Abstract
Calcium oxalate (CaOx) crystals in higher plants occur in five forms: raphides, styloids, prisms, druses, and crystal sand. CaOx crystals are formed in almost all tissues in intravacuolar crystal chambers. However, the mechanism of crystallization and the role of CaOx crystals have not been clearly explained. The aim of this study was to explore the occurrence and location of CaOx crystals in organs of Tinantia anomala (Torr.) C.B. Clarke (Commelinaceae) with special attention to ultrastructural changes in the quantity of tapetal raphides during microsporogenesis. We observed various parts of the plant, that is, stems, leaves, sepals, petals, anthers, staminal trichomes and stigmatic papillae and identified CaOx crystals in all parts except staminal trichomes and stigmatic papillae in Tinantia anomala. Three morphological forms: styloids, raphides and prisms were found in different amounts in different parts of the plant. Furthermore, in this species, we identified tapetal raphides in anthers. The number of tapetal raphides changed during microsporogenesis. At the beginning of meiosis, the biosynthesis of raphides proceeded intensively in the provacuoles. These organelles were formed from the endoplasmic reticulum system. In the tetrad stage, we observed vacuoles with needle-shaped raphides (type I) always localised in the centre of the organelle. When the amoeboid tapetum was degenerating, vacuoles also began to fade. We observed a small number of raphides in the stage of mature pollen grains.
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References
Arnott HJ, Webb MA (1999) Twinned raphides of calcium oxalate in grape (Vitis): implications for crystal stability and function. Int J Plant Sci 161:133–142
Bednarska E, Butowt R (1994) Calcium in pollen-pistil interaction in Petunia hybrida Hort. Folia Histochem Cytochem 33:43–52
Bremer K (1994) Asteraceae: Cladistics and classification. Timber Press, Portland
Buvat R (1989) Ontogeny, cell differentiation, and structure of vascular plants. Springer-Verlag, Heidelberg, pp 481–482
Carniel K (1952) Das Verhalten der Kernc in Tapetum der Angi-spermen mit bcsonderer Berucksichtigung yo11 endomitosen und sogenannten Endomitosen. Osterr Bot Zeitschrift 99:318–362
Chase MW, Stevenson DW, Wilkin P, Rudall P (1995) Monocot systematics: combined analysis. In: Rudall P, Crihb P, Cutler D, Humphries C (eds) Monocotyledons: systematics and evolution. Royal Botanic Gardens, Kew, pp 685–730
Coté GG (2009) Diversity and distribution of idioblasts producing calcium oxalate crystals in Dieffenbachia seguine (Araceae). Am J Bot 96:1245–1254
Crowther A (2009) Reviewing raphides: issues with the identification and interpretation of calcium oxalate crystals in microfossil assemblages. In: Fairbairn A, O’Connor S, Marwick B (eds) New directions in archaeological science. Terra Australis:28. ANU E-Press, Canberra, pp 105–118
D’Arcy WG, Keating RC, Buchmann SL (1996) The calcium oxalate package or so-called resorption tissue in some angiosperm anthers. In: D’Arcy WG, Keating RC (eds) The anther: form, function, and phylogeny. Cambridge University Press, Cambridge, pp 159–191
Foster AS (1956) Plant idioblasts: remarkable examples of cell specialization. Protoplasma 46:184–193
Franceschi VR, Horner HT (1980) Calcium oxalate crystals in plants. Bot Rev 46:361–427
Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Annu Rev Plant Biol 56:41–71
Hamann U (1966) Embryologische, morphologisch-anatomische und systematische Untersuchungen an Philydraceen. Willdenowia Beiheft 4:1–178
Hardy CR, Stevenson DW (2000) Development of the gametophytes, flower and floral vasculature in Cochliostema odoratissimum (Commelinaceae). Bot J Linn Soc 134:131–157
Hardy CR, Stevenson DW, Kiss HG (2000) Development of the gametophytes, flower, and floral vasculature in Dichorisandra thyrsiflora (Commelinaceae). Am J Bot 87:1228–1239
Hayat MA (2000) Principles and techniques of electron microscopy for biological applications, 4th edn. Cambridge University Press, New York
He H, Veneklaas EJ, Kuo J, Lambers H (2014) Physiological and ecological significance of biomineralization in plants. Trends Plant Sci 19:166–174
Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155
Horner HT (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
Horner HT, Wagner BL (1995) Calcium oxalate formation in higher plants. In: Khan SR (ed) Calcium oxalate in biological systems. CRC Press, Boca Raton, pp 53–72
Ilarslan H, Palmer RG, Horner HT (2001) Calcium oxalate crystals in developing seeds of soybean. Ann Bot 88:243–257
Iwano ML, 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
Kauss H (1987) Some aspects of calcium dependent regulation in plant metabolism. Ann Rev PI Physiol 38:47–72
Khan AS, Siddiqi R (2014) Environmental factors affect calcium oxalate crystals formation Tradescantia pallida (Commelinaceae). Pak J Bot 46:477–482
Kinzel H (1989) Calcium in the vacuoles and cell walls of plant tissue: forms of deposition and their physiological and ecological significance. Flora 182:99–125
Kohno T, Shimmen T (1987) Ca 2+-induced fragmentation of actin filaments in pollen tubes. Protoplasma 141:177–179
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 Physiol 125:634–640
Maheshwari P, Singh B (1934) A preliminary note on the morphology of the aerial and underground flowers of Commelina benghalensis. Linn Curr Sci 3:158–160
Mascre M (1925) Sur l’evolution de l’etamine des Commelinacees. Bulletin Soc Bot de France 72:1060–1066
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
Molano-Flores B (2001) Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae). Ann Bot 88:387–391
Nakata PA (2003) Advances in our understanding of calcium oxalate crystal formation and function in plants. Plant Sci 164:901–909
Nakata PA, McConn MM (2000) Isolation of Medicago truncatula mutants defective in calcium oxalate crystal formation. Plant Physiol 124:1097–1104
Nanda K, Gupta SC (1977) Development of tapetal periplasmodium in Rheo spathacea. Mod Phytomorphol 27:308–314
Pacini E (1997) Tapetum character states: analytical keys for tapetum types and activities. Can J Bot 75:1448–1459
Pacini E, Juniper BE (1983) The ultrastructure of the formation and development of the amoeboid tapetum in Arum italicum Miller. Protoplasma 117:116–129
Prychid ChJ, Rudall PJ (1999) Calcium oxalate crystals in monocotyledons: a review of their structure and systematics. Ann Bot 84:725–739
Prychid ChJ, Furness CA, Rudall PJ (2003) Systematic significance of cell inclusions in Haemodoraceae and allied families: silica bodies and tapetal raphides. Ann Bot 92:571–580
Prywer J (2009) Theoretical analysis of specific evolution of some faces of plant COM crystals. Cryst Eng Comm 11:196–202
Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spore terminology. Rev Palaeobot Palynol 143:1–81
Raman V, Horner HT, Khan IA (2014) New and unusual forms of calcium oxalate raphide crystals in the plant kingdom. J Plant Res 127:721–730
Simpson MG (1988) Embryological development of Lachnantches caroliniana (Haemodoraceae). Am J Bot 75:1394–1408
Stejskal-Streit V (1940) Vergleichende Untersuchungen gehemmter Staublatter. Osterr Bot Z 89:1–56
Stevenson DW, Owens SJ (1978) Some aspects of the reproductive morphology of Gibasis venustula (Kunth) DR Hunt (Commelinaceae). Bot J Linn Soc 77:157–175
Tian GW, Shen JH (1991) Embryology of Astragalus mongholicus Bunge. Acta Bot Sinica 33:19–25
Tirlapur UK, Willemse MTM (1992) Changes in calcium and calmodulin levels during microsporogenesis, pollen development and germination in Gasteria verrucosa (Mill.)H. Duval. Sex Plant Reprod 5:214–223
Tomlinson PB (1966) Anatomical data in the classification of Commelinaceae. Bot J Linn Soc 59:371–395
Tomlinson PB (1969) Commelinales-Zingiberales. In: Metcalfe CR (ed) Anatomy of the monocotyledons III. Clarendon Press, Oxford
Tütüncü KS, Öztürk N, Feruzan D (2014) Occurrence, types and distribution of calcium oxalate crystals in leaves and stems of some species of poisonous plants. Bot Stud 55:32
Vogel S (1978) Evolutionary shifts from reward to deception in pollen flowers. In: Richards AJ (ed) The pollination of flowers by insects. Linnaean Society Symposium Series No. 6, New York, pp 89–104
Walker GWR (1957) The effects of colchicine on microsporogenesis in cultured anthers of Tradescantia paludosa. Am J Bot 44:690–696
Webb MA (1999) Cell-mediated crystallization of calcium oxalate in plants. Plant Cell 11:751–761
Willemse MTM (1993) Calcium and calmodulin distribution in the tapetum of Gasteria verrucosa during anther development. In: Hesse M, Paccini E, Willemse M (eds) The tapetum: cytology, function, biochemistry and evolution. Springer-Verlag, New York, pp 107–116
Zindler-Frank E (1976) Oxalate biosynthesis in relation to photosynthetic pathway and plant productivity-a survey. Z Pflanzenphysiol 80:1–13
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The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (http://www.plantcell.org): Krystyna Winiarczyk (krystyna.winiarczyk@poczta.umcs.lublin.pl.
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Gębura, J., Winiarczyk, K. A study on calcium oxalate crystals in Tinantia anomala (Commelinaceae) with special reference to ultrastructural changes during anther development. J Plant Res 129, 685–695 (2016). https://doi.org/10.1007/s10265-016-0812-5
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DOI: https://doi.org/10.1007/s10265-016-0812-5