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

  • Paul A. NAKATA
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  • USDA-ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030-2600, USA

Received date: 18 Jan 2012

Accepted date: 26 Feb 2012

Published date: 01 Jun 2012

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

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.

Cite this article

Paul A. NAKATA . Plant calcium oxalate crystal formation, function, and its impact on human health[J]. Frontiers in Biology, 2012 , 7(3) : 254 -266 . DOI: 10.1007/s11515-012-1224-0

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.
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

DOI

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

PMID

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

PMID

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

PMID

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

PMID

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

DOI PMID

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI

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

DOI

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

DOI

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

DOI

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

DOI PMID

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

DOI

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

PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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