Genetic evidence for differences in the pathways of druse and prismatic calcium oxalate crystal formation in Medicago truncatula
Paul A. Nakata A B and Michele M. McConn AA USDA-ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, 1100 Bates St., Houston, TX 77030-2600, USA.
B Corresponding author. Email: pnakata@bcm.tmc.edu
C This paper originates from an International Symposium in Memory of Vincent R. Franceschi, Washington State University, Pullman, Washington, USA, June 2006.
Functional Plant Biology 34(4) 332-338 https://doi.org/10.1071/FP06268
Submitted: 26 October 2006 Accepted: 4 January 2007 Published: 19 April 2007
Abstract
Current evidence supports a single pathway of oxalate biosynthesis utilising ascorbic acid as the precursor. In this study, we begin to address the possibility that more than one pathway of oxalate biosynthesis and calcium oxalate formation occurs in Medicago truncatula Gaertn. (cv. Jemalong genotype A17). Like the wild type, developing leaves of the calcium oxalate defective (cod) 4 mutant contain prismatic crystals along the vascular strand, but this mutant also hyper-accumulates druse crystals within the mesophyll cells. A second mutant, cod5, fails to accumulate prismatic crystals along the vascular strand, but is capable of wild type druse crystal accumulation in maturing leaves. To assess whether a single pathway of oxalate biosynthesis and calcium oxalate formation occurs in M. truncatula, we generated and characterised the cod4/cod5 double mutant. Microscopic examination of the cod4/cod5 revealed that the double mutant exhibits both cod4 and cod5 mutant crystal phenotypes simultaneously, suggesting there are differences in the pathways leading to the two crystal types. Measured ascorbic acid levels and ascorbate induction studies were consistent with the acid as precursor to oxalate in druse crystal formation but not necessarily prismatic crystal formation. On the basis of these findings, we propose a working model depicting possible pathways of oxalate biosynthesis and calcium oxalate formation.
Acknowledgements
This work was supported by the USA Department of Agriculture, Agriculture Research Service, under Cooperative Agreement 58–6250–6-001. The contents of this publication do not necessarily reflect the views or policies of the USA Department of Agriculture, nor does mention of trade names, commercial products, or organisations imply endorsement by the USA government. We thank Ken Fraley for his help with statistical analysis and Kendal Hirschi for his comments on the manuscript. This paper is dedicated to the memory of Vincent R Franceschi.
Bucciarelli B,
Hanan J,
Palmquist D, Vance CP
(2006) A standardized method for analysis of Medicago truncatula phenotypic development. Plant Physiology 142, 207–219.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Franceschi VR, Nakata PA
(2005) Calcium oxalate in plants: formation and function. Annual Review of Plant Biology 56, 41–71.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grusak MA
(1994) Iron transport to developing ovules of Pisum sativum: I. Seed import characteristics and phloem iron-loading capacity of source regions. Plant Physiology 104, 649–655.
| PubMed |
Horner HT,
Kausch AP, Wagner BL
(2000) Ascorbic acid: a precursor of oxalate in crystal idioblasts of Yucca Torreyi in liquid root culture. International Journal of Plant Sciences 161, 861–868.
| Crossref | GoogleScholarGoogle Scholar |
Kampfenkel K,
Van Montagu M, Inzé D
(1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Analytical Biochemistry 225, 165–167.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kausch AP, Horner HT
(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, 35–43.
| Crossref | GoogleScholarGoogle Scholar |
Keates SA,
Tarlyn N,
Loewus FA, Franceschi VR
(2000) l-Ascorbic acid and l-galactose are sources of oxalic acid and calcium oxalate in Pistia stratiotes. Phytochemistry 53, 433–440.
| Crossref | l-Ascorbic acid and l-galactose are sources of oxalic acid and calcium oxalate in Pistia stratiotes.&journal=Phytochemistry&volume=53&pages=433-440&publication_year=2000&author=VR%20Franceschi&hl=en&doi=10.1016/S0031-9422(99)00448-3" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed |
Korth KL,
Doege SJ,
Park S-H,
Goggin FL, Wang Q , et al.
(2006) Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiology 141, 188–195.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kostman TA, Koscher JR
(2003) l-galactono-gamma-lactone dehydrogenase is present in calcium oxalate crystal idioblasts of two plant species. Plant Physiology and Biochemistry 41, 201–206.
| Crossref | l-galactono-gamma-lactone dehydrogenase is present in calcium oxalate crystal idioblasts of two plant species.&journal=Plant Physiology and Biochemistry&volume=41&pages=201-206&publication_year=2003&author=JR%20Koscher&hl=en&doi=10.1016/S0981-9428(03)00011-1" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar |
Kostman TA,
Tarlyn NM,
Loewus FA, Franceschi VR
(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 Physiology 125, 634–640.
| Crossref | l-ascorbic acid and conversion of carbons 1 and 2 of l-ascorbic acid to oxalic acid occurs within individual calcium oxalate crystal idioblasts.&journal=Plant Physiology&volume=125&pages=634-640&publication_year=2001&author=VR%20Franceschi&hl=en&doi=10.1104/pp.125.2.634" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed |
Li XX, Franceschi VR
(1990) Distribution of peroxisomes and glycolate metabolism in relation to calcium oxalate formation in Lemna minor L. European Journal of Cell Biology 51, 9–16.
| PubMed |
Libert B, Franceschi VR
(1987) Oxalate in crop plants. Journal of Agricultural and Food Chemistry 35, 926–938.
| Crossref | GoogleScholarGoogle Scholar |
McNair JB
(1932) The interrelation between substances in plants: essential oils and resins, cyanogen and oxalate. American Journal of Botany 19, 255–271.
| Crossref | GoogleScholarGoogle Scholar |
Nakata PA, McConn MM
(2000) Isolation of Medicago truncatula mutants defective in calcium oxalate crystal formation. Plant Physiology 124, 1097–1104.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nakata PA, McConn MM
(2003a) Calcium oxalate crystal formation is not essential for growth of Medicago truncatula. Plant Physiology and Biochemistry 41, 325–329.
| Crossref | GoogleScholarGoogle Scholar |
Nakata PA, McConn MM
(2003b) Influence of the calcium oxalate defective 4 (cod4) mutation on the growth, oxalate content, and calcium content of Medicago truncatula. Plant Science 164, 617–621.
| Crossref | GoogleScholarGoogle Scholar |
Nakata PA, McConn MM
(2006) A genetic mutation that reduces calcium oxalate content increases calcium availability in Medicago truncatula. Functional Plant Biology 33, 703–706.
| Crossref | GoogleScholarGoogle Scholar |
Nuss RF, Loewus FA
(1978) Further studies on oxalic acid biosynthesis in oxalate-accumulating plants. Plant Physiology 61, 590–592.
| PubMed |
Smirnoff N,
Conklin PL, Loewus FA
(2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annual Review of Plant Physiology and Plant Molecular Biology 52, 437–467.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Volk GM,
Lynch-Holm VJ,
Kostman TA,
Goss LJ, Franceschi VR
(2002) The role of druse and raphide calcium oxalate crystals in tissue calcium regulation in Pistia stratiotes leaves. Plant Biology 4, 34–45.
Wagner G, Loewus F
(1973) The biosynthesis of (+)-tartaric acid in Pelargonium crispum. Plant Physiology 52, 651–654.
| PubMed |
Xu H-W,
Ji X-M,
He Z-H,
Shi W-P, Zhu G-H , et al.
(2006) Oxalate accumulation and regulation is independent of glycolate oxidase in rice leaves. Journal of Experimental Botany 57, 1899–1908.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yang J, Loewus FA
(1975) Metabolic conversion of l-ascorbic acid in oxalate-accumulating plants. Plant Physiology 56, 283–285.
| PubMed |
Zindler-Frank E
(1976) Oxalate biosynthesis in relation to photosynthetic pathways and plant productivity: a survey. Zeitschrift für Pflanzenphysiologie 80, 1–13.