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Scanning Electron Microscopy Coupled with Energy Dispersive Spectrometric Analysis Reveals for the First Time Weddellite and Sylvite Crystals on the Surface of Involucral Bracts and Petals of two Xeranthemum L. (Compositae) Species

Part of: Micrographia Collection

Published online by Cambridge University Press:  26 May 2017

Milan Gavrilović ,
Suzana Erić ,
Petar D. Marin ,
Núria Garcia-Jacas ,
Alfonso Susanna  and
Pedja Janaćković
Milan Gavrilović*
Affiliation:
Institute of Botany and Botanical Garden “Jevremovac”, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000, Belgrade, Serbia
Suzana Erić
Affiliation:
Faculty of Mining and Geology, University of Belgrade, Ðušina 7, 11000 Belgrade, Serbia
Petar D. Marin
Affiliation:
Institute of Botany and Botanical Garden “Jevremovac”, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000, Belgrade, Serbia
Núria Garcia-Jacas
Affiliation:
Botanic Institute of Barcelona (IBB-CSIC-ICUB), Pg. del Migdia s. n., 08038 Barcelona, Spain
Alfonso Susanna
Affiliation:
Botanic Institute of Barcelona (IBB-CSIC-ICUB), Pg. del Migdia s. n., 08038 Barcelona, Spain
Pedja Janaćković
Affiliation:
Institute of Botany and Botanical Garden “Jevremovac”, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000, Belgrade, Serbia
*
* Corresponding author. [email protected]
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Abstract

In this work, weddellite and sylvite crystals are identified for the first time on the involucral bracts and petals of Xeranthemum annuum and Xeranthemum cylindraceum using scanning electron microscopy coupled with energy dispersive spectrometric (SEM-EDS) analysis. Well-developed crystals of weddellite (CaC2O4·2H2O) occur in the form of a tetragonal bipyramid (hhl), rarely in combination of a bipyramid and tetragonal prism (h00). Indumentum of involucral bracts of X. cylindraceum consists of nonglandular and glandular trichomes. Sylvite (KCl) crystals are observed only on the petal surface of X. cylindraceum. The crystals of sylvite occur in the form of perfect cubes (hexahedrons), but some crystals are deformed, i.e., partially elongated. Taxonomic significance of investigated microcharacters as well as the use of SEM-EDS analysis in taxonomic studies of plants are discussed.

Keywords

SEM-EDSweddellite and sylvite crystalsXeranthemumCardueaeinvolucral bracts and petals
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 23 , Issue 3 , June 2017 , pp. 679 - 686
Copyright
© Microscopy Society of America 2017 

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References

Arnott, H.J. (1982). Three systems of biomineralization in plants with comments on the associated organic matrix. In Biological Mineralization and Demineralization, Nancollas G.H. (Ed.), pp 199–218. Berlin: Springer Verlag.Google Scholar
Barabé, D. & Lacroix, C. (2000). Homeosis in the flower of the Araceae: The case of Philodendron melinonii (Araceae). Ann Bot 86, 479–491.Google Scholar
Barabé, D., Lacroix, C., Chouteau, M. & Gibernau, M. (2004). On the presence of extracellular calcium oxalate crystals on the inflorescences of Araceae . Bot J Linn Soc 146, 181–190.Google Scholar
Bárcenas-Argüello, M.L., Gutiérrez-Castorena, M.C.D.C. & Terrazas, T. (2015). The polymorphic weddellite crystals in three species of Cephalocereus (Cactaceae). Micron 77, 1–8.Google Scholar
Berg, RH. (1994). A calcium oxalate-secreting tissue in branchlets of the Casuarinaceae. Protoplasma 183, 29–36.Google Scholar
Borchert, R. (1984). Functional anatomy of the calcium-excreting system of Gleditsia triacanthos L. Bot Gaz 145, 474–482.Google Scholar
Brizuel, M., Montenegro, T., Carjuzaa, P. & Maldonado, S. (2007). Insolubilization of potassium chloride crystals in Tradescantia pallida . Protoplasma 231, 145–149.Google Scholar
Chase, M.W. & Peacor, D.R. (1987). Crystals of calcium oxalate hydrate on the perianth of Stelis SW. Lindleyana 2, 91–94.Google Scholar
Dane, F., Meric, C. & Hüseyinova, G. (2000). Some ultrastructural observations on calcium oxalate raphide crystal idioblasts and meristematic cells of the adventive root tips of Sternbergia lutea (L.) Ker-Gawl. ex Sprengel (Amaryllidaceae). Turk J Bot 24, 71–80.Google Scholar
Daumann, E. (1930). Nektarabscheidung in der Blütenregion einiger Araceen. Zugleich ein Hinweis auf die Bargersche Methode. Planta 12, 38–48.Google Scholar
Daumann, E. (1970). Das Blütennektarium der Monocotyledon unter besonderer Berücksichtigung seiner sytematischen und phylogenetischen Bedeutung. Feddes Repert 80, 463–590.Google Scholar
De Yoreo, J.J. & Dove, P.M. (2004). Shaping crystals with biomolecules. Science 306, 1301–1302.Google Scholar
Dekić, M., Radulović, N., Ranđelović, V., Stojanović-Radić, Z. & Veljković, B. (2015). Essential oils and diethyl ether extracts of Serbian Xeranthemum cylindraceum and X. annuum: Chemical composition, antimicrobial activity, and chemotaxonomic implications. Chem Biodivers 12, 1378–1397.CrossRefGoogle Scholar
Dickison, W.C. (2000). Integrative Plant Anatomy. London: Academic Press.Google Scholar
Dormer, K.J. (1961). The crystals in the ovaries of certain Compositae. Ann Bot 25, 241–254.Google Scholar
Dormer, K.J. (1962). The taxonomic significance of crystal forms in Centaurea . New Phytol 61, 32–35.Google Scholar
Echigo, T., Kimata, M., Kyono, A. & Shimizu, M. (2005). Re-investigation of the crystal structure of whewellite [Ca (C2O4)·H2O] and the dehydration mechanism of caoxite [Ca (C2O4)·3H2O]. Mineral Mag 69, 77–88.Google Scholar
Endress, P.K., Baas, P. & Gregory, M. (2000). Systematic plant morphology and anatomy: 50 years of progress. Taxon 49, 401–434.Google Scholar
Franceschi, V.R. & Horner, H.T. Jr. (1980). Calcium oxalate crystals in plants. Bot Rev 46, 361–427.Google Scholar
Franceschi, V.R. & Nakata, P.A. (2005). Calcium oxalate in plants: Formation and function. Annu Rev Plant Biol 56, 41–71.Google Scholar
Frey-Wyssling, A. (1981). Crystallography of the two hydrates of crystalline calcium oxalate in plants. Am J Bot 68, 130–141.Google Scholar
Frost, R.L. (2006). Raman spectroscopy of natural oxalates. Anal Chim Acta 517, 207–214.Google Scholar
Gajić, M. (1975). Xeranthemum . In Flora of Serbia, vol. 7, Josifović M. (Ed.), p. 176. Belgrade: SANU.Google Scholar
Garnatje, T., Vallès, J., Vilatersana, R., Garcia-Jacas, N., Susanna, A. & Siljak-Yakovlev, S. (2004). Molecular cytogenetics of Xeranthemum L. and related genera (Asteraceae, Cardueae). Plant Biol 6, 140–146.CrossRefGoogle ScholarPubMed
Garnatje, T. & Martín, J. (2007). Pollen studies in the genus Echinops L. and Xeranthemum group (Asteraceae). Bot J Linn Soc 154, 549–557.Google Scholar
Garty, J., Kunin, P., Delarea, J. & Weiner, S. (2002). Calcium oxalate and sulphate-containing structures on the thallial surface of the lichen Ramalina lacera: Response to polluted air and simulated acid rain. Plant Cell Environ 25, 1591–1604.Google Scholar
Hîbel, W., Nahrstedt, A., Fikenscher, L.H. & Hegnauer, R. (1982). Zierinxyloside, a new Cyanogenic glycoside from Xeranthemum cylindraceum . Planta Med 44, 178–189.Google Scholar
Horner, H.T. (1977). A comparative light and electron-microscopic study of microsporogenesis in male-fertile and cytoplasmic male-sterile sunflower (Helianthus annuus). Am J Bot 64, 745–759.Google Scholar
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, 861–868.Google Scholar
Horner, H.T., Wanke, S. & Samain, M.S. (2009). Evolution and systematic value of leaf crystal macropatterns: A phylogenetic approach in the genus Peperomia (Piperaceae). Int J Plant Sci 170, 343–354.Google Scholar
Horner, H.T., Wanke, S. & Samain, M.S. (2012). A comparison of leaf crystal macropatterns in the two sister genera Piper and Peperomia (Piperaceae). Am J Bot 99, 983–997.Google Scholar
Ilarslan, H., Palmer, R.G. & Horner, H.T. (2001). Calcium oxalate crystals in developing seeds of soybean. Ann Bot 88, 243–257.CrossRefGoogle Scholar
Iwano, M., Entani, T., Shiba, H., Takayama, S. & Isogai, A. (2004). Calcium crystals in the anther of Petunia: The existence and biological significance in the pollination process. Plant Cell Physiol 45, 40–47.Google Scholar
Kartal, C. (2016). Calcium oxalate crystals in some species of the tribe Cardueae (Asteraceae). Bot Sci 94, 107–119.Google Scholar
Kausch, A.P. & Horner, H.T. (1984). Differentiation of raphide crystal idioblasts in isolated root cultures of Yucca torreyi (Agavaceae). Can J Botany 62, 1474–1484.Google Scholar
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, 188–195.CrossRefGoogle ScholarPubMed
Kostman, T.A. & Franceschi, V.R. (2000). Cell and calcium oxalate crystals growth is coordinated to achieve high-capacity calcium regulation in plants. Protoplasma 214, 166–179.Google Scholar
Kuo-Huang, L. (1992). Ultrastructural study on the development of crystal-forming sclereids in Nymphaea tetragona . Taiwania 37, 104–113.Google Scholar
Kuo-Huang, L.L., Ku., M.S.B. & Franceschi, V.R. (2007). Correlations between calcium oxalate crystals and photosynthetic activities in palisade cells of shade-adapted Peperomia glabella . Bot Stud 48, 155–164.Google Scholar
Lersten, N.R. & Horner, H.T. (2000). Calcium oxalate crystals types and trends in their distribution patterns in leaves of Prunus (Rosaceae: Prunoideae). Plant Syst Evol 224, 83–96.Google Scholar
Meric, C. (2008). Calcium oxalate crystals in Conyza canadensis (L.) Cronq. and Conyza bonariensis (L.) Cronq. (Asteraceae: Astereae). Acta Biol Szeged 52, 295–299.Google Scholar
Meric, C. (2009 a). Calcium oxalate crystals in some species of the tribe Inuleae (Asteraceae). Acta Biol Crac Ser Bot 51, 105–110.Google Scholar
Meric, C. (2009 b). Calcium oxalate crystals in Aster squamatus and Bellis perennis (Asteraceae: Astereae). Phytol Balc 15, 255–259.Google Scholar
Meric, C. & Dane, F. (2004). Calcium oxalate crystals in floral organs of Helianthus annuus L. and H. tuberosus L. (Asteraceae). Acta Biol Szeged 48, 19–23.Google Scholar
Molano-Flores, B. (2001). Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae). Ann Bot 88, 387–391.CrossRefGoogle Scholar
Monje, P.V. & Baran, E.J. (2002). Characterization of calcium oxalates generated as biominerals in cacti. Plant Physiol 128, 707–713.Google Scholar
Pennisi, S.V. & McConnell, D.B. (2001). Taxonomic relevance of calcium oxalate cuticular deposits in Dracaena Vand. ex L. Hortscience 36, 1033–1036.Google Scholar
Pennisi, S.V., McConnell, D.B., Gower, L.B., Kane, M.E. & Lucansky, T. (2001). Periplasmic cuticular calcium oxalate crystal deposition in Dracaena sanderiana . New Phytol 149, 209–218.Google Scholar
Powell, R.G., Smith, C.R. Jr. & Wolff, I.A. (1967). cis-5,cis-9,cis-12-octadecatrienoic and some unusual oxygenated acids in Xeranthemum annuum seed oil. Lipids 2, 172–177.Google Scholar
Prychid, C.J., Furness, C.A. & Rudall, P.J. (2003). Systematic significance of cell inclusions in Haemodoraceae and allied families: Silica bodies and tapetal raphides. Ann Bot 92, 571–580.Google Scholar
Prychid, C.J. & Rudall, P.J. (1999). Calcium oxalate crystals in monocotyledons: A review of their structure and systematics. Ann Bot 84, 725–739.Google Scholar
Richards, A.J. (1986). Plant Breeding Systems. London: George Allen & Unwin.Google Scholar
Robinson, H. (2009). An introduction to micro-characters of Compositae. In Systematics, Evolution and Biogeography of Compositae, Funk A.V., Susanna A., Stuessy F.T. & Bayer J.R. (Eds.), pp. 89–100. Vienna: IAPT.Google Scholar
Samek, Z., Holub, M., Drożdż, B., Grabarczyk, H. & Hładoń, B. (1977). Xerantholide—A new cytotoxically active sesquiterpenic lactone from Xeranthemum cylindraceum Sibth. et Smith. Collect Czech ChemCommun 42, 2441–2447.Google Scholar
Skaltsa, H.D., Lazari, D.M. & Constantinidis, T. (2000). Composition of the essential oil of Xeranthemum annuum L. from Greece. J Essent Oil Res 12, 742–744.Google Scholar
Stanković, SM., Radojević, D.I., Stefanović, D.O., Topuzović, D.M., Čomić, L.R. & Branković, R.S. (2011). Immortelle (Xeranthemum annuum L.) as a natural source of biologically active substances. EXCLI J 10, 230–239.Google Scholar
Susanna, A. & Garcia-Jacas, N. (2009). Cardueae (Carduoideae). In Systematics, Evolution and Biogeography of Compositae, Funk A.V, Susanna A, Stuessy F.T & Bayer J.R. (Eds.), pp. 293–313. Vienna: IAPT.Google Scholar
Tilton, V.R & Horner, H.T. Jr. (1980). Calcium oxalate raphide crystals and crystalliferous idioblasts in the carpels of Ornithogalum caudatum . Ann Bot 46, 533–539.Google Scholar
Valant-Vetschera, K.M. & Wollenweber, E. (2007). Chemodiversity of exudate flavonoids in seven tribes of Cichorioideae and Asteroideae (Asteraceae). Z Naturforsch C 62, 155–163.Google Scholar
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, 34–45.Google Scholar
Volcani, B.E. (1983). Aspects of silicification in biological systems. In Biomineralization and Biological Metal Accumulation, Westbroeck P & De Jong E.W. (Eds.), pp 389–405. Dordrecht: D. Reidel Publishing Co.Google Scholar
Volovnik, S.V. (2016). On oviposition in weevils of the genus Larinus Dej. (Coleoptera, Curculionidae). Entomol Rev 96, 309–317.Google Scholar
Willey, N. (2016). Environmental Plant Physiology. New York, NY: Garland Science.Google Scholar
Zemtsova, G.N. & Molchanova, L.P. (1979). Flavonoids and triterpenoids of Xeranthemum annuum . Chem Nat Comp 15, 762.Google Scholar