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

Abstract

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.

Keywords

calcium / oxalate / crystals / biomineral / idioblast / nutrition

References

[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: 533–538

[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<PublisherName Language="chs"/>, 375–446

[3] Assailly A (1954). Sur les rapports de l'oxalate de chaux et de l'amidon. Cr Acad Sci D, 238: 1902–1904

[4] Barnabas A D, Arnott H J (1990). Calcium oxalate crystal formation in the bean (Phaseolus vulgaris L.) seed coat. Bot Gaz, 151(3): 331–341

[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): 301–310

[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): 571–578

[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): 1881–1888

[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): 704–707

[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): 189–198

[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): 147–151

[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): 45–50

[12] Coté G G (2009). Diversity and distribution of idioblasts producing calcium oxalate crystals in Dieffenbachia seguine (Araceae). Am J Bot, 96(7): 1245–1254

[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): 2233–2248

[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–F1132

[15] Franceschi V R (1989). Calcium oxalate formation is a rapid and reversible process in Lemna minor L. Protoplasma, 148(2-3): 130–137

[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: 61–75

[17] Franceschi V R, Horner H T Jr (1980). Calcium oxalate crystals in plants. Bot Rev, 46(4): 361–427

[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): 6986–6990

[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<PublisherName Language="chs"/>, 113–130

[20] Franceschi V R, Nakata P A (2005). Calcium oxalate in plants: formation and function. Annu Rev Plant Biol, 56(1): 41–71

[21] Franceschi V R, Schueren A M (1986). Incorporation of strontium into plant calcium oxalate crystals. Protoplasma, 130(2-3): 199–205

[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): 649–656

[23] Frank E, Jensen W A (1970). On the formation of the pattern of crystal idiobalsts in Canavalia ensiformis DC. IV. The fine structure of the crystal cells. Planta, 95: 202–217

[24] Frey-Wyssling A (1981). Crystallography of the two hydrates of crystalline calcium oxalate in plants. Am J Bot, 68(1): 130–141

[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): 351–371

[26] Gallaher R N (1975). The occurrence of calcium in plant tissue as crystals of calcium oxalate. Commun Soil Sci Plan, 6(3): 315–330

[27] Gélinas B, Seguin P (2007). Oxalate in grain amaranth. J Agric Food Chem, 55(12): 4789–4794

[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): 83–87

[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): 955–962

[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): 501–517

[31] Heaney R P, Recker R R, Hinders S M (1988). Variability of calcium absorption. Am J Clin Nutr, 47(2): 262–264

[32] Heaney R P, Weaver C M (1989). Oxalate: effect on calcium absorbability. Am J Clin Nutr, 50(4): 830–832

[33] Heaney R P, Weaver C M (1990). Calcium absorption from kale. Am J Clin Nutr, 51(4): 656–657

[34] Hodgkinson A (1977). Oxalic Acid Biology and Medicine. Academic Press: New York

[35] Holmes R P, Goodman H O, Assimos D G (1995). Dietary oxalate and its intestinal absorption. Scanning Microsc, 9(4): 1109–1118, discussion 1118–1120

[36] Holmes R P, Goodman H O, Assimos D G (2001). Contribution of dietary oxalate to urinary oxalate excretion. Kidney Int, 59(1): 270–276

[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): 861–868

[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): 1347–1360

[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, 53–72

[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): 677–690

[41] Ilarslan H, Palmer R G, Horner H T (2001). Calcium oxalate crystals in developing seeds of soybean. Ann Bot (Lond), 88(2): 243–257

[42] Ji X M, Peng X X (2005). Oxalate accumulation as regulated by nitrogen forms and its relationship to photosynthesis in rice (Oryza sativa L.). J IntPlant Biol, 47(7): 831–838

[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): 353–359

[44] Katayama H, Fujibayashi Y, Nagaoka S, Sugimura Y (2007). Cell wall sheath surrounding calcium oxalate crystals in mulberry idioblasts. Protoplasma, 231(3-4): 245–248

[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): 1474–1484

[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): 35–43

[47] Keates S E, Tarlyn N M, Loewus F A, Franceschi V R (2000). L-Ascorbic acid and L-galactose are sources for oxalic acid and calcium oxalate in Pistia stratiotes. Phytochemistry, 53(4): 433–440

[48] Kochian L V (1995). Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol, 46(1): 237–260

[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): 188–195

[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): 166–179

[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): 205–212

[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): 201–206

[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): 339–342

[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): 634–640

[55] Kröger N, Poulsen N (2008). Diatoms-from cell wall biogenesis to nanotechnology. Annu Rev Genet, 42(1): 83–107

[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): 155–164

[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: 337–345

[58] Lazzaro M D, Thomson W W (1989). Ultrastructure of organic acid secreting trichomes of chickpea (Cicer arietinum). Can J Bot, 67(9): 2669–2677

[59] Leeuwenhoek A (1675). Microscopical observations. Philos T Roy Soc, 10: 380–385

[60] Lersten N, Horner H (2008a). Crystal macropatterns in leaves of Fagaceae and Nothofagaceae: a comparative study. Plant Syst Evol, 271(3--4): 239–253

[61] Lersten N, Horner H (2008b). Subepidermal idioblasts and crystal macropattern in leaves of Ticodendron (Ticodendraceae). Plant Syst Evol, 276(3--4): 255–260

[62] Lersten N, Horner H (2009). Crystal diversity and macropatterns in leaves of Oleaceae. Plant Syst Evol, 282(1--2): 87–102

[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: 83–96

[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): 1–11

[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): 9–16

[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): 549–559

[67] Libert B (1987). Breeding a low-oxalate rhubarb (Rheum sp. L.). J Hortic Sci Biotechnol, 62(4): 523–529

[68] Libert B, Franceschi V R (1987). Oxalate in crop plants. J Agric Food Chem, 35(6): 926–938

[69] Loewus F (1999). Biosynthesis and metabolism of ascorbic acid in plants and of analogs of ascorbic acid in fungi. Phytochemistry, 52(2): 193–210

[70] Loewus F A, Wagner G, Yang J C (1975). Biosynthesis and metabolism of ascorbic acid in plants. Ann N Y Acad Sci, 258(1 Second Confer): 7–23

[71] Ma J F, Hiradate S, Nomoto K, Iwashita T, Matsumoto H (1997a). Internal detoxification mechanism of Al in hydrangea. Plant Physiol, 113(4): 1033–1039

[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): 273–278

[73] Ma J F, Zheng S J, Matsumoto H, Hiradate S (1997b). Detoxifying aluminium with buckwheat. Nature, 390(6660): 569–570

[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): 4262–4266

[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): 281–285

[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): 435–448

[77] McConn M M, Nakata P A (2002). Calcium oxalate crystal morphology mutants from Medicago truncatula. Planta, 215(3): 380–386

[78] McConn M M, Nakata P A (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): 1371–1374

[79] McNair J B (1932). The interrelation between substances in plants: essential oils and resins, cyanogen and oxalate. Am J Bot, 19(3): 255–271

[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): 145

[81] Molano-Flores B (2001). Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae). Ann Bot (Lond), 88(3): 387–391

[82] Monje P V, Baran E J (2002). Characterization of calcium oxalates generated as biominerals in cacti. Plant Physiol, 128(2): 707–713

[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): 303–306

[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): 613–618

[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): 10–19

[86] Nakata P A (2003). Advances in our understanding of calcium oxalate crystal formation and function in plants. Plant Sci, 164(6): 901–909

[87] Nakata P A (2012). Influence of calcium oxalate crystal accumulation on the calcium content of seeds from Medicago truncatula. Plant Sci, 185-186(0): 246–249

[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): 425–430

[89] Nakata P A, McConn M (2002). Sequential subtractive approach facilitates identification of differentially expressed genes. Plant Physiol Biochem, 40(4): 307–312

[90] Nakata P A, McConn M M (2000). Isolation of Medicago truncatula mutants defective in calcium oxalate crystal formation. Plant Physiol, 124(3): 1097–1104

[91] Nakata P A, McConn M M (2003a). Calcium oxalate crystal formation is not essential for growth of Medicago truncatula. Plant Physiol Biochem, 41(4): 325–329

[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): 617–621

[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): 703–706

[94] Nakata P A, McConn M M (2007a). Calcium oxalate content affects the nutritional availability of calcium from Medicago truncatula leaves. Plant Sci, 172(5): 958–961

[95] Nakata P A, 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): 332–338

[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): 216–220

[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, 1091

[98] Nuss R F, Loewus F A (1978). Further studies on oxalic acid biosynthesis in oxalate-accumulating plants. Plant Physiol, 61(4): 590–592

[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): 77–116

[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): 559–562

[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): 208–215

[102] Parsons H T, Fry S C (2012). Oxidation of dehydroascorbic acid and 2,3-diketogulonate under plant apoplastic conditions. Phytochemistry, 75(0): 41–49

[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): 375–383

[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: 1187–1191

[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): 111–120

[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): 717–723

[107] Prychid C J, Jabaily R S, Rudall P J (2008). Cellular ultrastructure and crystal development in Amorphophallus (Araceae). Ann Bot (Lond), 101(7): 983–995

[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): 725–739

[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): 141–144

[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): 137–139

[111] Ritter M M C, Savage G P (2007). Soluble and insoluble oxalate content of nuts. J Food Compost Anal, 20(3–4): 169–174

[112] Ruiz N, Ward D, Saltz S (2002a). Calcium oxalate crystals in leaves of Pancratium sickenbergeri: constitutive or induced defense? Funct Ecol, 16(1): 99–105

[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): 472–479

[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, 265–290

[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): 527–560

[116] Saito K, Ohmoto J, Kuriha N (1997). Incorporation of ¹⁸O into oxalic, L-threonic and L-tartaric acids during cleavage of L-ascorbic and 5-keto-D-gluconic acids in plants. Phytochemistry, 44(5): 805–809

[117] Saltz S, Ward D (2000). Responding to a three-pronged attack: desert lilies subject to herbivory by dorcas gazelles. Plant Ecol, 148(2): 127–138

[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): 83–86

[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): 201–206

[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): 220–224

[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): 3008–3011

[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): 277–283

[123] Sugiyama N, Okutani I (1996). Relationship between nitrate reduction and oxalate synthesis in spinach leaves. J Plant Physiol, 149(1-2): 14–18

[124] Taylor G J (1991). Current views of the aluminum stress response; the physiological basis of tolerance. Curr Top Plant Biochem Physiol, 10: 57–93

[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): 120–131

[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): 710–718

[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): 131–137

[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): 34–45

[129] Wagner G, Loewus F (1973). The biosynthesis of (+)-tartaric acid in Pelargonium crispum. Plant Physiol, 52(6): 651–654

[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): 333–346

[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): 1903–1906

[132] Webb M A (1999). Cell-mediated crystallization of calcium oxalate in plants. Plant Cell, 11(4): 751–761

[133] Webb M A, Arnott H J (1981). An ultrastructural study of druse crystals in okra cotyledons. Scan Electron Microsc, 3: 285–292

[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: 1759–1770

[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): 633–648

[136] Weiner S, Addadi L (1991). Acidic macromolecules of mineralized tissues: the controllers of crystal formation. Trends Biochem Sci, 16(7): 252–256

[137] Xu H W, Ji X M, He Z H, Shi W 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): 1899–1908

[138] Yang J C, Loewus F A (1975). Metabolic conversion of L-ascorbic acid in oxalate-accumulating plants. Plant Physiol, 56(2): 283–285

[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): 1019–1026

[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): 1625–1634

[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: 80–85

[142] Zindler-Frank E (1976). Oxalate biosynthesis in relation to photosynthetic pathways and plant productivity: a survey. Z Pflanzenphysiol, 80: 1–13

[143] Zindler-Frank E (1987) Calcium oxalate in legumes. In: Advances in Legume Systematics (Stirton E, Ed.)Royal Botanic Gardens: Kew, UK, 279–316

[144] Zindler-Frank E (1991). Calcium oxalate crystal formation and growth in two legume species as altered by strontium. Bot Acta, 104: 229–232

[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): 139–144

Acknowledgments

Thanks go to Michele McConn, Bin Luo, and Justin Foster for comments on the manuscript. The contents of this publication do not necessarily reflect the views or policies of the US Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government. This research was supported in part by the US Department of Agriculture, Agricultural Research Service, under Cooperative Agreement number 58-6250-0-008.

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