Advances in our understanding of calcium oxalate crystal formation and function in plants

doi:10.1016/S0168-9452(03)00120-1

Plant Science

Volume 164, Issue 6, June 2003, Pages 901-909

https://doi.org/10.1016/S0168-9452(03)00120-1 Get rights and content

Abstract

Calcium oxalate crystal formation in plants appears to play a central role in a variety of important functions, including tissue calcium regulation, protection from herbivory, and metal detoxification. Evidence is mounting to support ascorbic acid as the primary precursor to oxalate biosynthesis. The ascorbic acid utilized in oxalate biosynthesis is synthesized directly within the calcium oxalate crystal-accumulating cell, called the crystal idioblast. Several unique features of the crystal idioblast have been proposed as factors that influence calcium oxalate formation. These features include an abundance of endoplasmic reticulum (ER), acidic proteins, cytoskeletal components, and the intravacuolar matrix. A number of mutants defective in different aspects of calcium oxalate crystal formation have been isolated. Cellular and biochemical characterizations of the various mutants have revealed mutations affecting crystal nucleation, morphology, distribution, and/or amount. Such mutants will be useful tools in continued efforts to decipher the pathways of crystal formation and function in plants.

Introduction

The plant calcium oxalate crystal is considered one of the first reported objects to have been seen under a light microscope [1]. Since this initial report, oxalate crystals have been found throughout nature. They have been observed [2] in rocks, soil, and among multiple members of all of the five kingdoms (Monera, Protista, Fungi, Plantae, and Animalia). In all cases, the crystals are formed from environmentally derived calcium and from biologically synthesized oxalate.

In plants, calcium oxalate deposition is common. Members of more than 215 plant families accumulate crystals within their tissues [3]. Oxalate-producing plants, which include many crop plants, accumulate oxalate in the range of 3–80% (w/w) of their dry weight. As much as 90% of the total calcium of a plant can be found as the oxalate salt [4], [5], [6], [7]. Crystals have been observed in virtually all the tissues of a plant. In whatever tissue the crystals are found, they most often accumulate within the vacuoles of specialized cells called crystal idioblasts [7].

Plants produce a variety of calcium oxalate crystal shapes and sizes. Most crystals can be classified into one of five categories, based on their morphology: crystal sand, raphide, druse, styloid, and prismatic [8]. Usually, the morphology of a crystal, as well as its spatial distribution, is conserved within specific taxa. Several functions for crystal formation in plants have been proposed, based on such properties [8].

This review will delineate the ways in which the strides made in recent studies contribute to our current understanding of calcium oxalate formation and its functions in plants. Additional information is available to obtain a more comprehensive understanding of calcium oxalate in plants from earlier reviews [5], [7], [8], [9], [10], [11], [12].

Section snippets

Proposed functions of calcium oxalate

The diversity of crystal shapes and sizes, as well as their prevalence and spatial distribution, have led to a number of hypotheses regarding crystal function in plants. The proposed functions include calcium regulation, ion balance (e.g. sodium and potassium), plant protection, tissue support (plant rigidity), detoxification (e.g. heavy metals or oxalic acid), and light gathering and reflection [8]. Although evidence in support of many of these hypotheses is still lacking, support for a role

Oxalate biosynthesis

A number of pathways for oxalate production have been hypothesized. These pathways include the cleavage of isocitrate, hydrolysis of oxaloacetate, glycolate/glyoxylate oxidation, and/or oxidative cleavage of L-ascorbic acid [2]. Biochemical measurements, using radio-labeled precursors, support a C2/C3 cleavage of ascorbic acid as a major pathway of oxalate production [51], [52], [53], [54], [55], [56], [57]. Recently, there has been renewed interest in ascorbate as the precursor to oxalate

Calcium oxalate crystal formation

Crystals of calcium oxalate are usually formed in a defined shape and spatial location. This property may be a useful feature in plant taxonomy and systematics [7], [22], [64]. Spatially, crystal formation most commonly occurs inside the vacuoles of specialized cells called crystal idioblasts. Crystal idioblasts exhibit characteristic features including an enlarged nucleus, specialized plastids, increased ER, elevated levels of rRNA, and unique vacuolar components [7], [8], [9], [65].

Isolation of mutants of calcium oxalate formation

To complement existing biochemical and cellular investigations efforts have been made to identify a suitable genetic system to study calcium oxalate formation. A recent report [89] offered the model legume Medicago truncatula as such a system. Key attributes of M. truncatula include its short generation time, small genome size (three to four times the size of Arabidopsis), ability to be transformed, autogamous and diploid nature, and spatial pattern of calcium oxalate crystal formation [90]. By

Plant oxalates and human health

Oxalate in plant foods impacts human health in at least two significant ways [2], [5], [95]. First, oxalate is an antinutrient in that it renders calcium unavailable for nutritional absorption by humans [96], [97]. This issue of calcium bioavailability is important when one considers the reliance of different populations around the world on plant foods as their main source of calcium and other minerals, as well as the failure of many people in the United States to meet the recommended daily

Conclusion

Although much remains to be discovered about calcium oxalate crystal formation and function in plants, recent reports show that progress is being made. Studies indicate that the pathway of oxalate biosynthesis utilizes ascorbate as the primary precursor, and that the ascorbate utilized is produced directly within the crystal idioblast itself. Plant oxalate production appears to serve diverse functional roles that protect the plant from succumbing to a variety of environmental stresses such as

Acknowledgements

Thanks goes to Dr Todd Kostman and Dr Vincent Franceschi for contributing images to this review. This research was supported in part by the U.S. Department of Agriculture, Agricultural Research Service, under Cooperative Agreement number 58-6250-6-001.

References (105)

E. Zindler-Frank
Oxalate biosynthesis in relation to photosynthetic pathways and plant productivity: a survey
Z. Pflanzenphysiol.
(1976)
E. Zindler-Frank
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.
(1975)
V.R. Franceschi et al.
Use of Psychotria puncata callus in study of calcium oxalate crystal idioblast formation
Z. Pflanzenphysiol.
(1979)
H. Ilarslan et al.
Calcium oxalate crystals in developing seeds of soybean
Ann. Bot.
(2001)
E. Zindler-Frank et al.
Calcium and oxalate content of the leaves of Phaseolus vulgaris at different calcium supply in relation to calcium oxalate crystal formation
J. Plant Physiol.
(2001)
B. Molano-Flores
Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae)
Ann. Bot.
(2001)
A.-L. Cogne et al.
Study of two plants used in traditional medicine in Zimbabwe for skin problems and rhematism: Dioscorea sylvatica and Urginea altissima
J. Ethnopharmacol.
(2001)
J.F. Ma et al.
Aluminium tolerance in plants and the complexing role of organic acids
Trends Plant Sci.
(2001)
K. Saito et al.
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
(1997)
F. Loewus
Biosynthesis and metabolism of ascorbic acid in plants and of analogs of ascorbic acid in fungi
Phytochemistry
(1999)

S.A. Keates et al.

L-Ascorbic acid and L-galactose are sources of oxalic acid and calcium oxalate in Pistia stratiotes

Phytochemistry

(2000)

P.A. Nakata et al.

Influence of the calcium oxalate defective 4 (cod4) mutation on the growth, oxalate content, and calcium content of Medicago truncatula

Plant Sci.

(2003)

P.A. Nakata

Calcium oxalate crystal morphology

Trends Plant Sci.

(2002)

R.P. Holmes et al.

Glyoxylate synthesis and its modulation and influence on oxalate synthesis

J. Urol.

(1998)

R.P. Heaney et al.

Calcium absorbability from spinach

Am. J. Clin. Nutr.

(1988)

C.-L. Chen et al.

Acute oxalate nephropathy after ingestion of star fruit

Am. J. Kidney Dis.

(2001)

A. Bhandari et al.

Effects of oxalate on HK-2 cells, a line of proximal tubular epithelial cells from normal human kidney

J. Urol.

(2002)

A. Leeuwenhoek

Microscopical observations

Philos. Trans. R. Soc. Lond.

(1975)

A. Hodgkinson

Oxalic acid metabolism in higher plants

J.B. McNair

The intersection between substances in plants: essential oils and resins, cyanogen and oxalate

Am. J. Bot.

(1932)

B. Libert et al.

Oxalate in crop plants

J. Agric. Food. Chem.

(1987)

R.N. Gallaher

The occurrence of calcium in plant tissue as crystals of calcium oxalate

Comm. Soil Sci. Plant Anal.

(1975)

H.T. Horner et al.

Calcium oxalate formation in higher plants

V.R. Franceschi et al.

Calcium oxalate crystals in plants

Bot. Rev.

(1980)

H.J. Arnott et al.

Calcification in plants

E. Zindler-Frank

Calcium oxalate in legumes

V.R. Franceschi et al.

Oxalate biosynthesis and function in plants and fungi

M.A. Webb

Cell-mediated crystallization of calcium oxalate in plants

Plant Cell

(1999)

R. Borchert

Calcium-induced patterns of calcium-oxalate crystals in isolated leaflets of Gleditsia triacanthos L. and Albizia julibrissin Durazz

Planta

(1985)

R. Borchert

Calcium acetate induces calcium uptake and formation of calcium-oxalate crystals in isolated leaflets of Gleditsia tracanthos L

Planta

(1986)

V.R. Franceschi

Calcium oxalate formation is a rapid and reversible process in Lemna minor L

Protoplasma

(1989)

L.L. Kuo-Huang et al.

Structure of crystal cells and influences of leaf development on crystal cell development and vice versa in Phaseolus vulgaris (Leguminosae)

Bot. Acta

(1998)

S.V. Pennisi et al.

Inducible calcium sinks and preferential calcium allocation in leaf primordia of Dracaena sanderiana Hort. Sander ex M.T. Mast. (Dracaenaceae)

HortSci.

(2001)

P.V. Monje et al.

Characterization of calcium oxalates generated as biominerals in cacti

Plant Physiol.

(2002)

G.M. Volk et al.

The role of druse and raphide calcium oxalate crystals in tissue calcium regulation in Pistia stratiotes leaves

Plant Biol.

(2002)

A.C. Morrow et al.

Crystals associated with the intertracheid pit membrane of the woody fern Botrychium multifidum

Am. Fern J.

(2002)

J. Calmes et al.

Seasonal variations of calcium oxalate crystals in tissues of Vigne vierge

Can. J. Bot.

(1977)

V.R. Tilton et al.

Calcium oxalate raphide crystals and crystalliferous idioblasts in the carpels of Ornithogalum caudatum

Ann. Bot.

(1980)

H. Ilarslan et al.

Quantitative determination of calcium oxalate in developing seeds of soybean (Leguminosae)

Am. J. Bot.

(1997)

D.S. Finley

Patterns of calcium oxalate crystals in young tropical leaves: a possible role as an anti-herbivory defense

Rev. Biol. Trop.

(1999)

E. Tillman-Sutela et al.

Calcium oxalate crystals in the mature seeds of Norway spruce, Picea abies (L.) Karst

Trees

(1999)

S. Saltz et al.

Responding to a three-pronged attack: desert lilies subject to herbivory by dorcas gazelles

Plant Ecol.

(2000)

N. Ruiz et al.

Calcium oxalate crystals in leaves of Pancratium sickenbergeri: constitutive or induced defense?

Funct. Ecol.

(2002)

N. Ruiz et al.

Responses of Pancratium sickenbergeri to simulated bulb herbivory: combining defence and tolerance strategies

J. Ecol.

(2002)

D. Ward et al.

Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lilly

J. Chem. Ecol.

(1997)

D.B. Bruynzeel

Bulb dermatitis: dermatological problems in the flower bulb industries

Contact Dermatitis

(1997)

C.G. Julian et al.

The nature and distribution of daffodil picker's rash

Contact Dermatitis

(1997)

J.H. Bradbury et al.

The acridity of raphides from the edible aroids

J. Sci. Food Agric.

(1998)

M.L. Salinas et al.

Irritant contact dermatitis caused by needle-like calcium oxalate crystals, raphides, in Agave tequilana among workers in tequila distilleries and agave plantations

Contact Dermatitis

(2001)

P.R. Ryan et al.

Function and mechanism of organic anion exudation from plant roots

Annu. Rev. Plant Physiol. Plant Mol. Biol.

(2001)

Cited by (364)

Pathophysiology and management of enteric hyperoxaluria
2024, Clinics and Research in Hepatology and Gastroenterology
Enteric hyperoxaluria is a metabolic disorder resulting from conditions associated with fatty acid malabsorption and characterized by an increased urinary output of oxalate. Oxalate is excessively absorbed in the gut and then excreted in urine where it forms calcium oxalate crystals, inducing kidney stones formation and crystalline nephropathies. Enteric hyperoxaluria is probably underdiagnosed and may silently damage kidney function of patients affected by bowel diseases. Moreover, the prevalence of enteric hyperoxaluria has increased because of the development of bariatric surgical procedures. Therapeutic options are based on the treatment of the underlying disease, limitation of oxalate intakes, increase in calcium salts intakes but also increase in urine volume and correction of hypocitraturia. There are few data regarding the natural evolution of kidney stone events and chronic kidney disease in these patients, and there is a need for new treatments limiting kidney injury by calcium oxalate crystallization.
Ca-oxalate crystals are involved in cadmium storage in a high Cd accumulating cultivar of cacao
2024, Environmental and Experimental Botany
Cadmium (Cd) concentrations in cacao often exceed food limits. A better understanding of the molecular mechanisms of Cd accumulation in cacao trees is necessary to advance Cd mitigation strategies. This study explores Cd distribution and speciation (i.e., chemical form) within the vegetative organs of a high Cd accumulating cacao cultivar growing in soil with background Cd concentrations (0.28 mg Cd kg⁻¹) by synchrotron radiation-based micro- and nano-X-ray fluorescence imaging and X-ray absorption spectroscopy on duplicate samples of roots, young branches, mature branches, and leaves. In both the roots and branches, the incorporation of Cd in Ca-oxalate crystals with binding to oxygen-ligands was identified as a major mechanism of Cd regulation. The Ca-oxalate crystals were more abundant in the branches than in the roots. We suggest that the incorporation of Cd into the Ca-oxalate crystals may limit the transfer of Cd to other organs like the leaves and beans. The roots also featured Cd-sulfur species in dilated cells of the wood, probably for the retention of Cd in the roots by strong binding with Cd to thiol-containing ligands. A Cd hotspot in large, secreting channels of the branches suggested that mucilage may play a role in the transport of Cd within cacao trees. The leaves had local Cd enrichments in the parenchymatous tissues and displayed a higher Cd concentration in the mesophyll compared to the epidermis. These insights in Cd distribution and speciation underscore that Theobroma cacao L. develops original Cd detoxification strategies, strongly different from non-tolerant species such as cereals.
Effect of cooking on structural changes in the common black bean (Phaseolus vulgaris var. Jamapa)
2024, Heliyon
The cooking process is fundamental for bean consumption and to increase the bioavailability of its nutritional components. The study aimed to determine the effect of cooking on bean seed coat through morphological analyses with different microscopy techniques and image analyses. The chemical composition and physical properties of raw black bean (RBB) and cooked black bean (CBB) seeds were determined. The surface and cross-sectional samples were studied by Optical microscopy (OM), environmental scanning electron microscopy (ESEM), atomic force microscopy (AFM) and confocal laser scanning microscopy (CLSM). The composition of samples showed significant differences after the cooking process. OM images and gray level co-occurrence matrix algorithm (GLCM) analysis indicated that cuticle-deposited minerals significantly influence texture parameters. Seed coat surface ESEM images showed cluster cracking. Texture fractal dimension and lacunarity parameters were effective in quantitatively assessing cracks on CBB. AFM results showed arithmetic average roughness (R_a) (121.67 nm) and quadratic average roughness (R_q) (149.94 nm). The cross-sectional ESEM images showed a decrease in seed coat thickness. The CLSM results showed an increased availability of lipids along the different multilayer tissues in CBB. The results generated from this research work offer a valuable potential to carry out a strict control of bean seed cooking at industrial level, since the structural changes and biochemical components (cell wall, lipids and protein bodies) that occur in the different tissues of the seed are able to migrate from the inside to the outside through the cracks generated in the multilayer structure that are evidenced by the microscopic techniques used.
Rhubarb: A novel model plant to study the conundrum of calcium oxalate synthesis
2024, Food Chemistry
The study investigated calcium oxalate (CaOx) crystal composition, accumulation, synthesis, and degradation in five rhubarb species from the North-Western Indian Himalayas. Techniques like optical and scanning electron microscopy (SEM), SEM-energy-dispersive X-ray spectroscopy (SEM-EDS), inductively coupled plasma-optical emission spectrometry (ICP-OES), X-ray diffraction spectroscopy (XRD), and real-time (qRT-PCR) expression analysis of strategic genes were used to understand the processes of oxalate synthesis and precipitation. Results showed crystals tend to accumulate around vascular bundles in all species, irrespective of size, indicating a consistent pattern. Crystal synthesis and accumulation were stress-driven, linked to substrate composition, and in planta soluble oxalate and calcium levels, paralleling oxalate precursors. Based on their availability, CaOx crystals precipitated heavy metals mostly associated with its weddellite form. Crystal content correlated positively with mRNA levels of calcium/oxalate/ascorbate-related and stress-responsive genes, and negatively with oxalate oxidation/decarboxylation genes. CaOx crystals were suggested as potential biominerals for addressing heavy metal stress in agriculture.
Methodologies for determining oxalic acid in plant species consumed by humans: An integrative review
2023, Journal of Herbal Medicine
Plant species are highly consumed worldwide. Plant matrices are complex, containing bioactive compounds with pharmacological and/or toxicological effects. For example, oxalic acid or oxalate is a metabolite present at high concentrations in different plant species. Its consumption can cause short- and long-term renal complications, especially if plasma concentration is ≥ 0.8–2.5 μmol.L⁻¹ and urinary concentration is ≥ 20–30 mg 0.24 h⁻¹. People predisposed to kidney complications (e.g. those with noncommunicable chronic diseases - NCDs) make use of medicinal plant species as adjuvant therapy. This study consists of an integrative review of the main analytical methods for quantifying oxalic acid in plant species consumed by humans.
The authors conducted a search of the databases ScienceDirect, Web of Science, Scopus, Pubmed, and Scielo for publications from 2010 to 2020. A total of 808 studies were initially identified, out of which 21 were included in the review.
Oxalic acid was predominantly identified using chromatographic methods in over 140 plant species of food and medicinal interest. The total concentration of oxalic acid/oxalate ranged from undetected to 6.2 g per 100 g of dry plant matter.
The presence of oxalic acid in plant species raises concerns because of its role in the development or exacerbation of kidney problems. This concern has driven significant scientific research on the topic. However, most of the studies lack a comprehensive and validated methodological description.
Effects of exogenous calcium on cadmium accumulation in amaranth
2023, Chemosphere
Calcium oxalate (CaOx) crystals in plants act as a sink for excess Ca and play an essential role in detoxifying heavy metals (HMs). However, the mechanism and related influencing factors remain unclear. Amaranth (Amaranthus tricolor L.) is a common edible vegetable rich in CaOx and a potential Cd hyperaccumulation species. In this study, the hydroponic experiment was carried out to investigate the effect of exogenous Ca concentrations on Cd uptake by amaranth. The results showed that either insufficient or excess Ca supply inhibited amaranth growth, while the Cd bioconcentration factor (BCF) increased with Ca concentration. Meanwhile, the sequence extraction results demonstrated that Cd mainly accumulated as pectate and protein-bound species (NaCl extracted) in the root and stem, compared to pectate, protein, and phosphate-bound (acetic acid extractable) species in the leaf. Correlation analysis showed that the concentration of exogenous Ca was positively correlated with amaranth-produced CaOx crystals but negatively correlated with insoluble oxalate-bound Cd in the leaf. However, since the accumulated insoluble oxalate-bound Cd was relatively low, Cd detoxification via the CaOx pathway in amaranth is limited.

View all citing articles on Scopus

^☆: The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.

View full text

Published by Elsevier Ireland Ltd.

ReviewAdvances in our understanding of calcium oxalate crystal formation and function in plants☆

Abstract

Introduction

Section snippets

Proposed functions of calcium oxalate

Oxalate biosynthesis

Calcium oxalate crystal formation

Isolation of mutants of calcium oxalate formation

Plant oxalates and human health

Conclusion

Acknowledgements

Z. Pflanzenphysiol.

Z. Pflanzenphysiol.

Z. Pflanzenphysiol.

Ann. Bot.

J. Plant Physiol.

Ann. Bot.

J. Ethnopharmacol.

Trends Plant Sci.

Phytochemistry

Phytochemistry

Phytochemistry

Plant Sci.

Trends Plant Sci.

J. Urol.

Am. J. Clin. Nutr.

Am. J. Kidney Dis.

J. Urol.

Microscopical observations

Philos. Trans. R. Soc. Lond.

Oxalic acid metabolism in higher plants

The intersection between substances in plants: essential oils and resins, cyanogen and oxalate

Am. J. Bot.

Oxalate in crop plants

J. Agric. Food. Chem.

The occurrence of calcium in plant tissue as crystals of calcium oxalate

Comm. Soil Sci. Plant Anal.

Calcium oxalate formation in higher plants

Calcium oxalate crystals in plants

Bot. Rev.

Calcification in plants

Calcium oxalate in legumes

Oxalate biosynthesis and function in plants and fungi

Cell-mediated crystallization of calcium oxalate in plants

Plant Cell

Calcium-induced patterns of calcium-oxalate crystals in isolated leaflets of Gleditsia triacanthos L. and Albizia julibrissin Durazz

Planta

Calcium acetate induces calcium uptake and formation of calcium-oxalate crystals in isolated leaflets of Gleditsia tracanthos L

Planta

Calcium oxalate formation is a rapid and reversible process in Lemna minor L

Protoplasma

Structure of crystal cells and influences of leaf development on crystal cell development and vice versa in Phaseolus vulgaris (Leguminosae)

Bot. Acta

Inducible calcium sinks and preferential calcium allocation in leaf primordia of Dracaena sanderiana Hort. Sander ex M.T. Mast. (Dracaenaceae)

HortSci.

Characterization of calcium oxalates generated as biominerals in cacti

Plant Physiol.

The role of druse and raphide calcium oxalate crystals in tissue calcium regulation in Pistia stratiotes leaves

Plant Biol.

Crystals associated with the intertracheid pit membrane of the woody fern Botrychium multifidum

Am. Fern J.

Seasonal variations of calcium oxalate crystals in tissues of Vigne vierge

Can. J. Bot.

Calcium oxalate raphide crystals and crystalliferous idioblasts in the carpels of Ornithogalum caudatum

Ann. Bot.

Quantitative determination of calcium oxalate in developing seeds of soybean (Leguminosae)

Am. J. Bot.

Patterns of calcium oxalate crystals in young tropical leaves: a possible role as an anti-herbivory defense

Rev. Biol. Trop.

Calcium oxalate crystals in the mature seeds of Norway spruce, Picea abies (L.) Karst

Trees

Responding to a three-pronged attack: desert lilies subject to herbivory by dorcas gazelles

Plant Ecol.

Calcium oxalate crystals in leaves of Pancratium sickenbergeri: constitutive or induced defense?

Funct. Ecol.

Responses of Pancratium sickenbergeri to simulated bulb herbivory: combining defence and tolerance strategies

J. Ecol.

Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lilly

J. Chem. Ecol.

Bulb dermatitis: dermatological problems in the flower bulb industries

Review
Advances in our understanding of calcium oxalate crystal formation and function in plants☆