Plant Biol (Stuttg) 2002; 4(1): 34-45
DOI: 10.1055/s-2002-20434
Original Paper
Georg Thieme Verlag Stuttgart ·New York

The Role of Druse and Raphide Calcium Oxalate Crystals in Tissue Calcium Regulation in Pistia stratiotes Leaves

G. M. Volk 2 , V. J. Lynch-Holm 1 , T. A. Kostman 3 , L. J. Goss 1 , V. R. Franceschi 1
  • Current addresses: 1 School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA
  • 2 United States Department of Agriculture, Agricultural Research Service, National Seed Storage Laboratory, 1111 S. Mason St., Fort Collins, CO 80521, USA
  • 3 Department of Biology and Microbiology, University of Wisconsin Oshkosh, 800 Algoma Boulevard, Oshkosh, WI 54901-8640, USA
Further Information

Publication History

January 5, 2001

December 18, 2001

Publication Date:
28 February 2002 (online)

Abstract

Ca oxalate crystal formation was examined in Pistia stratiotes L. leaves during excess Ca and Ca-deficient conditions. Pistia produces druse crystal idioblasts in the adaxial mesophyll and raphide idioblasts in the abaxial aerenchyma. Raphide crystals were previously found to grow bidirectionally, and here we show that Ca is incorporated along the entire surfaces of developing druse crystals, which are coated with membrane-bound microprojections. Leaves formed on plants grown on 0 Ca medium have fewer and smaller druse crystals than leaves formed under 5 mM Ca (“control”) conditions, while raphide crystal formation is completely inhibited. When plants were moved from 0 to 15 mM (“high”) Ca, the size and number of crystals in new leaves returned to (druse) or exceeded (raphide) control levels. High Ca also induced formation of druse, but not raphide, crystals in differentiating chlorenchyma cells. When plants were transferred from 15 mM Ca to 0 Ca, young druse crystals were preferentially partially dissolved. Oxalate oxidase, an enzyme that degrades oxalate, increased during Ca deficiency and was localized to the crystal surfaces. The more dynamic nature of druse crystals is not due to hydration form as both crystal types are shown to be monohydrate. Part of the difference may be because raphide idioblasts have developmental constraints that interfere with a more flexible response to changing Ca. These studies demonstrate that excess Ca can be stored as Ca oxalate, the Ca can be remobilized under certain conditions, and different forms of Ca oxalate have different roles in bulk Ca regulation.

References

  • 01 Al-Rais,  A. H.,, Myers,  A.,, and Watson,  L.. (1971);  The isolation and properties of oxalate crystals from plants.  Annals Botany. 35 1213-1218
  • 02 Arnott,  H. J., and Pautard,  F. G. E.. (1970) Calcification in plants. Biological calcification; cellular and molecular aspects. Schraer, H., ed. New York; Appleton-Century-Crofts pp. 375-446
  • 03 Assailly,  A.. (1954);  Sur les rapports de l'oxalate de chaux et de l'amidon.  Compt. Rend. Acad. Sci. Ser. D Paris. 238 1902-1904
  • 04 Borchert,  R.. (1985);  Calcium-induced patterns of calcium-oxalate crystals in isolated leaflets of Gleditsia triacanthos L. and Albizia julibrissin Durazz.  Planta. 165 301-310
  • 05 Borchert,  R.. (1986);  Calcium acetate induces calcium uptake and formation of calcium-oxalate crystals in isolated leaflets of Gleditsia triacanthos L.  Planta. 168 571-578
  • 06 Borchert,  R.. (1990);  Ca2+ as developmental signal in the formation of Ca-oxalate crystal spacing patterns during leaf development in Carya ovata. .  Planta. 182 339-347
  • 07 Calmes,  M. J.. (1969);  Contribution a l'etude du metabolisme de l'acide oxalique chez la Vigne vierge (Parthenocissus tricuspidata Planchon).  Compt. Rend. Acad. Sci., Ser. D. 269 704-707
  • 08 Calmes,  J., and Carles,  J.. (1970);  Le repartition et l'evolution des cristaux d'oxalate de calcium dans les tissues de Vigne vierge au cours d'un cycle de vegetation.  Bull. Soc. Bot. Fr.. 117 189-198
  • 09 Foster,  A. S.. (1956);  Plant idioblasts: remarkable examples of cell specialization.  Protoplasma. 46 184-193
  • 10 Franceschi,  V. R.. (1984);  Developmental features of calcium oxalate crystal sand deposition in Beta vulgaris L. leaves.  Protoplasma. 120 216-223
  • 11 Franceschi,  V. R.. (1987);  Oxalic acid metabolism and calcium oxalate formation in Lemna minor L.  Plant Cell Environ.. 10 397-406
  • 12 Franceschi,  V. R.. (1989);  Calcium oxalate formation is a rapid and reversible process in Lemna minor L.  Protoplasma. 148 130-137
  • 13 Franceschi,  V. R., and Horner,  H. T. Jr.. (1980);  Calcium oxalate crystals in plants.  Bot. Rev.. 46 361-427
  • 14 Franceschi,  V. R., and Loewus,  F. A.. (1995) Oxalate biosynthesis and function in plants and fungi. Calcium oxalate in biological systems. Khan, S. R., ed. Boca Raton; CRC Press, Inc. pp. 117-121
  • 15 Franceschi,  V. R.,, Li,  L.,, Zhang,  D.,, and Okita,  T. O.. (1993);  Calsequestrin-like calcium binding protein is expressed in calcium accumulating cells of Pistia stratiotes. .  Proc. Natl. Acad. Sci. USA. 90 6986-6990
  • 16 Frank,  E.. (1972);  The formation of crystal idioblasts in Canavalia ensiformis D. C. at different levels of calcium supply.  Z. Pflanzenphysiol.. 67 350-358
  • 17 Frey-Wyssling,  A.. (1981);  Crystallography of the two hydrates of crystalline calcium oxalate in plants.  Amer. J. Bot.. 68 130-141
  • 18 Hepler,  P. K., and Wayne,  R. O.. (1985);  Calcium and plant development.  Ann. Rev. Plant Physiol.. 36 397-439
  • 19 Horner,  H. T., and Wagner,  B. L.. (1980);  The association of druse crystals with the developing stomium of Capsicum annum (Solanaceae) anthers.  Amer. J. Bot.. 67 1347-1360
  • 20 Horner,  H. T., and Wagner,  B. L.. (1995) Calcium oxalate formation in higher plants. Calcium Oxalate in Biological Systems. Khan, S. R., ed. Boca Raton; CRC Press pp. 53-72
  • 21 Keates,  S. E.,, Tarlyn,  N. M.,, Loewus,  F. A.,, and Franceschi,  V. R.. (2000);  L-Ascorbic acid and L-galactose are sources for oxalic acid and calcium oxalate in Pistia stratiotes. .  Phytochemistry. 53 433-440
  • 22 Kirkby,  E. A., and Pilbeam,  D. J.. (1984);  Calcium as a plant nutrient.  Plant Cell Environ.. 7 397-405
  • 23 Klauer,  S. F., and Franceschi,  V. R.. (1996);  Accumulation of vegetative storage proteins in vacuoles of soybean leaf paraveinal mesophyll is mediated by the Golgi apparatus.  Protoplasma. 200 174-185
  • 24 Kostman,  T. A., and Franceschi,  V. R.. (2000);  Cell and calcium oxalate crystal growth is coordinated to achieve high capacity calcium regulation in plants.  Protoplasma. 214 166-179
  • 25 Kostman,  T. A.,, Tarlyn,  N. M.,, Loewus,  F. A.,, and 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 1-7
  • 26 Kuballa,  B.,, Lugnier,  A. A. J.,, and Anton,  R.. (1981);  Study of Dieffenbachia-induced edema in mouse and rat hindpaw: respective role of oxalate needles and trypsin-like protease.  Toxicol. Appl. Pharmacol.. 58 441-451
  • 27 Lane,  B. G.. (1994);  Oxalate, germin, and the extracellular matrix of higher plants.  FASEB J.. 8 294-301
  • 28 Laemmli,  U. K.. (1970);  Cleavage of structural proteins during the assembly of the head of bacteriophage T4.  Nature. 227 680-685
  • 29 Libert,  B., and Franceschi,  V. R.. (1987);  Oxalate in crop plants.  J. Agric.Food Chem.. 35 926-938
  • 30 Monje,  P. V., and Baran,  E. J.. (1996);  On the formation of weddellite in Cahmaecereus silvestrii, a Cactaceae from northern Argentina.  Z. Naturforsch.. 51 c 426-428
  • 31 Monje,  P. V., and Baran,  E. J.. (1997);  On the formation of whewellite in the Cactaceae species Opuntia microdasys. .  Z. Naturforsch.. 52 c 267-269
  • 32 Rauber,  A.. (1985);  Observations on the idioblasts of Dieffenbachia. .  Clin. Toxicol.. 23 79-80
  • 33 Rivera,  E. R., and Smith,  B. N.. (1979);  Crystal morphology and 13Carbon/12Carbon composition of solid oxalate in cacti.  Plant Physiol.. 64 966-970
  • 34 Sakai,  W. S.,, Hanson,  M.,, and Jones,  R. C.. (1972);  Raphides with barbs and grooves in Xanthosoma sagittifolium (Araceae).  Science. 178 314-315
  • 35 Sakai,  W. S.,, Shiroma,  S. S.,, and Nagao,  M. A.. (1984);  A study of raphide microstructure in relation to irritation.  SEM. 2 979-986
  • 36 Schmidt,  R. J., and Moult,  S. P.. (1983);  The dermatitic properties of black bryony (Tamus communis L.).  Contact Derm.. 9 390-396
  • 37 Tarlyn,  N. M.,, Kostman,  T. A.,, Nakata,  P. A.,, Keates,  S. E.,, and Franceschi,  V. R.. (1998);  Axenic culture of Pistia stratiotes for use in plant biochemical studies.  Aquatic Botany. 60 161-168
  • 38 Towbin,  H.,, Stahelin,  T.,, and Gordon,  J.. (1979);  Electrophorectic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications.  Proc. Nat. Acad. Sci. USA. 76 4350-4354
  • 39 Webb,  M. A.. (1999);  Cell-mediated crystallization of calcium oxalate in plants.  Plant Cell. 11 751-761
  • 40 Webb,  M. A.,, Cavaletto,  N. C.,, Carpita,  N. C.,, Lopez,  L. E.,, and Arnott,  H. J.. (1995);  The intravacuolar organic matrix associated with calcium oxalate crystals in leaves of Vitis. .  Plant Journal. 7 633-648
  • 41 Zindler-Frank,  E.. (1975);  On the formation of the pattern of crystal idioblasts in Canavalia ensiformis DC. VII. Calcium and oxalate content of the leaves in dependence of calcium nutrition.  Z. Pflanzenphysiol.. 77 80-85

V. R. Franceschi

School of Biological Sciences
Washington State University

Pullman
WA 99164-4236
USA

Email: vfrances@mail.wsu.edu

Section Editor: A. Läuchli