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New and Unusual Forms of Calcium Oxalate Raphide Crystals in the Plant Kingdom

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New and Unusual Forms of Calcium Oxalate Raphide Crystals in the Plant Kingdom Genetics, Development and Cell Biology Publications Genetics, Development and Cell Biology 11-2014 New and unusual forms of calcium oxalate raphide crystals in the plant kingdom Vijayasankar Raman University of Mississippi Harry T. Horner Iowa State University, [email protected] Ikhlas A. Khan University of Mississippi Follow this and additional works at: https://lib.dr.iastate.edu/gdcb_las_pubs Part of the Cell and Developmental Biology Commons, and the Plant Biology Commons The complete bibliographic information for this item can be found at https://lib.dr.iastate.edu/ gdcb_las_pubs/236. For information on how to cite this item, please visit http://lib.dr.iastate.edu/howtocite.html. This Article is brought to you for free and open access by the Genetics, Development and Cell Biology at Iowa State University Digital Repository. It has been accepted for inclusion in Genetics, Development and Cell Biology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. New and unusual forms of calcium oxalate raphide crystals in the plant kingdom Abstract Calcium oxalate crystals in higher plants occur in five major forms namely raphides, styloids, prisms, druses and crystal sand. The form, shape and occurrence of calcium oxalate crystals in plants are species- and tissue-specific, hence the presence or absence of a particular type of crystal can be used as a taxonomic character. So far, four different types of needle-like raphide crystals have been reported in plants. The present work describes two new and unusual forms of raphide crystals from the tubers of Dioscorea polystachya—six-sided needles with pointed ends (Type V) and four-sided needles with beveled ends (Type VI). Both of these new types of needles are distinct from the other four types by each having a surrounding membrane that envelopes a bundle of 10–20 closely packed thin crystalline sheets. The previously known four types of needles have solid or homogenous crystalline material, surrounded by a membrane or lamellate sheath called a crystal chamber. Only the Type VI crystals have beveled ends and the needles of the other five types have pointed ends. Keywords Anatomy, Calcium oxalate crystals, Dioscorea polystachya, Light microscopy, Raphides, Scanning electron microscopy, Yams Disciplines Cell and Developmental Biology | Plant Biology | Plant Sciences Comments This is a manuscript of an article published as Raman, Vijayasankar, Harry T. Horner, and Ikhlas A. Khan. "New and unusual forms of calcium oxalate raphide crystals in the plant kingdom." Journal of plant research 127, no. 6 (2014): 721-730. doi: 10.1007/s10265-014-0654-y. Posted with permission. This article is available at Iowa State University Digital Repository: https://lib.dr.iastate.edu/gdcb_las_pubs/236 HHS Public Access Author manuscript Author ManuscriptAuthor Manuscript Author J Plant Res Manuscript Author . Author manuscript; Manuscript Author available in PMC 2017 September 05. Published in final edited form as: J Plant Res. 2014 November ; 127(6): 721–730. doi:10.1007/s10265-014-0654-y. New and unusual forms of calcium oxalate raphide crystals in the plant kingdom Vijayasankar Raman, National Center for Natural Products Research, School of Pharmacy, University of Mississippi, University, MS 38677, USA Harry T. Horner, and Department of Genetics, Development and Cell Biology and Microscopy and NanoImaging Facility, Iowa State University, Ames, Iowa 50011-1020, USA Ikhlas A. Khan National Center for Natural Products Research, School of Pharmacy, University of Mississippi, University, MS 38677, USA Department of Pharmacognosy, School of Pharmacy, University of Mississippi, University, MS 38677, USA Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh, Saudi Arabia Abstract Calcium oxalate crystals in higher plants occur in five major forms namely raphides, styloids, prisms, druses and crystal sand. The form, shape and occurrence of calcium oxalate crystals in plants are species- and tissue-specific, hence the presence or absence of a particular type of crystal can be used as a taxonomic character. So far, four different types of needle-like raphide crystals have been reported in plants. The present work describes two new and unusual forms of raphide crystals from the tubers of Dioscorea polystachya—six-sided needles with pointed ends (Type V) and four-sided needles with beveled ends (Type VI). Both of these new types of needles are distinct from the other four types by each having a surrounding membrane that envelopes a bundle of 10–20 closely packed thin crystalline sheets. The previously known four types of needles have solid or homogenous crystalline material, surrounded by a membrane or lamellate sheath called a crystal chamber. Only the Type VI crystals have beveled ends and the needles of the other five types have pointed ends. Keywords Anatomy; Calcium oxalate crystals; Dioscorea polystachya; Light microscopy; Raphides; Scanning electron microscopy; Yams Correspondence to: Ikhlas A. Khan. Raman et al. Page 2 Author ManuscriptAuthor Introduction Manuscript Author Manuscript Author Manuscript Author Inorganic calcium oxalate crystals are common in plants. They occur in different forms and shapes and are found in almost all major taxonomic groups of plants (Franceschi and Nakata 2005). Crystals have been observed in members of more than 215 plant families (McNair 1932) and occur in about 74 % of angiosperm families (Zindler-Frank 1976). The crystals are found in almost all organs of plants and in almost all types of tissues (Horner and Wagner 1995; Horner et al. 2012). The crystalline form can make up from about 1 % to over 90 % of a plant’s dry mass (Braissant et al. 2004; Horner and Wagner 1995; Nakata 2003; Zindler-Frank 1976; 1987). The primary role of calcium oxalate crystals may vary depending on the plant, organ and tissue in which they occur and can be characterized as: defense against herbivory, tissue support, calcium regulation and as an internal reservoir for calcium, ion balance, removal of toxic oxalic acid and gathering and reflection of light (Franceschi and Horner 1980; Franceschi and Nakata 2005; Nakata 2003). The formation of calcium oxalate crystals is genetically controlled and the crystals are usually formed in a defined shape and spatial location (Franceschi and Nakata 2005; Kausch and Horner 1982). Morphologically, the crystals are classified into five major forms: crystal sand, raphide, druse, styloid and prismatic (Franceschi and Horner 1980; Franceschi and Nakata 2005; Horner and Wagner 1995) and each category of crystal may show variations in its shape and size. Studies of the types of crystals and their macropatterns are species and genus specific and may contribute to understanding phylogenetic relationships (Horner et al. 2012; Lersten and Horner 2000; 2011; Prychid and Rudall 1999). The formation of calcium oxalate crystals in plants is not yet fully understood. Several studies have been conducted with the aim of filling this gap. Horner et al. (2000) showed the pathway of oxalate biosynthesis utilizes ascorbate as the primary precursor, and Nakata (2003) found that the ascorbate utilized is produced directly within the crystal idioblast itself. Plant crystals are formed from endogenously synthesized oxalic acid, which combines with calcium from the environment (Franceschi and Nakata 2005). Other subcellular features that influence crystal formation include changes in nuclear DNA (Kausch and Horner 1984b), an abundance of endoplasmic reticulum, acidic proteins, cytoskeletal components, and an intravacuolar matrix and organic paracrystalline bodies (Horner and Wagner 1995; Horner and Whitmoyer 1972; Nakata 2003). Needle-shaped crystals called raphides typically occur in large numbers as closely packed bundles in tissues from green algae to flowering plants. They form in crystal membrane chambers within the vacuoles in specialized cells sometimes called crystal idioblasts (Arnott and Pautard 1970; Horner and Wagner 1995). The characteristic appearance, development and distribution of raphides, as well as other crystal shapes, have been used for taxonomic, pharmacognostic and toxicological purposes (Horner et al. 2012; Lampe and Fagerström 1968; Metcalfe and Chalk 1957; Sakai and Hanson 1974). Several studies have been conducted to elucidate the development and formation of raphides and raphide-containing idioblasts (Frey 1929; Horner and Whitmoyer 1972; Kausch and Horner 1983a; 1983b; 1984a; Mollenhauer and Larson 1966; Parameswaran and Schultze 1974; Sakai and Hanson 1974; Tilton and Horner 1980; Wattendorff 1976). Bruni et al. (1982) have described raphide formation as a complex process involving several cellular compartments. According to J Plant Res. Author manuscript; available in PMC 2017 September 05. Raman et al. Page 3 Kostman and Franceschi (2000), raphide crystal idioblasts possess a cortical microtubule Author ManuscriptAuthor Manuscript Author Manuscript Author Manuscript Author network that appears to limit an increase in cell diameter, but not elongation, resulting in the ellipsoidal shape of idioblasts. The type of hydration of calcium oxalate influences the morphology of crystals. Two types of crystal forms, depending on the relative concentration of calcium and oxalate, are reported to occur in plants: (1) monohydrate (whewellite, CaC2O4·H2O; monoclinic crystal system) and (2) dihydrate (weddellite, CaC2O4·2H2O; tetragonal crystal
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