Frontiers in Biology

, Volume 7, Issue 3, pp 254–266 | Cite as

Plant calcium oxalate crystal formation, function, and its impact on human health

  • Paul A. NakataEmail author


Crystals of calcium oxalate have been observed among members from most taxonomic groups of photosynthetic organisms ranging from the smallest algae to the largest trees. The biological roles for calcium oxalate crystal formation in plant growth and development include high-capacity calcium regulation, protection against herbivory, and tolerance to heavy metals. Using a variety of experimental approaches researchers have begun to unravel the complex mechanisms controlling formation of this biomineral. Given the important roles for calcium oxalate formation in plant survival and the antinutrient and pathological impact on human health through its presence in plant foods, researchers are avidly seeking a more comprehensive understanding of how these crystals form. Such an understanding will be useful in efforts to design strategies aimed at improving the nutritional quality and production of plant foods.


calcium oxalate crystals biomineral idioblast nutrition 


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  1. Ahmed A K, Johnson K A (2000). The effect of the ammonium: nitrate nitrogen ration, total nitrogen, salinity (NaCl) and calcium on oxalate levels of Tetragonia tetragonioides Pallas. Kunz. J Hortic Sci Biotechnol, 75: 533–538Google Scholar
  2. Arnott H J, Pautard F G E (1970). Calcification in plants. In: Biological Calcification: Cellular and Molecular Aspects (Schraer H, Ed.). New York: Appleton-Century-Crofts, 375–446Google Scholar
  3. Assailly A (1954). Sur les rapports de l’oxalate de chaux et de l’amidon. Cr Acad Sci D, 238: 1902–1904Google Scholar
  4. Barnabas A D, Arnott H J (1990). Calcium oxalate crystal formation in the bean (Phaseolus vulgaris L.) seed coat. Bot Gaz, 151(3): 331–341Google Scholar
  5. Borchert R (1985). Calcium-induced patterns of calcium-oxalate crystals in isolated leaflets of Gleditsia triacanthos L. and Albizia julibrissin Durazz. Planta, 165(3): 301–310PubMedGoogle Scholar
  6. Borchert R (1986). Calcium acetate induces calcium uptake and formation of calcium-oxalate crystals in isolated leaflets of Gleditsia tracanthos L. Planta, 168(4): 571–578PubMedGoogle Scholar
  7. Bouropoulos N, Weiner S, Addadi L (2001). Calcium oxalate crystals in tomato and tobacco plants: morphology and in vitro interactions of crystal-associated macromolecules. Chemistry, 7(9): 1881–1888PubMedGoogle Scholar
  8. Calmes J (1969). Contribution a l’etude du metabolisme de l’acide oxalique chez la Vigne vierge (Parthenocissus tricuspidata Planchon). Cr Acad Sci D, 269(6): 704–707Google Scholar
  9. Calmes J, Carles J (1970). La repartition et l’evolution des cristaux d’oxalate de calcium dans les tissus de vigne vierge au cours d’un cycle de vegetation. B Soc Bot Fr, 117(5/6): 189–198Google Scholar
  10. Catherwood D J, Savage G P, Mason S M, Scheffer J J C, Douglas J A (2007). Oxalate content of cormels of Japanese taro (Colocasia esculenta (L.) Schott) and the effect of cooking. J Food Compost Anal, 20(3–4): 147–151Google Scholar
  11. Choi Y E, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H (2001). Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta, 213(1): 45–50PubMedGoogle Scholar
  12. Coté G G (2009). Diversity and distribution of idioblasts producing calcium oxalate crystals in Dieffenbachia seguine (Araceae). Am J Bot, 96(7): 1245–1254PubMedGoogle Scholar
  13. Crofts A J, Leborgne-Castel N, Hillmer S, Robinson D G, Phillipson B, Carlsson L E, Ashford D A, Denecke J (1999). Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant Cell, 11(11): 2233–2248PubMedPubMedCentralGoogle Scholar
  14. De Yoreo J J, Qiu S R, Hoyer J R (2006). Molecular modulation of calcium oxalate crystallization. Am J Physiol Renal Physiol, 291(6): F1123–F1132PubMedGoogle Scholar
  15. Franceschi V R (1989). Calcium oxalate formation is a rapid and reversible process in Lemna minor L. Protoplasma, 148(2–3): 130–137Google Scholar
  16. Franceschi V R, Horner H T Jr (1979). Use of Psychotria puncata callus in study of calcium oxalate crystal idioblast formation. Z Pflanzenphysiol, 67: 61–75Google Scholar
  17. Franceschi V R, Horner H T Jr (1980). Calcium oxalate crystals in plants. Bot Rev, 46(4): 361–427Google Scholar
  18. Franceschi V R, Li X, Zhang D, Okita T W (1993). Calsequestrinlike calcium-binding protein is expressed in calcium-accumulating cells of Pistia stratiotes. Proc Natl Acad Sci USA, 90(15): 6986–6990PubMedPubMedCentralGoogle Scholar
  19. Franceschi V R, Loewus F A (1995). Oxalate biosynthesis and function in plants and fungi. In: Calcium Oxalate in Biological Systems (Khan S R Ed.). Boca Raton: CRC Press, 113–130Google Scholar
  20. Franceschi V R, Nakata PA (2005). Calcium oxalate in plants: formation and function. Annu Rev Plant Biol, 56(1): 41–71PubMedGoogle Scholar
  21. Franceschi V R, Schueren A M (1986). Incorporation of strontium into plant calcium oxalate crystals. Protoplasma, 130(2–3): 199–205Google Scholar
  22. Franceschi V R, Tarlyn N M (2002). L-Ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants. Plant Physiol, 130(2): 649–656PubMedPubMedCentralGoogle Scholar
  23. Frank E, Jensen WA (1970). On the formation of the pattern of crystal idiobalsts in Canavalia ensiformis DC. IV. The fine structure of the crystal cells. Planta, 95: 202–217Google Scholar
  24. Frey-Wyssling A (1981). Crystallography of the two hydrates of crystalline calcium oxalate in plants. Am J Bot, 68(1): 130–141Google Scholar
  25. Furuhashi T, Schwarzinger C, Miksik I, Smrz M, Beran A (2009). Molluscan shell evolution with review of shell calcification hypothesis. Comp Biochem Physiol B Biochem Mol Biol, 154(3): 351–371PubMedGoogle Scholar
  26. Gallaher R N (1975). The occurrence of calcium in plant tissue as crystals of calcium oxalate. Commun Soil Sci Plan, 6(3): 315–330Google Scholar
  27. Gélinas B, Seguin P (2007). Oxalate in grain amaranth. J Agric Food Chem, 55(12): 4789–4794PubMedGoogle Scholar
  28. Green M A, Fry S C (2005). Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-L-threonate. Nature, 433(7021): 83–87PubMedGoogle Scholar
  29. Guo Z, Tan H, Zhu Z, Lu S, Zhou B (2005). Effect of intermediates on ascorbic acid and oxalate biosynthesis of rice and in relation to its stress resistance. Plant Physiol Biochem, 43(10–11): 955–962PubMedGoogle Scholar
  30. Hartl W P, Klapper H, Barbier B, Ensikat H J, Dronskowski R, Müller P, Ostendorp G, Tye A, Bauer R, Barthlott W (2007). Diversity of calcium oxalate crystals in Cactaceae. Can J Bot, 85(5): 501–517Google Scholar
  31. Heaney R P, Recker R R, Hinders S M (1988). Variability of calcium absorption. Am J Clin Nutr, 47(2): 262–264PubMedGoogle Scholar
  32. Heaney R P, Weaver C M (1989). Oxalate: effect on calcium absorbability. Am J Clin Nutr, 50(4): 830–832PubMedGoogle Scholar
  33. Heaney R P, Weaver C M (1990). Calcium absorption from kale. Am J Clin Nutr, 51(4): 656–657PubMedGoogle Scholar
  34. Hodgkinson A (1977). Oxalic Acid Biology and Medicine. Academic Press: New YorkGoogle Scholar
  35. Holmes R P, Goodman H O, Assimos D G (1995). Dietary oxalate and its intestinal absorption. Scanning Microsc, 9(4): 1109–1118, discussion 1118–1120PubMedGoogle Scholar
  36. Holmes R P, Goodman H O, Assimos D G (2001). Contribution of dietary oxalate to urinary oxalate excretion. Kidney Int, 59(1): 270–276PubMedGoogle Scholar
  37. Horner H T, Kausch A P, Wagner B L (2000). Ascorbic Acid: A precursor of oxalate in crystal idioblasts of Yucca Torreyi in liquid root culture. Int J Plant Sci, 161(6): 861–868Google Scholar
  38. Horner H T, Wagner B L (1980). The association of druse crystals with the developing stomium of Capsicum annuum (Solanaceae) anthers. Am J Bot, 67(9): 1347–1360Google Scholar
  39. Horner H T, Wagner B L (1995). Calcium oxalate formation in higher plants. In: Calcium Oxalate in Biological Systems. (Khan S R Ed.). Boca Raton: CRC Press, Florida, 53–72Google Scholar
  40. Hudgins J W, Krekling T, Franceschi V R (2003). Distribution of calcium oxalate crystals in the secondary phloem of conifers: a constitutive defense mechanism? New Phytol, 159(3): 677–690Google Scholar
  41. Ilarslan H, Palmer R G, Horner H T (2001). Calcium oxalate crystals in developing seeds of soybean. Ann Bot (Lond), 88(2): 243–257Google Scholar
  42. Ji XM, Peng X X (2005). Oxalate accumulation as regulated by nitrogen forms and its relationship to photosynthesis in rice (Oryza sativa L.). J Int Plant Biol, 47(7): 831–838Google Scholar
  43. Jou Y, Wang Y, Yen H E (2007). Vacuolar acidity, protein profile, and crystal composition of epidermal bladder cells of the halophyte Mesembryanthemum crystallinum. Funct Plant Biol, 34(4): 353–359Google Scholar
  44. Katayama H, Fujibayashi Y, Nagaoka S, Sugimura Y (2007). Cell wall sheath surrounding calcium oxalate crystals in mulberry idioblasts. Protoplasma, 231(3–4): 245–248PubMedGoogle Scholar
  45. Kausch A P, Horner H T (1984). Differentiation of raphide crystal idioblasts in isolated root cultures of Yucca torreyi (Agavaceae). Can J Bot, 62(7): 1474–1484Google Scholar
  46. Kausch A P, Horner H T (1985). Absence of CeCl3-detectable peroxisomal glycolate-oxidase activity in developing raphide crystal idioblasts in leaves of Psychotria punctata Vatke and roots of Yucca torreyi L. Planta, 164(1): 35–43PubMedGoogle Scholar
  47. Keates S E, Tarlyn N M, Loewus F A, Franceschi V R (2000). LAscorbic acid and L-galactose are sources for oxalic acid and calcium oxalate in Pistia stratiotes. Phytochemistry, 53(4): 433–440PubMedGoogle Scholar
  48. Kochian L V (1995). Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol, 46(1): 237–260Google Scholar
  49. Korth K L, Doege S J, Park S H, Goggin F L, Wang Q, Gomez S K, Liu G, Jia L, Nakata P A (2006). Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiol, 141(1): 188–195PubMedPubMedCentralGoogle Scholar
  50. Kostman T A, Franceschi V R (2000). Cell and calcium oxalate crystal growth is coordinated to achieve high-capacity calcium regulation in plants. Protoplasma, 214(3–4): 166–179Google Scholar
  51. Kostman T A, Franceschi V R, Nakata P A (2003). Endoplasmic reticulum sub-compartments are involved in calcium sequestration within raphide crystal idioblasts of Pistia stratiotes L. Plant Sci, 165(1): 205–212Google Scholar
  52. Kostman T A, Koscher J R (2003). L-galactono-gamma-lactone dehydrogenase is present in calcium oxalate crystal idioblasts of two plant species. Plant Physiol Biochem, 41(3): 201–206Google Scholar
  53. Kostman T A, Tarlyn N M, Franceschi V R (2007). Autoradiography utilising labelled ascorbic acid reveals biochemical and morphological details in diverse calcium oxalate crystal-forming species. Funct Plant Biol, 34(4): 339–342Google Scholar
  54. Kostman T A, Tarlyn N M, Loewus F A, Franceschi V R (2001). Biosynthesis of L-ascorbic acid and conversion of carbons 1 and 2 of L-ascorbic acid to oxalic acid occurs within individual calcium oxalate crystal idioblasts. Plant Physiol, 125(2): 634–640PubMedPubMedCentralGoogle Scholar
  55. Kröger N, Poulsen N (2008). Diatoms-from cell wall biogenesis to nanotechnology. Annu Rev Genet, 42(1): 83–107PubMedGoogle Scholar
  56. Kuo-Huang L L, Ku M S B, Franceschi V R (2007). Correlations between calcium oxalate crystals and photosynthetic activites in palisade cells of shade-adapted Peperomia glabella. Bot Stud (Taipei, Taiwan), 48(2): 155–164Google Scholar
  57. Kuo-Huang L L, Zindler-Frank E (1998). Structure of crystal cells and influences of leaf development on crystal cell development and vice versa in Phaseolus vulgaris (Leguminosae). Bot Acta, 111: 337–345Google Scholar
  58. Lazzaro M D, Thomson W W (1989). Ultrastructure of organic acid secreting trichomes of chickpea (Cicer arietinum). Can J Bot, 67(9): 2669–2677Google Scholar
  59. Leeuwenhoek A (1675). Microscopical observations. Philos T Roy Soc, 10: 380–385Google Scholar
  60. Lersten N, Horner H (2008a). Crystal macropatterns in leaves of Fagaceae and Nothofagaceae: a comparative study. Plant Syst Evol, 271(3–4): 239–253Google Scholar
  61. Lersten N, Horner H (2008b). Subepidermal idioblasts and crystal macropattern in leaves of Ticodendron (Ticodendraceae). Plant Syst Evol, 276(3–4): 255–260Google Scholar
  62. Lersten N, Horner H (2009). Crystal diversity and macropatterns in leaves of Oleaceae. Plant Syst Evol, 282(1–2): 87–102Google Scholar
  63. Lersten N R, Horner H T (2000). Types of calcium oxalate crystals and macro patterns in leaves of Prunus (Rosaceae: Prunoideae). Plant Syst Evol, 224: 83–96Google Scholar
  64. Lersten N R, Horner H T (2011). Unique calcium oxalate “duplex” and “concretion” idioblasts in leaves of tribe Naucleeae (Rubiaceae). Am J Bot, 98(1): 1–11PubMedGoogle Scholar
  65. Li X X, Franceschi V R (1990). Distribution of peroxisomes and glycolate metabolism in relation to calcium oxalate formation in Lemna minor L. Eur J Cell Biol, 51(1): 9–16PubMedGoogle Scholar
  66. Li X X, Zhang D Z, Lynch-Holm V J, Okita T W, Franceschi V R (2003). Isolation of a crystal matrix protein associated with calcium oxalate precipitation in vacuoles of specialized cells. Plant Physiol, 133(2): 549–559PubMedPubMedCentralGoogle Scholar
  67. Libert B (1987). Breeding a low-oxalate rhubarb (Rheum sp. L.). J Hortic Sci Biotechnol, 62(4): 523–529Google Scholar
  68. Libert B, Franceschi V R (1987). Oxalate in crop plants. J Agric Food Chem, 35(6): 926–938Google Scholar
  69. Loewus F (1999). Biosynthesis and metabolism of ascorbic acid in plants and of analogs of ascorbic acid in fungi. Phytochemistry, 52(2): 193–210Google Scholar
  70. Loewus F A, Wagner G, Yang J C (1975). Biosynthesis and metabolism of ascorbic acid in plants. Ann N YAcad Sci, 258(1 Second Confer): 7–23Google Scholar
  71. Ma J F, Hiradate S, Nomoto K, Iwashita T, Matsumoto H (1997a). Internal detoxification mechanism of Al in hydrangea. Plant Physiol, 113(4): 1033–1039PubMedPubMedCentralGoogle Scholar
  72. Ma J F, Ryan P R, Delhaize E (2001). Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci, 6(6): 273–278PubMedGoogle Scholar
  73. Ma J F, Zheng S J, Matsumoto H, Hiradate S (1997b). Detoxifying aluminium with buckwheat. Nature, 390(6660): 569–570Google Scholar
  74. Massey L K, Palmer R G, Horner H T (2001). Oxalate content of soybean seeds (Glycine max: Leguminosae), soyfoods, and other edible legumes. J Agric Food Chem, 49(9): 4262–4266PubMedGoogle Scholar
  75. Mazen A M A (2004). Calcium oxalate deposits in leaves of Corchorus olitotius as related to accumulation of toxic metals. Russ J Plant Physiol, 51(2): 281–285Google Scholar
  76. Mazen A M A, Zhang D Z, Franceschi V R (2004). Calcium oxalate formation in Lemna minor: physiological and ultrastructural aspects of high capacity calcium sequestration. New Phytol, 161(2): 435–448Google Scholar
  77. McConn M M, Nakata PA (2002). Calcium oxalate crystal morphology mutants from Medicago truncatula. Planta, 215(3): 380–386PubMedGoogle Scholar
  78. McConn M M, Nakata PA (2004). Oxalate reduces calcium availability in the pads of the prickly pear cactus through formation of calcium oxalate crystals. J Agric Food Chem, 52(5): 1371–1374PubMedGoogle Scholar
  79. McNair J B (1932). The interrelation between substances in plants: essential oils and resins, cyanogen and oxalate. Am J Bot, 19(3): 255–271Google Scholar
  80. Melino V J, Soole K L, Ford C M (2009). Ascorbate metabolism and the developmental demand for tartaric and oxalic acids in ripening grape berries. BMC Plant Biol, 9(1): 145PubMedPubMedCentralGoogle Scholar
  81. Molano-Flores B (2001). Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae). Ann Bot (Lond), 88(3): 387–391Google Scholar
  82. Monje P V, Baran E J (2002). Characterization of calcium oxalates generated as biominerals in cacti. Plant Physiol, 128(2): 707–713PubMedPubMedCentralGoogle Scholar
  83. Moreau A G, Savage G P (2009). Oxalate content of purslane leaves and the effect of combining them with yoghurt or coconut products. J Food Compost Anal, 22(4): 303–306Google Scholar
  84. Morris J, Nakata P A, McConn M, Brock A, Hirschi K D (2007). Increased calcium bioavailability in mice fed genetically engineered plants lacking calcium oxalate. Plant Mol Biol, 64(5): 613–618PubMedGoogle Scholar
  85. Morrow A C, Dute R R (2002). Crystals associated with the intertracheid pit membrane of the woody fern Botrychium multifidum. Am Fern J, 92(1): 10–19Google Scholar
  86. Nakata P A (2003). Advances in our understanding of calcium oxalate crystal formation and function in plants. Plant Sci, 164(6): 901–909Google Scholar
  87. Nakata PA (2012). Influence of calcium oxalate crystal accumulation on the calcium content of seeds from Medicago truncatula. Plant Sci, 185–186(0): 246–249PubMedGoogle Scholar
  88. Nakata P A, Kostman T A, Franceschi V R (2003). Calreticulin is enriched in the crystal idioblasts of Pistia stratiotes. Plant Physiol Biochem, 41(5): 425–430Google Scholar
  89. Nakata P A, McConn M (2002). Sequential subtractive approach facilitates identification of differentially expressed genes. Plant Physiol Biochem, 40(4): 307–312Google Scholar
  90. Nakata P A, McConn M M (2000). Isolation of Medicago truncatula mutants defective in calcium oxalate crystal formation. Plant Physiol, 124(3): 1097–1104PubMedPubMedCentralGoogle Scholar
  91. Nakata PA, McConn MM (2003a). Calcium oxalate crystal formation is not essential for growth of Medicago truncatula. Plant Physiol Biochem, 41(4): 325–329Google Scholar
  92. Nakata P A, McConn M M (2003b). Influence of the calcium oxalate defective 4 (cod4) mutation on the growth, oxalate content, and calcium content of Medicago truncatula. Plant Sci, 164(4): 617–621Google Scholar
  93. Nakata P A, McConn M M (2006). A genetic mutation that reduces calcium oxalate content increases calcium availability in Medicago truncatula. Funct Plant Biol, 33(7): 703–706Google Scholar
  94. Nakata PA, McConn M M (2007a). Calcium oxalate content affects the nutritional availability of calcium from Medicago truncatula leaves. Plant Sci, 172(5): 958–961Google Scholar
  95. Nakata PA, McConn M M (2007b). Genetic evidence for differences in the pathways of druse and prismatic calcium oxalate crystal formation in Medicago truncatula. Funct Plant Biol, 34(4): 332–338Google Scholar
  96. Nakata P A, McConn M M (2007c). Isolated Medicago truncatula mutants with increased calcium oxalate crystal accumulation have decreased ascorbic acid levels. Plant Physiol Biochem, 45(3–4): 216–220PubMedGoogle Scholar
  97. Nordin B E C, Hodgkinson A, Peacock M, Robertson W G (1979). Urinary tract calculi. In: Nephrology (Hamburger J, Crosnier J, Grunfeld J P, Eds). Wiley: New York and Paris, 1091Google Scholar
  98. Nuss R F, Loewus F A (1978). Further studies on oxalic acid biosynthesis in oxalate-accumulating plants. Plant Physiol, 61(4): 590–592PubMedPubMedCentralGoogle Scholar
  99. Olszta M J, Cheng X, Jee S S, Kumar R, Kim Y Y, Kaufman M J, Douglas E P, Gower L B (2007). Bone structure and formation: A new perspective. Mater Sci Eng Rep, 58(3–5): 77–116Google Scholar
  100. Oscarsson K V, Savage G P (2007). Composition and availability of soluble and insoluble oxalates in raw and cooked taro (Colocasia esculenta var. Schott) leaves. Food Chem, 101(2): 559–562Google Scholar
  101. Park S H, Doege S J, Nakata P A, Korth K L (2009). Medicago truncatula-derived calcium oxalate crystals have a negative impact on chewing insect performance via their physical properties. Entomol Exp Appl, 131(2): 208–215Google Scholar
  102. Parsons H T, Fry S C (2012). Oxidation of dehydroascorbic acid and 2,3-diketogulonate under plant apoplastic conditions. Phytochemistry, 75(0): 41–49PubMedGoogle Scholar
  103. Parsons H T, Yasmin T, Fry S C (2011). Alternative pathways of dehydroascorbic acid degradation in vitro and in plant cell cultures: novel insights into vitamin C catabolism. Biochem J, 440(3): 375–383PubMedGoogle Scholar
  104. Pennisi S V, McConnell D B (2001). Inducible calcium sinks and preferential calcium allocation in leaf primordia of Dracaena sanderiana Hort. Sander ex M.T. Mast. (Dracaenaceae). HortScience, 36: 1187–1191Google Scholar
  105. Pennisi S V, McConnell D B, Gower L B, Kane M E, Lucansky T (2001). Intracellular calcium oxalate crystal structure in Dracaena sanderiana. New Phytol, 150(1): 111–120Google Scholar
  106. Proietti S, Moscatello S, Famiani F, Battistelli A (2009). Increase of ascorbic acid content and nutritional quality in spinach leaves during physiological acclimation to low temperature. Plant Physiol Biochem, 47(8): 717–723PubMedGoogle Scholar
  107. Prychid C J, Jabaily R S, Rudall P J (2008). Cellular ultrastructure and crystal development in Amorphophallus (Araceae). Ann Bot (Lond), 101(7): 983–995Google Scholar
  108. Prychid C J, Rudall P J (1999). Calcium oxalate crystals in monocotyledons: A review of their structure and systematics. Ann Bot (Lond), 84(6): 725–739Google Scholar
  109. Rahman M M, Ishii Y, Niimi M, Kawamura O (2010). Effect of application form of nitrogen on oxalate accumulation and mineral uptake by napiergrass (Pennisetum purpureum). Grassland Sci, 56(3): 141–144Google Scholar
  110. Rinallo C, Modi G (2002). Content of oxalate in Actinidia deliciosa plants grown in nutrient solutions with different nitrogen forms. Biol Plant, 45(1): 137–139Google Scholar
  111. Ritter M M C, Savage G P (2007). Soluble and insoluble oxalate content of nuts. J Food Compost Anal, 20(3–4): 169–174Google Scholar
  112. Ruiz N, Ward D, Saltz S (2002a). Calcium oxalate crystals in leaves of Pancratium sickenbergeri: constitutive or induced defense? Funct Ecol, 16(1): 99–105Google Scholar
  113. Ruiz N, Ward D, Saltz S (2002b). Responses of Pancratium sickenbergeri to simulated bulb herbivory: combining defence and tolerance strategies. J Ecol, 90(3): 472–479Google Scholar
  114. Ryall R L, Stapleton A M F (1995) Urinary macromolecules in calcium oxalate stone and crystal matrix: good, bad, or indifferent? In: Calcium oxalate in biological systems (Kahn S R, Ed.). CRC Press, Inc.: Boca Raton, 265–290Google Scholar
  115. Ryan P R, Delhaize E, Jones D L (2001). Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol, 52(1): 527–560PubMedGoogle Scholar
  116. Saito K, Ohmoto J, Kuriha N (1997). Incorporation of 18O into oxalic, Lthreonic and L-tartaric acids during cleavage of L-ascorbic and 5-keto-D-gluconic acids in plants. Phytochemistry, 44(5): 805–809Google Scholar
  117. Saltz S, Ward D (2000). Responding to a three-pronged attack: desert lilies subject to herbivory by dorcas gazelles. Plant Ecol, 148(2): 127–138Google Scholar
  118. Savage G P, Mårtensson L, Sedcole J R (2009). Composition of oxalates in baked taro (Colocasia esculenta var. Schott) leaves cooked alone or with additions of cows milk or coconut milk. J Food Compost Anal, 22(1): 83–86Google Scholar
  119. Savage G P, Vanhanen L, Mason S M, Ross A B (2000). Effect of cooking on the soluble and insoluble oxalate content of some New Zealand foods. J Food Compost Anal, 13(3): 201–206Google Scholar
  120. Siener R, Hönow R, Seidler A, Voss S, Hesse A (2006a). Oxalate contents of species of the Polygonaceae, Amaranthaceae and Chenopodiaceae families. Food Chem, 98(2): 220–224Google Scholar
  121. Siener R, Hönow R, Voss S, Seidler A, Hesse A (2006b). Oxalate content of cereals and cereal products. J Agric Food Chem, 54(8): 3008–3011PubMedGoogle Scholar
  122. Smith K T, Shortle W C, Connolly J H, Minocha R, Jellison J (2009). Calcium fertilization increases the concentration of calcium in sapwood and calcium oxalate in foliage of red spruce. Environ Exp Bot, 67(1): 277–283Google Scholar
  123. Sugiyama N, Okutani I (1996). Relationship between nitrate reduction and oxalate synthesis in spinach leaves. J Plant Physiol, 149(1–2): 14–18Google Scholar
  124. Taylor G J (1991). Current views of the aluminum stress response; the physiological basis of tolerance. Curr Top Plant Biochem Physiol, 10: 57–93Google Scholar
  125. Thongboonkerd V, Semangoen T, Chutipongtanate S (2006). Factors determining types and morphologies of calcium oxalate crystals: molar concentrations, buffering, pH, stirring and temperature. Clin Chim Acta, 367(1–2): 120–131PubMedGoogle Scholar
  126. Thurston E L (1976). Morphology, fine structure and ontogeny of the stinging emergence of Tragia ramosa and T. saxicola (Euphorbiaceae). Am J Bot, 63(6): 710–718Google Scholar
  127. Tillman-Sutela E, Kauppi A (1999). Calcium oxalate crystals in the mature seeds of Norway spruce, Picea abies (L.) Karst. Trees (Berl), 13(3): 131–137Google Scholar
  128. Volk G M, Lynch-Holm V J, Kostman T A, Goss L J, Franceschi V R (2002). The role of druse and raphide calcium oxalate crystals in tissue calcium regulation in Pistia stratiotes leaves. Plant Biol, 4(1): 34–45Google Scholar
  129. Wagner G, Loewus F (1973). The biosynthesis of (+)-tartaric acid in Pelargonium crispum. Plant Physiol, 52(6): 651–654PubMedPubMedCentralGoogle Scholar
  130. Ward D, Spiegel M, Saltz S (1997). Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lilly. J Chem Ecol, 23(2): 333–346Google Scholar
  131. Weaver C M, Martin B R, Ebner J S, Krueger C A (1987). Oxalic acid decreases calcium absorption in rats. J Nutr, 117(11): 1903–1906PubMedGoogle Scholar
  132. Webb M A (1999). Cell-mediated crystallization of calcium oxalate in plants. Plant Cell, 11(4): 751–761PubMedPubMedCentralGoogle Scholar
  133. Webb M A, Arnott H J (1981). An ultrastructural study of druse crystals in okra cotyledons. Scan Electron Microsc, 3: 285–292Google Scholar
  134. Webb M A, Arnott H J (1983). Inside plant crystals: a study of the noncrystalline core in druses of Vitis vinifera endosperm. Scan Electron Microsc, IV: 1759–1770Google Scholar
  135. Webb M A, Cavaletto J M, Carpita N C, Lopez L E, Arnott H J (1995). The intravacuolar organic matrix associated with calcium oxalate crystals in leaves of Vitis. Plant J, 7(4): 633–648Google Scholar
  136. Weiner S, Addadi L (1991). Acidic macromolecules of mineralized tissues: the controllers of crystal formation. Trends Biochem Sci, 16(7): 252–256PubMedGoogle Scholar
  137. Xu HW, Ji X M, He Z H, ShiW P, Zhu G H, Niu J K, Li B S, Peng X X (2006). Oxalate accumulation and regulation is independent of glycolate oxidase in rice leaves. J Exp Bot, 57(9): 1899–1908PubMedGoogle Scholar
  138. Yang J C, Loewus F A (1975). Metabolic conversion of L-ascorbic acid in oxalate-accumulating plants. Plant Physiol, 56(2): 283–285PubMedPubMedCentralGoogle Scholar
  139. Yang Y Y, Jung J Y, Song W Y, Suh H S, Lee Y (2000). Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiol, 124(3): 1019–1026PubMedPubMedCentralGoogle Scholar
  140. Yu L, Jiang J, Zhang C, Jiang L, Ye N, Lu Y, Yang G, Liu E, Peng C, He Z, Peng X (2010). Glyoxylate rather than ascorbate is an efficient precursor for oxalate biosynthesis in rice. J Exp Bot, 61(6): 1625–1634PubMedPubMedCentralGoogle Scholar
  141. Zindler-Frank E (1975). On the formation of the pattern of crystal idioblasts in Canavalia ensiformis D.C.: VII. Calcium and oxalate content of the leaves in dependence of calcium nutrition. Z Pflanzenphysiol, 77: 80–85Google Scholar
  142. Zindler-Frank E (1976). Oxalate biosynthesis in relation to photosynthetic pathways and plant productivity: a survey. Z Pflanzenphysiol, 80: 1–13Google Scholar
  143. Zindler-Frank E (1987) Calcium oxalate in legumes. In: Advances in Legume Systematics (Stirton E, Ed.)Royal Botanic Gardens: Kew, UK, 279–316Google Scholar
  144. Zindler-Frank E (1991). Calcium oxalate crystal formation and growth in two legume species as altered by strontium. Bot Acta, 104: 229–232Google Scholar
  145. Zindler-Frank E, Honow R, Hesse A (2001). Calcium and oxalate content of the leaves of Phaseolus vulgaris at different calcium supply in relation to calcium oxalate crystal formation. J Plant Physiol, 158(2): 139–144Google Scholar

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© Higher Education Press and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.USDA-ARS Children’s Nutrition Research Center, Department of PediatricsBaylor College of MedicineHoustonUSA

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