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Abstract
In this study, the micromorphology of the vegetative and reproductive structures of the endemic Centaurea glaberrima Tausch subsp. divergens (Vis.) Hayek (Asteraceae), using scanning electron microscope (SEM), is presented for the first time. Uniseriate whip-like non-glandular and biseriate glandular trichomes are found on the surface of all aboveground parts (stem, leaves, peduncles, involucral bract). On the adaxial leaf epidermis ribbed thickenings (striation pattern) of outer periclinal cell walls, slightly curved anticlinal cell walls and anomocytic stomata are noticed. Rugose abaxial surface with thorny protuberances of the involucral bract is documented. Corolla is glabrous with longitudinally parallel epidermal cells with distinct straight outline. Isopolar, radially symmetric and tricolporate microechinate pollen grains are seen. Short stylar hairs, without cuticular striations, are present along the outer sides of the style, while the inner sides (abaxial surface) constitute the papillate stigmatic surface. Microcharacters found in cypsela are as follows: slightly ribbed body; rotund base; lateral and concave insertion; short, unicellular curly acute trichomes; smooth epidermis; fine-sulcate ornamentation; rod shaped epidermal cells with short, obtuse end walls and straight anticlinal walls; poorly developed minutely dentate pericarp rim; and dimorphic pappus with bristles of different length and morphology, with pinnules restricted to the margins of the bristles. The results obtained contribute to knowledge about the micromorphology of the studied endemic species and provide features for its better identification. The taxonomic significance of the analyzed characters is discussed. Some well defined microcharacters of the studied species might have taxonomic value.
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Copyright (c) 2022 Milan Gavrilovic, Pedja Janackovic
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References
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- Baagøe, J., 1977: Microcharacters in the ligules of the Compositae. In: Heywood, V.H., Harbourne, J.B., Turner, B.L. (eds.), The biology and chemistry of Compositae, 119–139. Academic Press, New York.
- Barthlott, W., 1981: Epidermal and seed surface characters of plants: systematic applicability and some evolutionary aspects. Nordic Journal of Botany 1, 345–355.
- Barthlott, W., 1984: Microstructural Features of Seed Surfaces. In: Heywood, V.H., Moore, D.M. (eds.), Current concepts in plant taxonomy, 95–105. Academic Press, London.
- Barthlott, W., Neinhuis, C., Cutler, D., Ditsch, F., Meusel, I., Theisen, I., Wilhelmi, H., 1998: Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean society 126, 237–260.
- Baser, B., Hayta, S., Dogan, G., Celik, S., Aksoy, H., 2019: Micromorphological study of Centaurea L. (Asteraceae); some taxa of eight sections analysed with scanning electron microscopy and light microscopy. Biologia 74, 583–597.
- Bean, A.R., 2001: Pappus morphology and terminology in Australian and New Zealand thistles (Asteraceae, tribe Cardueae). Austrobaileya 6, 139-152.
- Bona, M., 2014: Achene characteristics of Turkish Centaurea (Asteraceae) and their systematic application. Bangladesh Journal of Botany 43, 163–168.
- Candan, F., Uysal, T., Tugay, O., Bozkurt, M., Ertuğrul, K., Demirelma, H., 2016: The examinations of achene ultrastructural features of section Acrolophus (Centaurea, Asteraceae) via scanning electron microscopy. Turkish Journal of Botany 40, 147–163.
- Dittrich, M., 1968: Morphologische Untersuchungen An den Früchten der Subtribus Cardueae-Centaureinae (Compositae). Willdenowia 5, 67–107.
- Dittrich, M., 1977: Cynareae – systematic review. In: Heywood, V.H., Harborne, J.B., Turner, B.L. (eds.), The Biology and Chemistry of the Compositae 2, 999–1015. Academic Press, London, New York, San Francisco.
- Dostál, J., 1976: Centaurea glaberrima Tausch. In: Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M., Webb, D.A. (eds.), Flora Europaea. vol. 4, 278–279. Cambridge University Press.
- Erbar, C., Leins, P., 2015: Cuticular patterns on stylar hairs in Asteraceae: a new micromorphological feature. International Journal of Plant Sciences 176, 269–284.
- Erbar, C., Eichelser, C., Mögerle, S., 2018: Styles in Carduoideae (Asteraceae) – diversity in the uniformity. Plant Diversity and Evolution 132, 1–42.
- Gavrilović, M., Erić, S., Marin, P. D., Garcia-Jacas, N., Susanna, A., Janaćković, P., 2017: 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. Microscopy and Microanalysis 23, 679–686.
- Gavrilović, M., Garcia-Jacas, N., Susanna, A., Marin, P.D., Janaćković, P., 2019: How does micromorphology reflect taxonomy within the Xeranthemum group (Cardueae-Asteraceae)? Flora 252, 51–61.
- Gavrilović, M., Tešević, V., Đorđević, I., Rajčević, N., Bakhia, A., Garcia-Jacas, N., Susanna, A., Marin, P.D., Janaćković, P., 2018: Leaf micromorphology, antioxidative activity and a new record of 3-deoxyamphoricarpolide of relict and limestone endemic Amphoricarpos elegans Albov (Compositae) from Georgia. Archives of Biological Sciences 70, 613–620.
- Ghimire, B., Jeong, M.J., Lee, K.M., Heo, K., Lee, C.H., Suh, G.U., 2016: Achene morphology of Saussurea species (Asteraceae, Cardueae) in Korea and its systematic implications. Botanical Journal of the Linnean Society 181, 692–710.
- Häffner, E., 2000: On the phylogeny of the subtribe Carduinae (tribe Cardueae, Compositae). Englera 21, 1–208.
- Haratym, W., Weryszko-Chmielewska, E., Konarska, A., 2020: Microstructural and histochemical analysis of aboveground organs of Centaurea cyanus used in herbal medicine. Protoplasma 257, 285–298.
- Herrando-Moraira, S., Calleja, J.A., Galbany-Casals, M., Garcia-Jacas, N., Liu, J.Q., López-Alvarado, J., López-Pujol, J., Mandel, J.R., Massó, S., Montes-Moreno, N., Roquet, C., Sáez, L., Sennikov, A., Susanna, A., Vilatersana, R., 2019: Nuclear and plastid DNA phylogeny of the tribe Cardueae (Compositae) with Hyb-Seq data: a new subtribal classification and a temporal diversification framework. Molecular Phylogenetics and Evolution 137, 313–332.
- Hilpold, A., Garcia-Jacas, N., Vilatersana, R., Susanna, A., 2014: Taxonomical and nomenclatural notes on Centaurea: A proposal of classification, a description of new sections and subsections, and a species list of the redefined section Centaurea. Collectanea Botanica 33, e001.
- Kalmuk, N.A., Inceer, H., Imamoğlu, K.V., 2018: Achene micromorphology of 26 Crepis L. (Asteraceae) taxa from Turkey with notes on its systematic and ecological significance. Botany Letters 165, 292–306.
- Luković, J., Malenčić, D., Zorić, L., Kodranov, M., Karanović, D., Kiprovski, B., Boža, P., 2013: Anatomical characteristics and antioxidant ability of Centaurea sadleriana reveals an adaptation towards drought tolerance. Central European Journal of Biology 8, 788–798.
- Metcalfe, C.R., Chalk, L., 1972: Anatomy of the Dicotyledons: leaves, stem, and wood in relation to taxonomy, with notes on economic uses. Clarendon Press, Oxford.
- Nikolić, T., 2020: Flora Croatica – vascular flora of the Republic of Croatia, vol. 2. Alfa d.d., Zagreb (In Croatian).
- Ozcan, M., Akinci, N., 2019: Micromorpho-anatomical fruit characteristics and pappus features of representative Cardueae (Asteraceae) taxa: Their systematic significance. Flora 256, 16–35.
- Özler, H., Kaya, Z., Pehlivan, S., 2009: Pollen morphology of some Centaurea L., Psephellus Cass. and Cyanus Miller taxa. Acta Biologica Cracoviensia, Series Botanica, 51, 53–66.
- Rahiminejad, M.R., Mozaffarian, V., Montazerolghaem S., 2010: A taxonomic revision of Centaurea section Acrocentron (Asteraceae) in Iran. Botanical Journal of the Linnean Society 163, 99–106.
- Robinson, H., 2009: An introduction to micro-characters of Compositae. In: Funk, V.A., Susanna, A., Stuessy, T.F., Bayer, R.J. (eds.), Systematics, Evolution, and Biogeography of Compositae, 89–100. IAPT, Vienna.
- Rusak, G., Plese, N., Kustrak, D., 1992: Anatomical investigations of endemic species Centaurea rupestris L. and C. fritschii Hayek (Asteraceae). Acta Botanica Croatica 51, 27–36.
- Šilić, Č., 1990: Endemic plants. IP Svjetlost, Sarajevo (in Bosnian).
- Shabestari, E.S.B., Attar, F., Riahi, H., Sheidai, M., 2013: Pollen morphology of Centaurea L. (Asteraceae) in Iran. Acta Botanica Brasilica 27, 669–679.
- Small, J., 1919: The origin and development of the Compositae. New Phytologist 18, 129–176.
- Susanna, A., Garcia-Jacas, N., 2007: Tribe Cardueae. In: Kadereit, J.W., Jeffrey, C. (eds.), The families and genera of vascular plants. vol. 8, 123–146. Springer Verlag, Berlin.
- Susanna, A., Garcia-Jacas, N., 2009: Cardueae (Carduoideae). In: Funk, V.A., Susanna, A., Stuessy, T.F., Bayer, R.J. (eds.), Systematics, Evolution, and Biogeography of Compositae, 293–313. IAPT, Vienna.
- Tešević, V., Milosavljević, S., Vajs, V., Janaćković, P., Đorđević, I., Jadranin, M., Vučković, I., 2007: Quantitative analysis of sesquiterpene lactone cnicin in seven Centaurea species wild-growing in Serbia and Montenegro using 1H-NMR spectroscopy. Journal of the Serbian Chemical Society 72, 1275–1280.
- Thiers, B., 2019: Index Herbariorum: A global directory of public herbaria and associated staff, New York Botanical Garden's Virtual Herbarium. Retrieved March 21, 2021 from http://sweetgum.nybg.org/science/ih/
- Torres, C., Galetto, L., 2007: Style morphological diversity of some Asteraceae species from Argentina: systematic and functional implications. Journal of Plant Research 120, 359–364.
- Wagenitz, G., 1955: Pollen Morphologie und Systematik in der Gattung Centaurea weldeniana (Asteraceae). s.l. Flora 142, 213–279.
- Zhang, J.W., Boufford, D.E., Sun, H., 2013: Systematic significance of achene morphology in Soroseris, Syncalathium and Parasyncalathium (Asteraceae: Cichorieae). Botanical Journal of the Linnean Society 173, 476–486.
References
Adedeji, O., Jewoola, O.A., 2008: Importance of leaf epidermal characters in the Asteraceae family. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 36, 7–16.
Baagøe, J., 1977: Microcharacters in the ligules of the Compositae. In: Heywood, V.H., Harbourne, J.B., Turner, B.L. (eds.), The biology and chemistry of Compositae, 119–139. Academic Press, New York.
Barthlott, W., 1981: Epidermal and seed surface characters of plants: systematic applicability and some evolutionary aspects. Nordic Journal of Botany 1, 345–355.
Barthlott, W., 1984: Microstructural Features of Seed Surfaces. In: Heywood, V.H., Moore, D.M. (eds.), Current concepts in plant taxonomy, 95–105. Academic Press, London.
Barthlott, W., Neinhuis, C., Cutler, D., Ditsch, F., Meusel, I., Theisen, I., Wilhelmi, H., 1998: Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean society 126, 237–260.
Baser, B., Hayta, S., Dogan, G., Celik, S., Aksoy, H., 2019: Micromorphological study of Centaurea L. (Asteraceae); some taxa of eight sections analysed with scanning electron microscopy and light microscopy. Biologia 74, 583–597.
Bean, A.R., 2001: Pappus morphology and terminology in Australian and New Zealand thistles (Asteraceae, tribe Cardueae). Austrobaileya 6, 139-152.
Bona, M., 2014: Achene characteristics of Turkish Centaurea (Asteraceae) and their systematic application. Bangladesh Journal of Botany 43, 163–168.
Candan, F., Uysal, T., Tugay, O., Bozkurt, M., Ertuğrul, K., Demirelma, H., 2016: The examinations of achene ultrastructural features of section Acrolophus (Centaurea, Asteraceae) via scanning electron microscopy. Turkish Journal of Botany 40, 147–163.
Dittrich, M., 1968: Morphologische Untersuchungen An den Früchten der Subtribus Cardueae-Centaureinae (Compositae). Willdenowia 5, 67–107.
Dittrich, M., 1977: Cynareae – systematic review. In: Heywood, V.H., Harborne, J.B., Turner, B.L. (eds.), The Biology and Chemistry of the Compositae 2, 999–1015. Academic Press, London, New York, San Francisco.
Dostál, J., 1976: Centaurea glaberrima Tausch. In: Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M., Webb, D.A. (eds.), Flora Europaea. vol. 4, 278–279. Cambridge University Press.
Erbar, C., Leins, P., 2015: Cuticular patterns on stylar hairs in Asteraceae: a new micromorphological feature. International Journal of Plant Sciences 176, 269–284.
Erbar, C., Eichelser, C., Mögerle, S., 2018: Styles in Carduoideae (Asteraceae) – diversity in the uniformity. Plant Diversity and Evolution 132, 1–42.
Gavrilović, M., Erić, S., Marin, P. D., Garcia-Jacas, N., Susanna, A., Janaćković, P., 2017: 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. Microscopy and Microanalysis 23, 679–686.
Gavrilović, M., Garcia-Jacas, N., Susanna, A., Marin, P.D., Janaćković, P., 2019: How does micromorphology reflect taxonomy within the Xeranthemum group (Cardueae-Asteraceae)? Flora 252, 51–61.
Gavrilović, M., Tešević, V., Đorđević, I., Rajčević, N., Bakhia, A., Garcia-Jacas, N., Susanna, A., Marin, P.D., Janaćković, P., 2018: Leaf micromorphology, antioxidative activity and a new record of 3-deoxyamphoricarpolide of relict and limestone endemic Amphoricarpos elegans Albov (Compositae) from Georgia. Archives of Biological Sciences 70, 613–620.
Ghimire, B., Jeong, M.J., Lee, K.M., Heo, K., Lee, C.H., Suh, G.U., 2016: Achene morphology of Saussurea species (Asteraceae, Cardueae) in Korea and its systematic implications. Botanical Journal of the Linnean Society 181, 692–710.
Häffner, E., 2000: On the phylogeny of the subtribe Carduinae (tribe Cardueae, Compositae). Englera 21, 1–208.
Haratym, W., Weryszko-Chmielewska, E., Konarska, A., 2020: Microstructural and histochemical analysis of aboveground organs of Centaurea cyanus used in herbal medicine. Protoplasma 257, 285–298.
Herrando-Moraira, S., Calleja, J.A., Galbany-Casals, M., Garcia-Jacas, N., Liu, J.Q., López-Alvarado, J., López-Pujol, J., Mandel, J.R., Massó, S., Montes-Moreno, N., Roquet, C., Sáez, L., Sennikov, A., Susanna, A., Vilatersana, R., 2019: Nuclear and plastid DNA phylogeny of the tribe Cardueae (Compositae) with Hyb-Seq data: a new subtribal classification and a temporal diversification framework. Molecular Phylogenetics and Evolution 137, 313–332.
Hilpold, A., Garcia-Jacas, N., Vilatersana, R., Susanna, A., 2014: Taxonomical and nomenclatural notes on Centaurea: A proposal of classification, a description of new sections and subsections, and a species list of the redefined section Centaurea. Collectanea Botanica 33, e001.
Kalmuk, N.A., Inceer, H., Imamoğlu, K.V., 2018: Achene micromorphology of 26 Crepis L. (Asteraceae) taxa from Turkey with notes on its systematic and ecological significance. Botany Letters 165, 292–306.
Luković, J., Malenčić, D., Zorić, L., Kodranov, M., Karanović, D., Kiprovski, B., Boža, P., 2013: Anatomical characteristics and antioxidant ability of Centaurea sadleriana reveals an adaptation towards drought tolerance. Central European Journal of Biology 8, 788–798.
Metcalfe, C.R., Chalk, L., 1972: Anatomy of the Dicotyledons: leaves, stem, and wood in relation to taxonomy, with notes on economic uses. Clarendon Press, Oxford.
Nikolić, T., 2020: Flora Croatica – vascular flora of the Republic of Croatia, vol. 2. Alfa d.d., Zagreb (In Croatian).
Ozcan, M., Akinci, N., 2019: Micromorpho-anatomical fruit characteristics and pappus features of representative Cardueae (Asteraceae) taxa: Their systematic significance. Flora 256, 16–35.
Özler, H., Kaya, Z., Pehlivan, S., 2009: Pollen morphology of some Centaurea L., Psephellus Cass. and Cyanus Miller taxa. Acta Biologica Cracoviensia, Series Botanica, 51, 53–66.
Rahiminejad, M.R., Mozaffarian, V., Montazerolghaem S., 2010: A taxonomic revision of Centaurea section Acrocentron (Asteraceae) in Iran. Botanical Journal of the Linnean Society 163, 99–106.
Robinson, H., 2009: An introduction to micro-characters of Compositae. In: Funk, V.A., Susanna, A., Stuessy, T.F., Bayer, R.J. (eds.), Systematics, Evolution, and Biogeography of Compositae, 89–100. IAPT, Vienna.
Rusak, G., Plese, N., Kustrak, D., 1992: Anatomical investigations of endemic species Centaurea rupestris L. and C. fritschii Hayek (Asteraceae). Acta Botanica Croatica 51, 27–36.
Šilić, Č., 1990: Endemic plants. IP Svjetlost, Sarajevo (in Bosnian).
Shabestari, E.S.B., Attar, F., Riahi, H., Sheidai, M., 2013: Pollen morphology of Centaurea L. (Asteraceae) in Iran. Acta Botanica Brasilica 27, 669–679.
Small, J., 1919: The origin and development of the Compositae. New Phytologist 18, 129–176.
Susanna, A., Garcia-Jacas, N., 2007: Tribe Cardueae. In: Kadereit, J.W., Jeffrey, C. (eds.), The families and genera of vascular plants. vol. 8, 123–146. Springer Verlag, Berlin.
Susanna, A., Garcia-Jacas, N., 2009: Cardueae (Carduoideae). In: Funk, V.A., Susanna, A., Stuessy, T.F., Bayer, R.J. (eds.), Systematics, Evolution, and Biogeography of Compositae, 293–313. IAPT, Vienna.
Tešević, V., Milosavljević, S., Vajs, V., Janaćković, P., Đorđević, I., Jadranin, M., Vučković, I., 2007: Quantitative analysis of sesquiterpene lactone cnicin in seven Centaurea species wild-growing in Serbia and Montenegro using 1H-NMR spectroscopy. Journal of the Serbian Chemical Society 72, 1275–1280.
Thiers, B., 2019: Index Herbariorum: A global directory of public herbaria and associated staff, New York Botanical Garden's Virtual Herbarium. Retrieved March 21, 2021 from http://sweetgum.nybg.org/science/ih/
Torres, C., Galetto, L., 2007: Style morphological diversity of some Asteraceae species from Argentina: systematic and functional implications. Journal of Plant Research 120, 359–364.
Wagenitz, G., 1955: Pollen Morphologie und Systematik in der Gattung Centaurea weldeniana (Asteraceae). s.l. Flora 142, 213–279.
Zhang, J.W., Boufford, D.E., Sun, H., 2013: Systematic significance of achene morphology in Soroseris, Syncalathium and Parasyncalathium (Asteraceae: Cichorieae). Botanical Journal of the Linnean Society 173, 476–486.