Please wait a minute...
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front Biol    2012, Vol. 7 Issue (3) : 254-266    https://doi.org/10.1007/s11515-012-1224-0
REVIEW
Plant calcium oxalate crystal formation, function, and its impact on human health
Paul A. NAKATA()
USDA-ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030-2600, USA
 Download: PDF(471 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
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     
Corresponding Author(s): NAKATA Paul A.,Email:pnakata@bcm.tmc.edu   
Issue Date: 01 June 2012
 Cite this article:   
Paul A. NAKATA. Plant calcium oxalate crystal formation, function, and its impact on human health[J]. Front Biol, 2012, 7(3): 254-266.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-012-1224-0
https://academic.hep.com.cn/fib/EN/Y2012/V7/I3/254
Fig.1  Ultrastructure of the calcium oxalate raphide crystal idioblast. (A) Low magnification TEM of a cross-section through a developing raphide crystal idioblast and adjacent mesophyll cells (for comparison) from a leaf. Note some of the unique characteristic features of the crystal idioblast which include an enlarged nucleus, specialized plastids, increased ER, and unique vacuolar components. Bar= 2 μm. (B) Higher magnification view of crystal idioblast ER stacks, modified plastids, and adjacent mesophyll cells. The raphide calcium oxalate crystals appear as rectangular white profiles (*) within the vacuole. The ER stacks are denoted by arrows. Id, idioblast; m, mesophyll cell; n, nucleus; cl, chloroplast; p, plastid; v, vacuole; as, airspace. Bar= 1 μm. (Images used with permission from Elsevier, ).
Fig.2  Calcium oxalate crystal formation in high-capacity calcium regulation. High calcium flux can result in rapid formation of calcium oxalate crystals as exhibited in this sequential series of calcium treatments using a single live root of . Under calcium deficient conditions, the calcium bound in the crystal is remobilized for use in plant growth and development. Raphide bundles of calcium oxalate crystals appear as white blotches. (A) Longitudinal section through a root tip. RC, root cap; S, root stele; C, root cortex. Bar, 250 μm. (B) Whole-mount of live root tip after pretreated with 0 mM calcium solution as viewed between crossed-polarizers. (C) Whole-mount of the same live root tip after a 30 minute exposure to a 7 mM calcium solution as viewed between crossed-polarizers. (D) Whole-mount of the same live root tip viewed in (B) after returned to a 0 mM calcium solution for 3 hours as viewed between crossed-polarizers. (Images used with permission from Springer-Verlag, ).
Fig.3  Generation of a calcium oxalate deficient plant with improved calcium bioavailability. Wild-type and plants were grown hydroponically in the presence of Ca. (A) A comparison of the leaves (top) and calcium oxalate crystal phenotypes (bottom) of wild-type and 5. Note the crystals along the secondary vascular strand (boxed region on leaf image) in wild-type and the absence of crystals in the modified plant, 5. Bar= 25 μm. (B) Percent difference of the calcium found in the form of the calcium oxalate crystal in wild-type and 5. Both plants had similar calcium content but differed in the amount each sequestered as the calcium oxalate salt. (C) Percent difference in Ca absorbed and incorporated into the bones from wild-type and fed mice. Note, that the increase absorption and utilization of calcium from the modified plant was directly proportional to the decrease in the percentage of calcium bound in the oxalate crystal ().
FoodServing sizeCalcium content (mg)Fractional Absorption (%) *Est. absorbable Ca/serving (mg)
Cow milk1 cup2883292
Kale, boiled1 cup944139
Spinach, boiled1 cup244512
“No CaOx” spinach1 cup24441 ?100 ?
Tab.1  Potential nutritional impact
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, 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: 10.1086/337833
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: 10.1007/BF00392226
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: 10.1007/BF00392278
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: 10.1002/1521-3765(20010504)7:9<1881::AID-CHEM1881>3.0.CO;2-I pmid:11405466
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: 10.1016/j.jfca.2005.12.012
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: 10.1007/s004250000487 pmid:11523655
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: 10.3732/ajb.0800276 pmid:21628273
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: 10.1105/tpc.11.11.2233 pmid:10559446
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: 10.1152/ajprenal.00136.2006 pmid:17082348
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: 10.1007/BF02079332
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: 10.1007/BF02860532
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: 10.1073/pnas.90.15.6986 pmid:8346206
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, 113–130
20 Franceschi V R, Nakata P A (2005). Calcium oxalate in plants: formation and function. Annu Rev Plant Biol , 56(1): 41–71
doi: 10.1146/annurev.arplant.56.032604.144106 pmid:15862089
21 Franceschi V R, Schueren A M (1986). Incorporation of strontium into plant calcium oxalate crystals. Protoplasma , 130(2-3): 199–205
doi: 10.1007/BF01276601
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: 10.1104/pp.007062 pmid:12376632
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: 10.1007/BF00385088
24 Frey-Wyssling A (1981). Crystallography of the two hydrates of crystalline calcium oxalate in plants. Am J Bot , 68(1): 130–141
doi: 10.2307/2443000
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: 10.1016/j.cbpb.2009.07.011 pmid:19665573
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: 10.1080/00103627509366570
27 Gélinas B, Seguin P (2007). Oxalate in grain amaranth. J Agric Food Chem , 55(12): 4789–4794
doi: 10.1021/jf070384d pmid:17511467
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: 10.1038/nature03172 pmid:15608627
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: 10.1016/j.plaphy.2005.08.007 pmid:16310370
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: 10.1139/B07-046
31 Heaney R P, Recker R R, Hinders S M (1988). Variability of calcium absorption. Am J Clin Nutr , 47(2): 262–264
pmid:3341257
32 Heaney R P, Weaver C M (1989). Oxalate: effect on calcium absorbability. Am J Clin Nutr , 50(4): 830–832
pmid:2801588
33 Heaney R P, Weaver C M (1990). Calcium absorption from kale. Am J Clin Nutr , 51(4): 656–657
pmid:2321572
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:8819892
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: 10.1046/j.1523-1755.2001.00488.x pmid:11135080
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: 10.1086/317565
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: 10.2307/2442137
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: 10.1046/j.1469-8137.2003.00839.x
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: 10.1006/anbo.2001.1453
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: 10.1071/FP06269
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: 10.1007/s00709-007-0263-x pmid:17922267
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: 10.1139/b84-197
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: 10.1007/BF00391023
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: 10.1016/S0031-9422(99)00448-3 pmid:10731019
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: 10.1146/annurev.pp.46.060195.001321
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: 10.1104/pp.106.076737 pmid:16514014
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: 10.1007/BF01279061
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: 10.1016/S0168-9452(03)00160-2
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: 10.1016/S0981-9428(03)00011-1
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: 10.1071/FP06275
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: 10.1104/pp.125.2.634 pmid:11161021
55 Kr?ger N, Poulsen N (2008). Diatoms-from cell wall biogenesis to nanotechnology. Annu Rev Genet , 42(1): 83–107
doi: 10.1146/annurev.genet.41.110306.130109 pmid:18983255
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: 10.1139/b89-344
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: 10.1007/s00606-007-0620-4
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: 10.1007/s00606-008-0098-8
62 Lersten N, Horner H (2009). Crystal diversity and macropatterns in leaves of Oleaceae. Plant Syst Evol , 282(1--2): 87–102
doi: 10.1007/s00606-009-0209-1
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: 10.1007/BF00985267
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: 10.3732/ajb.1000247 pmid:21613079
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:2184039
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: 10.1104/pp.103.023556 pmid:14555781
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: 10.1021/jf00078a019
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: 10.1016/S0031-9422(99)00145-4
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: 10.1111/j.1749-6632.1975.tb29265.x pmid:1106305
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:12223659
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: 10.1016/S1360-1385(01)01961-6 pmid:11378470
73 Ma J F, Zheng S J, Matsumoto H, Hiradate S (1997b). Detoxifying aluminium with buckwheat. Nature , 390(6660): 569–570
doi: 10.1038/37518 pmid:9403684
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: 10.1021/jf010484y pmid:11559120
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: 10.1023/B:RUPP.0000019226.03536.21
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: 10.1111/j.1469-8137.2004.00923.x
77 McConn M M, Nakata P A (2002). Calcium oxalate crystal morphology mutants from Medicago truncatula. Planta , 215(3): 380–386
doi: 10.1007/s00425-002-0759-8 pmid:12111218
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: 10.1021/jf035332c pmid:14995148
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: 10.2307/2436337
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: 10.1186/1471-2229-9-145 pmid:19995454
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: 10.1006/anbo.2001.1492
82 Monje P V, Baran E J (2002). Characterization of calcium oxalates generated as biominerals in cacti. Plant Physiol , 128(2): 707–713
doi: 10.1104/pp.010630 pmid:11842173
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: 10.1016/j.jfca.2009.01.013
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: 10.1007/s11103-007-9180-9 pmid:17514431
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: 10.1640/0002-8444(2002)092[0010:CAWTIP]2.0.CO;2
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: 10.1016/S0168-9452(03)00120-1
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: 10.1016/j.plantsci.2011.11.004 pmid:22325887
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: 10.1016/S0981-9428(03)00049-4
89 Nakata P A, McConn M (2002). Sequential subtractive approach facilitates identification of differentially expressed genes. Plant Physiol Biochem , 40(4): 307–312
doi: 10.1016/S0981-9428(02)01380-3
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: 10.1104/pp.124.3.1097 pmid:11080287
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: 10.1016/S0981-9428(03)00026-3
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: 10.1016/S0168-9452(03)00013-X
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: 10.1071/FP06068
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: 10.1016/j.plantsci.2007.01.005
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: 10.1071/FP06268
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: 10.1016/j.plaphy.2007.01.013 pmid:17400466
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: 10.1104/pp.61.4.590 pmid:16660342
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: 10.1016/j.mser.2007.05.001
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: 10.1016/j.foodchem.2006.02.014
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: 10.1111/j.1570-7458.2009.00846.x
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: 10.1016/j.phytochem.2011.12.005 pmid:22226246
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: 10.1042/BJ20110939 pmid:21846329
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: 10.1046/j.1469-8137.2001.00075.x
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: 10.1016/j.plaphy.2009.03.010 pmid:19376730
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: 10.1093/aob/mcn022 pmid:18285357
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: 10.1006/anbo.1999.0975
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: 10.1111/j.1744-697X.2010.00186.x
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: 10.1023/A:1015189616477
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: 10.1016/j.jfca.2006.12.001
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: 10.1046/j.0269-8463.2001.00594.x
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: 10.1046/j.1365-2745.2002.00678.x
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: 10.1146/annurev.arplant.52.1.527 pmid:11337408
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: 10.1016/S0031-9422(96)00642-5
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: 10.1023/A:1009895512145
118 Savage G P, M?rtensson 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: 10.1016/j.jfca.2008.05.011
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: 10.1006/jfca.2000.0879
120 Siener R, H?now 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: 10.1016/j.foodchem.2005.05.059
121 Siener R, H?now R, Voss S, Seidler A, Hesse A (2006b). Oxalate content of cereals and cereal products. J Agric Food Chem , 54(8): 3008–3011
doi: 10.1021/jf052776v pmid:16608223
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: 10.1016/j.envexpbot.2009.07.007
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: 10.1016/S0176-1617(96)80166-0
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: 10.1016/j.cca.2005.11.033 pmid:16458875
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: 10.2307/2442029
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: 10.1007/s004680050197
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: 10.1055/s-2002-20434
129 Wagner G, Loewus F (1973). The biosynthesis of (+)-tartaric acid in Pelargonium crispum. Plant Physiol , 52(6): 651–654
doi: 10.1104/pp.52.6.651 pmid:16658623
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: 10.1023/B:JOEC.0000006363.34360.9d
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:3681480
132 Webb M A (1999). Cell-mediated crystallization of calcium oxalate in plants. Plant Cell , 11(4): 751–761
doi: 10.1105/tpc.11.4.751 pmid:10213791
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: 10.1046/j.1365-313X.1995.7040633.x
136 Weiner S, Addadi L (1991). Acidic macromolecules of mineralized tissues: the controllers of crystal formation. Trends Biochem Sci , 16(7): 252–256
doi: 10.1016/0968-0004(91)90098-G pmid:1926334
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: 10.1093/jxb/erj131 pmid:16595582
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: 10.1104/pp.56.2.283 pmid:16659288
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: 10.1104/pp.124.3.1019 pmid:11080279
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: 10.1093/jxb/erq028 pmid:20194922
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: 10.1078/0176-1617-00045
[1] Jalali, Seyyed Mostafa, Morteza Abdollahi, Atiyeh Hosseini, Dehghani Kari Bozorg, Ajami, Marjan Azadeh, Kimia Moiniafshar. The positive effects of Mediterranean-neutropenic diet on nutritional status of acute myeloid leukemia patients under chemotherapy[J]. Front. Biol., 2018, 13(6): 475-480.
[2] Hanane Gourine, Hadria Grar, Wafaa Dib, Nabila Mehedi, Ahmed Boualga, Djamel Saidi, Omar Kheroua. Effect of a normal protein diet on oxidative stress and organ damage in malnourished rats[J]. Front. Biol., 2018, 13(5): 366-375.
[3] Johanna Morrow, Kyle T. Willenburg, Emmanuel Liscum. Phototropism in land plants: Molecules and mechanism from light perception to response[J]. Front. Biol., 2018, 13(5): 342-357.
[4] Amir Abdoli. High salt and fat intake, inflammation, and risk of cancer[J]. Front. Biol., 2017, 12(6): 387-391.
[5] Lijun WANG, Marit NILSEN-HAMILTON. Biomineralization proteins: from vertebrates to bacteria[J]. Front Biol, 2013, 8(2): 234-246.
[6] WANG Lihong, LIN Liu, ZHANG Li, HE Qian, ZHANG Jinguo. Analysis of nutrient components of food for Asian Elephants in the wild and in captivity[J]. Front. Biol., 2007, 2(3): 351-355.
[7] Jia Gang, Feng Jian, Qin Zhibiao. Studies on the Fatty Liver Diseases of Sciaenops ocellatus Caused by Different Ether Extract Levels in Diets[J]. Front. Biol., 2006, 1(1): 9-12.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed