CrossRefGoogle Scholar
  13. Binkley N (2009) A perspective on male osteoporosis. Best Pract Res Clin Rheumatol 23:755–768PubMedCrossRefGoogle Scholar
  14. Bonomelli C, Ruiz R (2010) Effects of foliar and soil calcium application on yield and quality of table grape cv. 'Thompson Seedless'. J Plant Nutr 33:299–314Google Scholar
  15. Bramley H, Turner NC, Turner DW, Tyerman SD (2009) Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots. Plant Physiol 150:348–364PubMedCrossRefGoogle Scholar
  16. Bramley H, Turner NC, Turner DW, Tyerman SD (2010) The contrasting influence of short-term hypoxia on the hydraulic properties of cells and roots of wheat and lupin. Func Plant Biol 37:183–193CrossRefGoogle Scholar
  17. Campanella V, Ippolito A, Nigro F (2002) Activity of calcium salts in controlling Phytophthora root rot of citrus. Crop Prot 21:751–756CrossRefGoogle Scholar
  18. Cantu D, Vicente AR, Greve LC, Dewey FM, Bennett AB, Labavitch JM, Powell ALT (2008) The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea. Proc Natl Acad Sci USA 105:859–864PubMedCrossRefGoogle Scholar
  19. Catala R, Santos E, Alonso JM, Ecker JR, Martinez-Zapater JM, Salinas J (2003) Mutations in the Ca2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940–2951PubMedCrossRefGoogle Scholar
  20. Centeno V, de Barboza GD, Marchionatti A, Rodriguez V, de Talamoni NT (2009) Molecular mechanisms triggered by low-calcium diets. Nutr Res Rev 22:163–174PubMedCrossRefGoogle Scholar
  21. Chan GM, McElligott K, McNaught T, Gill G (2006) Effects of dietary calcium intervention on adolescent mothers and newborns—a randomized controlled trial. Obstet Gynecol 108:565–571PubMedCrossRefGoogle Scholar
  22. Chan FWK, Wong SYS, Leung JCS, Leung PC, Woo J (2007) Experience of famine and bone health in post-menopausal women. Int J Epidemiol 36:1143–1150CrossRefGoogle Scholar
  23. Chang YC, Miller WB (2004) The relationship between leaf enclosure, transpiration, and upper leaf necrosis on Lilium 'Star gazer'. J Am Soc Hortic Sci 129:128–133Google Scholar
  24. Charoenkiatkul S, Kriengsinyos W, Tuntipopipat S, Suthutvoravut U, Weaver CM (2008) Calcium absorption from commonly consumed vegetables in healthy Thai women. J Food Sci 73:H218–H221PubMedCrossRefGoogle Scholar
  25. Cheng NH, Hirschi KD (2003) Cloning and characterization of CXIP1, a novel PICOT domain-containing Arabidopsis protein that associates with CAX1. J Biol Chem 278:6503–6509PubMedCrossRefGoogle Scholar
  26. Cheng NH, Pittman JK, Barkla BJ, Shigaki T, Hirschi KD (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15:347–364PubMedCrossRefGoogle Scholar
  27. Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B, Salt DE, Hirschi KD (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol 138:2048–2060PubMedCrossRefGoogle Scholar
  28. Cholewa E, Peterson CA (2004) Evidence for symplastic involvement in the radial movement of calcium in onion roots. Plant Physiol 134:1793–1802PubMedCrossRefGoogle Scholar
  29. Chung MY, Han JS, Giovannoni J, Liu Y, Kim CK, Lim KB, Chung JD (2010) Modest calcium increase in tomatoes expressing a variant of Arabidopsis cation/H+ antiporter. Plant Biotech Rep 4:15–21CrossRefGoogle Scholar
  30. Clarkson DT (1984) Calcium-transport between tissues and its distribution in the plant. Plant Cell Environ 7:449–456CrossRefGoogle Scholar
  31. Conn S, Gilliham M (2010) Comparative physiology of elemental distributions in plants. Ann Bot 105:1081–1102PubMedCrossRefGoogle Scholar
  32. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861PubMedCrossRefGoogle Scholar
  33. DeMichele DW, Sharpe PJH (1973) Analysis of mechanics of guard cell motion. J Theor Biol 41:77–96PubMedCrossRefGoogle Scholar
  34. Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404PubMedCrossRefGoogle Scholar
  35. Desilva DLR, Mansfield TA (1994) The stomatal physiology of calcicoles in relation to calcium delivered in the xylem sap. Proc Roy Soc Lond B 257:81–85CrossRefGoogle Scholar
  36. DeSilva DLR, Honour SJ, Mansfield TA (1996a) Estimations of apoplastic concentrations of K+ and Ca2+ in the vicinity of stomatal guard cells. New Phytol 134:463–469CrossRefGoogle Scholar
  37. DeSilva DLR, Hetherington AM, Mansfield TA (1996b) Where does all the calcium go? Evidence of an important regulatory role for trichomes in two calcicoles. Plant Cell Environ 19:80–886Google Scholar
  38. DeSilva DLR, Mansfield TA, McAinsh MR (2001) Changes in stomatal behaviour in the calcicole Leontodon hispidus due to the disruption by ozone of the regulation of apoplastic Ca2+ by trichomes. Planta 214:158–162CrossRefGoogle Scholar
  39. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620PubMedCrossRefGoogle Scholar
  40. Ehret DL, Menzies JG, Bogdanoff C, Utkhede RS, Frey B (2002) Foliar applications of fertilizer salts inhibit powdery mildew on tomato. Can J Plant Pathol-Rev Can Phytopathol 24:437–444CrossRefGoogle Scholar
  41. Elmer PAG, Spiers TM, Wood PN (2007) Effects of pre-harvest foliar calcium sprays on fruit calcium levels and brown rot of peaches. Crop Prot 26:11–18CrossRefGoogle Scholar
  42. Erickson RO (1986) Symplastic growth and symplasmic transport. Plant Physiol 82:1153PubMedCrossRefGoogle Scholar
  43. Faiyue B, Al-Azzawi MJ, Flowers TJ (2010a) The role of lateral roots in bypass flow in rice (Oryza sativa L.). Plant Cell Environ 33:702–716PubMedGoogle Scholar
  44. Faiyue B, Vijayalakshmi C, Nawaz S, Nagato Y, Taketa S, Ichii M, Al-Azzawi MJ, Flowers TJ (2010b) Studies on sodium bypass flow in lateral rootless mutants lrt1 and lrt2, and crown rootless mutant crl1 of rice (Oryza sativa L.). Plant Cell Environ 33:687–701PubMedGoogle Scholar
  45. Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Annu Rev Plant Biol 56:41–71PubMedCrossRefGoogle Scholar
  46. Frantz JM, Ritchie G, Cometti NN, Robinson J, Bugbee B (2004) Exploring the limits of crop productivity: beyond the limits of tipburn in lettuce. J Am Soc Hortic Sci 129:331–338PubMedGoogle Scholar
  47. Fricke W, Leigh RA, Tomos AD (1994) Concentrations of inorganic and organic solutes in extracts from individual epidermal, mesophyll and bundle-sheath cells of barley leaves. Planta 192:310–316Google Scholar
  48. Fritz E (2007) Measurement of cation exchange capacity (CEC) of plant cell walls by X-ray microanalysis (EDX) in the transmission electron microscope. Microsc Microanal 13:233–244PubMedCrossRefGoogle Scholar
  49. Galon Y, Finkler A, Fromm H (2010) Calcium regulated transcription in plants. Mol Plant. doi:10.1093/mp/ssq019 PubMedGoogle Scholar
  50. Genc Y, Humphries JM, Lyons GH, Graham RD (2005) Exploiting genotypic variation in plant nutrient accumulation to alleviate micronutrient deficiency in populations. J Trace Elem Med Biol 18:319–324PubMedCrossRefGoogle Scholar
  51. Gerasopoulos D, Chouliaras V, Lionakis S (1996) Effects of preharvest calcium chloride sprays on maturity and storability of Hayward kiwifruit. Postharvest Biol Technol 7:65–72CrossRefGoogle Scholar
  52. Gilliham M, Campbell M, Dubos C, Becker D, Davenport R (2006a) The Arabidopsis thaliana glutamate-like receptor family (AtGLR). In: Baluska F, Mancuso S, Volkmann D (eds) Communication in plants: neuronal aspects of plant life. Springer, Berlin, pp 187–204Google Scholar
  53. Gilliham M, Sullivan W, Tester M, Tyerman SD (2006b) Simultaneous flux and current measurement from single plant protoplasts reveals a strong link between K+ fluxes and current, but no link between Ca2+ fluxes and current. Plant J 46:134–144PubMedCrossRefGoogle Scholar
  54. Gomez-Galera S, Rojas E, Sudhakar D, Zhu CF, Pelacho AM, Capell T, Christou P (2010) Critical evaluation of strategies for mineral fortification of staple food crops. Transgenic Res 19:165–180PubMedCrossRefGoogle Scholar
  55. Gong HJ, Randall DP, Flowers TJ (2006) Silicon deposition in the root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow. Plant Cell Environ 29:1970–1979PubMedCrossRefGoogle Scholar
  56. Graham RD, Welch RM, Saunders DA, Ortiz-Monasterio I, Bouis HE, Bonierbale M, de Haan S, Burgos G, Thiele G, Liria R, Meisner CA, Beebe SE, Potts MJ, Kadian M, Hobbs PR, Gupta RK, Twomlow S (2007) Nutritious subsistence food systems. In: Sparks D (ed) Advances in Agronomy. Academic Press, San Diego, pp 1–74Google Scholar
  57. Greenspan MD, Shackel KA, Matthews MA (1994) Developmental changes in the diurnal water budget of the grape berry exposed to water deficits. Plant Cell Environ 17:811–820CrossRefGoogle Scholar
  58. Han JS, Park S, Shigaki T, Hirschi KD, Kim CK (2009) Improved watermelon quality using bottle gourd rootstock expressing a Ca2+/H+ antiporter. Mol Breed 24:201–211CrossRefGoogle Scholar
  59. Hartz TK, Johnstone PR, Smith RF, Cahn MD (2007) Soil calcium status unrelated to tipburn of romaine lettuce. Hortscience 42:1681–1684Google Scholar
  60. Heaney RP (1993a) Nutritional factors in osteoporosis. Annu Rev Nutr 13:287–316PubMedCrossRefGoogle Scholar
  61. Heaney RP (1993b) Thinking straight about calcium. New Engl J Med 328:503–505PubMedCrossRefGoogle Scholar
  62. Heaney RP, Bargerlux MJ (1994) Low-calcium intake - the culprit in many chronic diseases. J Dairy Sci 77:1155–1160PubMedCrossRefGoogle Scholar
  63. Heaney RP, Weaver CM, Fitzsimmons ML (1991) Soybean pytate content—effect on calcium-absorption. Am J Clin Nutr 53:745–747PubMedGoogle Scholar
  64. Heaney RP, Weaver CM, Hinders SM, Martin B, Packard PT (1993) Absorbability of calcium from Brassica vegetables—broccoli, bok-choy, and kale. J Food Sci 58:1378–1380CrossRefGoogle Scholar
  65. Heaney RP, Dowell MS, Rafferty K, Bierman J (2000) Bioavailability of the calcium in fortified soy imitation milk, with some observations on method. Am J Clin Nutr 71:1166–1169PubMedGoogle Scholar
  66. Hedfalk K, Tornroth-Horsefield S, Nyblom M, Johanson U, Kjellbom P, Neutze R (2006) Aquaporin gating. Curr Opin Struck Biol 16:447–456CrossRefGoogle Scholar
  67. Hepler PK, Winship LJ (2010) Calcium at the cell wall-cytoplast interface. J Integr Plant Biol 52:147–160PubMedCrossRefGoogle Scholar
  68. Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122PubMedCrossRefGoogle Scholar
  69. Hirschi K (2008) Nutritional improvements in plants: time to bite on biofortified foods. Trends Plant Sci 13:459–463PubMedCrossRefGoogle Scholar
  70. Hirschi KD (2009) Nutrient biofortification of food crops. Annu Rev Nutr 29:401–421PubMedCrossRefGoogle Scholar
  71. Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28:491–533PubMedCrossRefGoogle Scholar
  72. Jeong J, Guerinot ML (2008) Biofortified and bioavailable: the gold standard for plant-based diets. Proc Natl Acad Sci USA 105:1777–1778PubMedCrossRefGoogle Scholar
  73. Jiang SL, Wu JG, Feng Y, Yang XE, Shi CH (2007) Correlation analysis of mineral element contents and quality traits in milled rice (Oryza stavia L.). J Agri Food Chem 55:9608–9613CrossRefGoogle Scholar
  74. Johnstone PR, Hartz TK, May DM (2008) Calcium fertigation ineffective at increasing fruit yield and quality of muskmelon and honeydew melons in California. HortTechnology 18:685–689Google Scholar
  75. Karley AJ, Leigh RA, Sanders D (2000a) Differential ion accumulation and ion fluxes in the mesophyll and epidermis of barley. Plant Physiol 122:835–844PubMedCrossRefGoogle Scholar
  76. Karley AJ, Leigh RA, Sanders D (2000b) Where do all the ions go? The cellular basis of differential ion accumulation in leaf cells. Trends Plant Sci 5:465–470PubMedCrossRefGoogle Scholar
  77. Kelly PJ, Eisman JA, Sambrook PN (1990) Interaction of genetic and environmental influences on peak bone density. Osteoporosis Int 1:56–60CrossRefGoogle Scholar
  78. Kerton M, Newbury HJ, Hand D, Pritchard J (2009) Accumulation of calcium in the centre of leaves of coriander (Coriandrum sativum L.) is due to an uncoupling of water and ion transport. J Exp Bot 60:227–235PubMedCrossRefGoogle Scholar
  79. Kim KM, Park YH, Kim CK, Hirschi K, Sohn JK (2005) Development of transgenic rice plants overexpressing the Arabidopsis H+/Ca2+ antiporter CAX1 gene. Plant Cell Rep 23:678–682PubMedCrossRefGoogle Scholar
  80. Kim CK, Han JS, Lee HS, Oh JY, Shigaki T, Park SH, Hirschi K (2006) Expression of an Arabidopsis CAX2 variant in potato tubers increases calcium levels with no accumulation of manganese. Plant Cell Rep 25:1226–1232PubMedCrossRefGoogle Scholar
  81. Knight H, Knight MR (2000) Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis. J Exp Bot 51:1679–1686PubMedCrossRefGoogle Scholar
  82. Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267PubMedCrossRefGoogle Scholar
  83. Korenkov V, King B, Hirschi K, Wagner GJ (2009) Root-selective expression of AtCAX4 and AtCAX2 results in reduced lamina cadmium in field-grown Nicotiana tabacum L. Plant Biotechnol J 7:219–226PubMedCrossRefGoogle Scholar
  84. Korth KL, Doege SJ, Park SH, Goggin FL, Wang Q, Gomez SK, Liu G, Jia L, Nakata PA (2006) Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiol 141:188–195PubMedCrossRefGoogle Scholar
  85. Kranz S, Lin P-J, Wagstaff DA (2007) Children's dairy intake in the United States: too little, too fat? J Pediatr 151:642–646, e642PubMedCrossRefGoogle Scholar
  86. Lanham-New SA (2006) Fruit and vegetables: the unexpected natural answer to the question of osteoporosis prevention? Am J Clin Nutr 83:1254–1255PubMedGoogle Scholar
  87. Lanham-New SA (2008) Importance of calcium, vitamin D and vitamin K for osteoporosis prevention and treatment. Proc Nutr Soc 67:163–176PubMedCrossRefGoogle Scholar
  88. Leclerc J, Miller ML, Joliet E, Thicoipe JP, Despujols J (1992) Necrosis prevention and mineral and vitamin contents of Webb lettuce. Agrochimica 36:108–115Google Scholar
  89. Leigh RA (1997) Solute composition of vacuoles. In: Leigh RA, Sanders D (eds) The plant vacuole: advances in botanical research incorporating advances in plant pathology, vol. 25. Academic Press, New York, pp 298–337Google Scholar
  90. Liang W, Wang M, Ai X (2009) The role of calcium in regulating photosynthesis and related physiological indexes of cucumber seedlings under low light intensity and supoptimal temperature stress. Sci Hort 123:34–38Google Scholar
  91. Logan DC, Knight MR (2003) Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol 133:21–24PubMedCrossRefGoogle Scholar
  92. Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends Ecol Evol 17:457–461CrossRefGoogle Scholar
  93. MacRobbie EAC (2006a) Control of volume and turgor in stomatal guard cells. J Membr Biol 210:131–142PubMedCrossRefGoogle Scholar
  94. MacRobbie EAC (2006b) Osmotic effects on vacuolar ion release in guard cells. Proc Natl Acad Sci USA 103:1135–1140PubMedCrossRefGoogle Scholar
  95. Malone M, White P, Morales MA (2002) Mobilization of calcium in glasshouse tomato plants by localized scorching. J Exp Bot 53:83–88PubMedCrossRefGoogle Scholar
  96. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, San Diego, CaliforniaGoogle Scholar
  97. Martinez-Ballesta MC, Dominguez-Perles R, Moreno DA, Muries B, Alcaraz-Lopez C, Bastias E, Garcia-Viguera C, Carvajal M (2010) Minerals in plant food: effect of agricultural practices and role in human health. A review. Agron Sustain Dev 30:295–309CrossRefGoogle Scholar
  98. Matas AJ, Gapper NE, Chung MY, Giovannoni JJ, Rose JKC (2009) Biology and genetic engineering of fruit maturation for enhanced quality and shelf-life. Curr Opin Biotechnol 20:197–203PubMedCrossRefGoogle Scholar
  99. McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294PubMedCrossRefGoogle Scholar
  100. McGuire RG, Kelman A (1986) Calcium in potato-tuber cell-walls in relation to tissue maceration by Erwinia carotovora Pv Atroseptica. Phytopathol 76:401–406CrossRefGoogle Scholar
  101. Michaelsson K (2009) The calcium quandary. Nutr 25:655–656CrossRefGoogle Scholar
  102. Michaelsson K, Melhus H, Ferm H, Ahlbom A, Pedersen NL (2005) Genetic liability to fractures in the elderly. Arch Intern Med 165:1825–1830PubMedCrossRefGoogle Scholar
  103. Milott J, Green S, Schapia M (2000) Osteoporosis: evaluation and treatment. Compr Ther 26:183–189PubMedCrossRefGoogle Scholar
  104. Møller IS, Gilliham M, Jha J, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178PubMedCrossRefGoogle Scholar
  105. Morris J, Nakata PA, McConn M, Brock A, Hirschi KD (2007) Increased calcium bioavailability in mice fed genetically engineered plants lacking calcium oxalate. Plant Mol Biol 64:613–618PubMedCrossRefGoogle Scholar
  106. Morris J, Hawthorne KM, Hotze T, Abrams SA, Hirschi KD (2008) Nutritional impact of elevated calcium transport activity in carrots. Proc Natl Acad Sci USA 105:1431–1435PubMedCrossRefGoogle Scholar
  107. Moscatiello R, Mariani P, Sanders D, Maathuis FJM (2006) Transcriptional analysis of calcium-dependent and calcium-independent signalling pathways induced by oligogalacturonides. J Exp Bot 57:2847–2865PubMedCrossRefGoogle Scholar
  108. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  109. Murakami K, Edamoto M, Hata N, Itami Y, Masuda M (2009) Low-oxalate spinach mutant induced by chemical mutagenesis. J Jpn Soc Hort Sci 78:180–184CrossRefGoogle Scholar
  110. Naradisorn M, Able AJ, Scott E, Klieber A, Sedgley M (2006) Effect of preharvest calcium application on grey mould development and postharvest quality in strawberries. Acta Hortic 708:147–150Google Scholar
  111. Narasimhan V, Ramadoss N, Sridhar VV, Kareem AA (1994) Using gypsum to manage sheath rot in rice. Int Rice Res Newsl 19:27–28Google Scholar
  112. OA (2010) Osteoporosis Australia. Available at: http://www.osteoporosis.org.au/. Accessed 18 May 2010
  113. Olle M, Bender I (2009a) Causes and control of calcium deficiency disorders in vegetables: a review. J Hortic Sci Biotech 84:577–584Google Scholar
  114. Olle M, Bender I (2009b) Causes and control of calcium deficiency disorders in vegetables: a review. J Hortic Sci Biotechnol 84:577–584Google Scholar
  115. Oramasionwu GE, Thacher TD, Pam SD, Pettifor JM, Abrams SA (2008) Adaptation of calcium absorption during treatment of nutritional rickets in Nigerian children. Brit J Nutr 100:387–392PubMedCrossRefGoogle Scholar
  116. Park S, Kim CK, Pike LM, Smith RH, Hirschi KD (2004) Increased calcium in carrots by expression of an Arabidopsis H+/Ca2+ transporter. Mol Breed 14:275–282CrossRefGoogle Scholar
  117. Park S, Cheng NH, Pittman JK, Yoo KS, Park J, Smith RH, Hirschi KD (2005a) Increased calcium levels and prolonged shelf life in tomatoes expressing Arabidopsis H+/Ca2+ transporters. Plant Physiol 139:1194–1206PubMedCrossRefGoogle Scholar
  118. Park S, Kang TS, Kim CK, Han JS, Kim S, Smith RH, Pike LM, Hirschi KD (2005b) Genetic manipulation for enhancing calcium content in potato tuber. J Agric Food Chem 53:5598–5603PubMedCrossRefGoogle Scholar
  119. Park S, Elless MP, Park J, Jenkins A, Lim W, Chambers E, Hirschi KD (2009) Sensory analysis of calcium-biofortified lettuce. Plant Biotechnol J 7:106–117PubMedCrossRefGoogle Scholar
  120. Paula TJ, Vieira RF, Teixeira H, Carneiro JES (2009) Foliar application of calcium chloride and calcium silicate decreases white mold intensity on dry beans. Trop Plant Pathol 34:171–174Google Scholar
  121. Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux M, Hetherington AM, Sanders D (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408PubMedCrossRefGoogle Scholar
  122. Peremarti A, Twyman RM, Gomez-Galera S, Naqvi S, Farre G, Sabalza M, Miralpeix B, Dashevskaya S, Yuan DW, Ramessar K, Christou P, Zhu CF, Bassie L, Capell T (2010) Promoter diversity in multigene transformation. Plant Mol Biol 73:363–378PubMedCrossRefGoogle Scholar
  123. Pettifor JM (2008) Vitamin D and/or calcium deficiency rickets in infants and children: a global perspective. Indian J Med Res 127:245–249PubMedGoogle Scholar
  124. Pettifor JM, Ross P, Wang J, Moodley G, Coupersmith J (1978) Rickets in children of rural origin in South-Africa—is low dietary calcium a factor. J Pediatr 92:320–324PubMedCrossRefGoogle Scholar
  125. Pettifor JM, Fischer PR, Thacher TD, Arnaud J, Meissner CA (2008) Dietary calcium deficiency and rickets. Indian J Med Res 128:673–674PubMedGoogle Scholar
  126. Pittman JK, Hirschi KD (2001) Regulation of CAX1, an Arabidopsis Ca2+/H+ antiporter. identification of an N-terminal autoinhibitory domain. Plant Physiol 127:1020–1029PubMedCrossRefGoogle Scholar
  127. Pittman JK, Sreevidya CS, Shigaki T, Ueoka-Nakanishi H, Hirschi KD (2002) Distinct N-terminal regulatory domains of Ca2+/H+ antiporters. Plant Physiol 130:1054–1062PubMedCrossRefGoogle Scholar
  128. Prentice A (2004) Diet, nutrition and the prevention of osteoporosis. Public Health Nutr 7:227–243PubMedCrossRefGoogle Scholar
  129. Ranf S, Wunnenberg P, Lee J, Becker D, Dunkel M, Hedrich R, Scheel D, Dietrich P (2008) Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses. Plant J 53:287–299PubMedCrossRefGoogle Scholar
  130. Rea PA, Britten CJ, Jennings IR, Calvert CM, Skiera LA, Leigh RA, Sanders D (1992) Regulation of vacuolar H+-pyrophosphatase by free calcium—a reaction kinetic analysis. Plant Physiol 100:1706–1715PubMedCrossRefGoogle Scholar
  131. Reid RJ, Smith FA (2000) The limits of sodium/calcium interactions in plant growth. Austr J Plant Physiol 27:709–715Google Scholar
  132. Rogiers SY, Greer DH, Hatfield JM, Orchard BA, Keller M (2006) Mineral sinks within ripening grape berries (Vitis vinifera L.). Vitis 45:115–123Google Scholar
  133. Roy SJ, Gilliham M, Berger B, Essah PA, Cheffings C, Miller AJ, Davenport RJ, Liu LH, Skynner MJ, Davies JM, Richardson P, Leigh RA, Tester M (2008) Investigating glutamate receptor-like gene co-expression in Arabidopsis thaliana. Plant Cell Environ 31:861–871PubMedCrossRefGoogle Scholar
  134. Sai J, Johnson CH (2002) Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell 14:1279–1291PubMedCrossRefGoogle Scholar
  135. Saladié M, Matas AJ, Isaacson T, Jenks MA, Goodwin SM, Niklas KJ, Xiaolin R, Labavitch JM, Shackel KA, Fernie AR, Lytovchenko A, O'Neill MA, Watkins CB, Rose JKC (2007) A re-evaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiol 144:1012–1028PubMedCrossRefGoogle Scholar
  136. Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706PubMedCrossRefGoogle Scholar
  137. Sattelmacher B (2001) The apoplast and its significance for plant mineral nutrition. New Phytol 149:167–192CrossRefGoogle Scholar
  138. Saure MC (1998) Causes of the tipburn disorder in leaves of vegetables. Sci Hortic 76:131–147CrossRefGoogle Scholar
  139. Schreiber L, Franke R, Hartmann KD, Ranathunge K, Steudle E (2005) The chemical composition of suberin in apoplastic barriers affects radial hydraulic conductivity differently in the roots of rice (Oryza sativa L. cv. IR64) and corn (Zea mays L. cv. Helix). J Exp Bot 56:1427–1436Google Scholar
  140. Schroder BG, Griffin IJ, Specker BL, Abrams SA (2005) Absorption of calcium from the carbonated dairy soft drink is greater than that from fat-free milk and calcium-fortified orange juice in women. Nutr Res 25:737–742CrossRefGoogle Scholar
  141. Sen F, Karacali I, Irget ME, Elmaci OL, Tepecik M (2010) A new strategy to enrich calcium nutrition of fruit: synergistic effects of postharvest foliar calcium and boron sprays. J Plant Nutr 33:175–184Google Scholar
  142. Setnick J (2010) Micronutrient deficiencies and supplementation in anorexia and bulimia nervosa: a review of literature. Nutr Clin Pract 25:137–142PubMedCrossRefGoogle Scholar
  143. Shigaki T, Pittman JK, Hirschi KD (2003) Manganese specificity determinants in the Arabidopsis metal/H+ antiporter CAX2. J Biol Chem 278:6610–6617PubMedCrossRefGoogle Scholar
  144. Singh D, Sharma RR (2009) Post-harvest behaviour of peaches (Prunus persica) pretreated with antagonist Debaryomyces hansenii and calcium chloride. Indian J Ag Sci 79:674–678Google Scholar
  145. Singh BP, Tandon DK, Kalra SK (1993) Changes in postharvest quality of mangoes affected by preharvest application of calcium salts. Sci Hort 54:211–219Google Scholar
  146. Singh R, Sharma RR, Tyagi SK (2007) Pre-harvest foliar application of calcium and boron influences physiological disorders, fruit yield and quality of strawberry (Fragaria x ananassa Duch.). Sci Hortic 112:215–220CrossRefGoogle Scholar
  147. Storey R, Leigh RA (2004) Processes modulating calcium distribution in citrus leaves. An investigation using X-ray microanalysis with strontium as a tracer. Plant Physiol 136:3838–3848PubMedCrossRefGoogle Scholar
  148. Storey R, Jones RGW, Schachtman DP, Treeby MT (2003) Calcium-accumulating cells in the meristematic region of grapevine root apices. Funct Plant Biol 30:719–727CrossRefGoogle Scholar
  149. Subbaiah CC, Bush DS, Sachs MM (1988) Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells. Plant Physiol 118:759–771CrossRefGoogle Scholar
  150. Sugimoto T, Watanabe K, Yoshida S, Aino M, Irie K, Matoh T, Biggs AR (2008) Select calcium compounds reduce the severity or phytophthora stem rot of soybean. Plant Dis 92:1559–1565CrossRefGoogle Scholar
  151. Tanner W, Beevers H (2001) Transpiration, a prerequisite for long-distance transport of minerals in plants? Proc Natl Acad Sci USA 98:9443–9447PubMedCrossRefGoogle Scholar
  152. Teotia SPS, Teotia M (2008a) Dietary calcium deficiency and rickets response. Indian J Med Res 128:674–676Google Scholar
  153. Teotia SPS, Teotia M (2008b) Nutritional bone disease in Indian population. Indian J Med Res 127:219–228PubMedGoogle Scholar
  154. Thompson DS (2008) Space and time in the plant cell wall: relationships between cell type, cell wall rheology and cell function. Ann Bot 101:203–211PubMedCrossRefGoogle Scholar
  155. Tilbrook J, Tyerman SD (2008) Cell death in grape berries: varietal differences linked to xylem pressure and berry weight loss. Funct Plant Biol 35:173–184CrossRefGoogle Scholar
  156. Tilbrook J, Tyerman SD (2009) Hydraulic connection of grape berries to the vine: varietal differences in water conductance into and out of berries, and potential for backflow. Funct Plant Biol 36:541–550CrossRefGoogle Scholar
  157. Tracy FE, Gilliham M, Dodd AN, Webb AAR, Tester M (2008) NaCl-induced changes in cytosolic free Ca2+ in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant Cell and Env 31:1063–1073CrossRefGoogle Scholar
  158. Tsantili E, Rouskas D, Christopoulos MV, Stanidis V, Akrivos J, Papanikolaou D (2007) Effects of two pre-harvest calcium treatments on physiological and quality parameters in 'Vogue' cherries during storage. J Hort Sci Biotechnol 82:657–663Google Scholar
  159. Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657PubMedCrossRefGoogle Scholar
  160. Vatanparast H, Bailey DA, Baxter-Jones ADG, Whiting SJ (2010) Calcium requirements for bone growth in Canadian boys and girls during adolescence. Brit J Nutr 103:575–580PubMedCrossRefGoogle Scholar
  161. Very A, Sentenac H (2002) Cation channels in the Arabidopsis plasma membrane. Trends Plant Sci 7:168–175PubMedCrossRefGoogle Scholar
  162. Weaver CM, Plawecki KL (1994) Dietary calcium: adequacy of a vegetarian diet. Am J Clin Nutr 59:1238S–1241SPubMedGoogle Scholar
  163. Weaver CM, Heaney RP, Martin BR, Fitzsimmons ML (1991) Human calcium-absorption from whole-wheat products. J Nutr 121:1769–1775PubMedGoogle Scholar
  164. Weaver CM, Heaney RP, Proulx WR, Hinders SM, Packard PT (1993) Absorbability of calcium from common beans. J Food Sci 58:1401–1403CrossRefGoogle Scholar
  165. Weaver CM, Heaney RP, Nickel KP, Packard PI (1997) Calcium bioavailability from high oxalate vegetables: Chinese vegetables, sweet potatoes and rhubarb. J Food Sci 62:524–525CrossRefGoogle Scholar
  166. Weaver CM, Proulx WR, Heaney R (1999) Choices for achieving adequate dietary calcium with a vegetarian diet. Am J Clin Nutr 70:543S–548SPubMedGoogle Scholar
  167. Weinl S, Held K, Schlucking K, Steinhorst L, Kuhlgert S, Hippler M, Kudla J (2008) A plastid protein crucial for Ca2+-regulated stomatal responses. New Phytol 179:675–686PubMedCrossRefGoogle Scholar
  168. White PJ (2001) The pathways of calcium movement to the xylem. J Exp Bot 52:891–899PubMedCrossRefGoogle Scholar
  169. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511PubMedCrossRefGoogle Scholar
  170. White PJ, Broadley MR (2005) Biofortifying crops with essential mineral elements. Trends Plant Sci 10:586–593PubMedCrossRefGoogle Scholar
  171. Wu QY, Lim W, Park SH (2009) Physiological characterization of co-expressing of a CAX1 calcium transporter and a CRT calcium-binding protein in plant. In Vitro Cell Dev Biol-Plant 45:511–511Google Scholar
  172. Wyatt SE, Tsou PL, Robertson D (2002) Expression of the high capacity calcium-binding domain of calreticulin increases bioavailable calcium stores in plants. Transgenic Res 11:1–10PubMedCrossRefGoogle Scholar
  173. Yamanaka T, Nakagawa Y, Mori K, Nakano M, Imamura T, Kataoka H, Terashima A, Iida K, Kojima I, Katagiri T, Shinozaki K, Iida H (2010) MCA1 and MCA2 that mediate Ca2+ uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol 152:1284–1296PubMedCrossRefGoogle Scholar
  174. Zhao YD, Martin BR, Weaver CM (2005) Calcium bioavailability of calcium carbonate fortified soymilk is equivalent to cow's milk in young women. J Nutr 135:2379–2382PubMedGoogle Scholar
  175. Zhao J, Barkla B, Marshall J, Pittman J, Hirschi K (2008) The Arabidopsis cax3 mutants display altered salt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227:659–669PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Maclin Dayod
    • 1
  • Stephen Donald Tyerman
    • 1
  • Roger Allen Leigh
    • 1
  • Matthew Gilliham
    • 1
  1. 1.Waite Research Institute, School of Agriculture, Food and WineUniversity of AdelaideGlen OsmondAustralia

Personalised recommendations