Petiole anatomical features in Salix and some of its relatives in the family Salicaceae

Document Type : Research Paper

Authors

1 MSc Graduate, Plant Systematics, Department of Plant Sciences, Faculty of Biological Sciences, Kharazmi University, Tehran 15719-14911, Iran

2 Prof., Department of Plant Sciences, Faculty of Biological Sciences, Kharazmi University, Tehran 15719-14911, Iran

3 Assistant Prof., Department of Plant Sciences, Faculty of Biological Sciences, Kharazmi University, Tehran 15719-14911, Iran

Abstract

The classification of the genus Salix is troubled by the intra-specific flexibility and diversity of the morphological features. The aim was to prepare a comparative description of petiole anatomy of 23 species of Salix, in addition to two species of Populus and Bivinia jalbertii, as well as to determine the taxonomic importance of petiole features. In order to do so, 10 quantitative and 10 qualitative petiole anatomical features were studied. Moreover, a Bayesian analysis was executed on the relevant ITS sequences obtained from GenBank, included 28 specimens from 17 species. The anatomical features were then mapped on the resulted cladogram and the ancestral states of some prominent petiole anatomical features were reconstructed. Based on the results, no stomata were observed in the petiole's epidermis of any of the species studied; therefore, it could be assumed that, the petiole in the studied species is dependent to the leaf blade for respiration and gas exchange. While the quantitative petiole anatomical features were turn to be variable in the individuals of the same species grown in different habitats, qualitative features showed a desirable consistency. The petiole anatomical features studied were proved to be useful in the differentiation and identification of taxa at sub-generic and specific levels. In addition, the reconstruction of the ancestral state of the studied features revealed that, polygonal cell shape, straight or slightly curved anticlinal wall pattern, horizontal compression of the petiole, the presence of lateral ribs, convex adaxial surface and ribbed petiole outline were primitive features in the species studied.
 

Keywords


Article Title [Persian]

صفات تشریحی دمبرگ در بید و برخی از خویشاوندانش در تیره بیدیان

Authors [Persian]

  • شکوفه حمزه لو 1
  • فرخ قهرمانی نژاد 2
  • احسان حسینی 3
1 دانش‌آموخته کارشناسی ارشد سیستماتیک گیاهی، گروه علوم گیاهی، دانشکده علوم زیستی، دانشگاه خوارزمی، تهران 14911-15719، ایران
2 استاد گروه علوم گیاهی، دانشکده علوم زیستی، دانشگاه خوارزمی، تهران 14911-15719، ایران
3 استادیار گروه علوم گیاهی، دانشکده علوم زیستی، دانشگاه خوارزمی، تهران 14911-15719، ایران
Abstract [Persian]

رده‌بندی جنس L.  Salix (تیره بیدیان) به دلیل انعطاف‌پذیری و تنوع درون گونه‌ای در صفات ریخت‌شناختی مشکل‌آفرین است. هدف از این پژوهش، توصیف و مقایسه تشریح دمبرگ 23 گونه از جنس Salix، دو گونه از جنس Populus L.  و گونه Tul.  Bivinia jalbertii و همچنین تعیین اهمیت سیستماتیکی صفات تشریحی دمبرگ است. به این منظور، 10 صفت کمّی و 10 صفت کیفی مرتبط با تشریح دمبرگ بررسی و ارزیابی شدند. علاوه بر این، تحلیل بیزین روی توالی ITS موجود از 28 نمونه از 17 گونه مرتبط موجود در GenBank انجام شد، صفات تشریحی روی کلادوگرام به دست آمده مکان‌یابی شدند و حالت اجدادی برخی صفات تشریحی بازسازی شد. براساس نتایج به دست آمده، هیچ یک از 26 گونه بررسی شده دارای روزنه در دمبرگ نبود و بنابراین، می‌توان نتیجه گرفت که دمبرگ برای تنفس و تبادل گاز متکی به پهنک است. با وجود آن که صفات کمّی بین افراد مختلف یک گونه که در زیستگاه‌های مختلف رویش کرده بودند متغیر بود، صفات کیفی ثبات خوبی از خود نشان دادند. صفات تشریحی دمبرگ در گونه‌های بررسی شده با موفقیت جهت تمایز بین آرایه‌های زیرجنسی و گونه‌ها به کار برده شدند. به علاوه، بازسازی حالت اجدادی صفات بررسی شده نشان داد که شکل سلولی چندضلعی، الگوی صاف تا اندکی خمیده در دیواره‌های آنتی‌کلینال سلول‌های اپیدرم، فشردگی افقی دمبرگ، حضور پره‌های جانبی در دمبرگ، سطح فوقانی محدب و حاشیه شیاردار دمبرگ، صفات ابتدایی در گونه‌های بررسی شده بودند.

Keywords [Persian]

  • تبارزایشی
  • شاتون‌داران
  • صنوبر
  • مالپیگیال
  • Bivinia
Abdollahzadeh, A., Kazempour, O.S. & Maassoumi, A.A. 2011. Molecular phylogeny of the genus Salix (Salicaceae) with an emphasize to its species in Iran. Iranian Journal of Botany 17(2): 244–253.
Anderssonn, N.J. 1868. Salicineae. Pp. 190–323. In: de Candolle, A. Prodromus Systematis Naturalis Regni Vegetabilis, Vol. 16(2). Treuttel & Wurtz, Paris.
Angaji, S.A., Ghahremaninejad, F., Mousavi, S.F. & Tabrizi, F.M. 2012. Study of genetic variation in Salix using molecular markers. Advances in Environmental Biology 6(11): 2982–2985.
Argus, G.W. 1997. Infrageneric classification of Salix (Salicaceae) in the new world. Systematic Botany Monographs 52: 1–121.
Argus, G.W. 2007. Salix distribution maps and synopsis of their classification in North American, North of Mexico. Harvard Press in Botany 12: 335–368.
Argus, G.W. 2010. Salix. Pp. 23–51. In: Flora of North America, Editorial Committee. Vol. 7: Magnoliophyta: Salicaceae to Brassicaceae. New York: Oxford University Press.
Barkalov, V.Y. & Kozyrenko, M.M. 2014a. Phylogenetic analysis of the Far Eastern Salix (Salicaceae) based on sequence data from chloroplast DNA regions and ITS of nuclear ribosomal DNA. Botanica Pacifica. Journal of Plant Science and Conservation 3(1): 3–19.
Barkalov, V.Y. & Kozyrenko, M.M. 2014b. Phylogenetic relationships of Salix L. subg. Salix species (Salicaceae) according to sequencing data of intergenic spacers of the chloroplast genome and ITS rDNA. Russian Journal of Genetics 50(8): 828–837.
Binns, W.W. & Blunden, G. 1980. Comparative leaf anatomy of Salix species and hybrids. Botanical Journal of the Linnean Society 81(3): 205–214.
Boissier, E.P. 1879. Flora Orientalis: sive, Enumerato plantarum in Oriente a Graecia et Aegypto ad Indiae fines hucusque observatarum. Corolliflorae et Monochlamydeae. Volumen quartum (Vol. 4). Apud H. Georg, Bibliopolam.
Chao, N., Gong, G.T. & Liu, J. 1998. On the classification and distribution of the family Salicaceae. Journal of Sichuan Forestry Science and Technology 19(4): 9–20.
Chase, M.W., Christenhusz, M.J.M., Fay, M.F., Byng, J.W., Judd, W.S., Soltis, D.E., Mabberley, D.J., Sennikov, A.N., Soltis, P.S. & Stevens, P.F. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181(1): 1–20.
Chase, M.W., Zmarzty, S., Lledo, M.D., Wurdack, K.J., Swensen, S.M. & Fay, M.F. 2002. When in doubt, put it in Flacourtiaceae: a molecular phylogenetic analysis based on plastid rbcL DNA sequences. KEW Bulletin 57(1): 141–181.‏
Chen, J.H., Sun, H., Wen, J. & Yang, Y.P. 2008a. Cladistic analysis of the genus Salix (Salicaceae). Acta Metallurgica Sinica 30: 1–7.
Chen, J.H., Sun, H. & Yang, Y.P. 2008b. Comparative morphology of leaf epidermis of Salix (Salicaceae) with special emphasis on sections Lindleyanae and Retusae. Botanical Journal of the Linnean Society 157(2): 311–322.
Chen, J.H., Sun, H., Wen, J. & Yang, Y.P. 2010. Molecular phylogeny of Salix L. (Salicaceae) inferred from three chloroplast datasets and its systematic implications. Taxon 59(1): 29–37.
Christenhusz, M.J.M. & Byng, J.W. 2016. The number of known plants species in the world and its annual increase. Phytotaxa 261(3): 201–217.
Dallwitz, M.J., Paine, T.A. & Zurcher, E.J. 2007. DELTA: Description Language for Taxonomy. Computer software and manuals, CSIRO. Available at: http://delta-intkey.com.
de Jussieu, A.L. 1789. Genera plantarum, secundum ordines naturales disposita, juxta methodum in Horto regio parisiensi exaratam, anno M. DCC. LXXIV. Parisiis: apud viduam Herissant et Theophilum Barrois.
de Mirbel C.F.B. 1815. Élemens de physiologie végétale et de botanique (Vol. 2). Magimel.
Diffey, J.M. 2017. Phylogenetic relationships of Salicaceaebased on analyses of nuclear DNA data. B.Sc. Thesis submitted in University of Southern Mississippi.
Dumortier, M.B. 1862. Monographie des Saules de la flore belge. Bulletin de la Société Royale de Botanique de Belgique 1: 130–147.
Engler, A. 1884. Botanische Jahrbücher fur Systematik, Pflanzengeschichte und Pflanzengeographie (Vol. 5). Leipzig: Verlag von Wilhelm Engelmann.
Ghahremaninejad, F., Khalili, Z., Maassoumi, A.A., Mirzaie-Nodoushan, H. & Riahi, M. 2012. Leaf epidermal features of Salix species (Salicaceae) and their systematic significance. American Journal of Botany 99(4): 769–777.
Gray, S.F. 1821. A natural arrangement of British plants: According to their relations to each other as pointed out by Jussieu, De Candolle, Brown & c. (Vol. 2). London: Baldwin, Cradock and Joy.
Hallier, H. 1908. Über Juliania: eine Terebinthaceen-Gattung mit Cupula, und die wahren Stammeltern der Kätzchenblütler. Neue Beiträge zur Stammesgeschichte der Dicotyledonen. Heinrich Press, Dresden, pp. 81–265.
Hardig, T.M., Anttila, C.K. & Brunsfeld, S.J. 2010. A phylogenetic analysis of Salix (Salicaceae) based on matK and ribosomal DNA sequence data. Journal of Botany. Article ID 197696.
doi: 10.1155/2010/197696.
Hooker, W.J. & Arnott, G.A.W. 1855. The British flora: comprising the phaenogamous or flowering plants, and the ferns. London: Longman, Brown, Green, and Longmans.
Humbert, H. & Leroy, J.F. 1946. Flore de Madagascar et des Comores: plantes vasculaires, fam 140 Flacourtiacées. Tananarive: Imprimerie officielle.
Isebrands, J.G. & Richardson, J. (eds). 2014. Poplars and willows: trees for society and the environment. CABI.
Khalili, Z., Maassoumi, A.A., Ghahremaninejad, F. & Mirzaie-Nodoushan, H. 2010. Foliar anatomy of some Salix species (Salicaceae) in Iran. Iranian Journal of Botany 16(2): 293–302.
Khalili, Z., Mirzaie-Nodoushan, H., Ghahremaninejad, F. & Maassoumi, A.A. 2012. Chromosome number and meiosis behavior in several Salix species of Iran. Caryologia 65(4): 258–262.
Kimura, A. 1928. Über Toisusu-eine neue Salicaceen-Gattung und die systematische stellung derselben. Botanical Magazine Tokyo 42: 287–290.
Klimov, A.V. & Proshkin, B.V. 2019. Identification of Populus nigra, P. laurifolia and P. × jrtyschensis by leaf petiole anatomy. Siberian Journal of Forest Science 6: 89–99.
Larkin,M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.
Lauron-Moreau, A., Pitre, F.E., Argus, G.W., Labrecque, M. & Brouillet, L. 2015. Phylogenetic relationships of American willows (Salix L., Salicaceae). PLoS One 10(4): e0121965.
doi: 10.1371/journal.pone.0121965.
Leskinen, E. & Alström-Rapaport, C. 1999. Molecular phylogeny of Salicaceae and closely related Flacourtiaceae: Evidence from 5.8 S, ITS 1 and ITS 2 of the rDNA. Plant Systematics and Evolution 215(1–4): 209–227.
Li, M.M., Wang, D.Y., Zhang, L., Kang, M.H., Lu, Z.Q., Zhu, R.B., Mao, X.X., Xi, Z.X. & Ma, T. 2019. Intergeneric relationships within the family Salicaceae s.l. based on plastid phylogenomics. International Journal of Molecular Sciences 20(15): 3788. https://doi.org/10.3390/ijms20153788.
Lindley, J. 1830. An introduction to the natural system of botany: or, A systematic view of the organisation, natural affinities, and geographical distribution, of the whole vegetable kingdom: together with the uses of the most important species in medicine, the arts, and rural or domestic economy, London: Longman, Rees, Orme, Brown, and Green.
Linnaeus, C. 1737. Genera plantarum: eorumque characteres naturales secundum numerum, figuram, situm, & proportionem omnium fructificationis partium. Leiden: Wishoff.
Linnaeus, C. 1753. Species plantarum: exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Vol. II. Holmiae: Impensis Laurentii Salvii.
Liu, X., Wang, Z., Wang, D. & Zhang, J. 2016. Phylogeny of Populus-Salix (Salicaceae) and their relative genera using molecular datasets. Biochemical Systematics and Ecology 68: 210–215.
Loudon, J.C. 1838. Arboretum et fruticetum Britannicum; or, The trees and shrubs of Britain (Vol. 2). Longman, Orme, Brown, Green, and Longmans.
Maassoumi, A.A. 2009. Experimental taxonomy of the genus Salix L. (Salicaceae) in Iran. Iranian Journal of Botany 15: 3–20.
Maassoumi, A.A., Assadi, M. & Hemmati, A. 2011. Salicaceae, In: Assadi et al. (eds), Flora of Iran No. 74. Research Institute of Forests and Rangelands Publication, Tehran.
Mabberley, D.J. 2018. Mabberley's plant-book: a portable dictionary of plants, their classification and uses (4th. ed.). Cambridge University Press.
Maddison, W.P. & D.R. Maddison 2019. Mesquite: a modular system for evolutionary analysis. Version 3.61. Available at: http://www.mesquiteproject.org.
Nylander, J.A.A. 2004. MrModeltest v. 2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
Ohashi, H. 2000. A systematic enumeration of Japanese Salix (Salicaceae). Journal of Japanese Botany 75(1): 1–41.‏
Paiero, P., Semenzato, P. & Urso, T. 1992. Anatomical and morphological microfeatures of the leaf in Salix L. species and their physioecological significance. Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences 98: 245–245.
Persson, C., Ståhl, B., Lægaard, S. & Balslev, H. 2014. Flora of Ecuador, Vol. 91: Parts 22  Myricaceae. 23. Juglandaceae: 24. Salicaceae. 25A. Betulaceae. 25B. Casuarinaceae. 26A Ulmaceae. 26B. Cannabaceae. In: Flora of Equador 91. University of Gothenburg.
Proshkin, B.V. & Klimov, A.V. 2019. Using petiole anatomy to identify hybrids between and species of Populus sections Aigeiros and Tacamahaca. Turczaninowia 22: 80–90. doi: 10.14258/turczaninowia.22.3.3.
Rambaut, A. 2012. “igTree: tree figure drawing tool version 1.4.4, Available at: http://tree.bio.ed.ac.uk/ software/figtree.
Rechinger, K.H. & Akeroyd, J.R. 1964. Salix L. Pp. 43–54. In: Tutin, T.G., Heywood, V.H., Burges, N.A. & Valentine, D.H. (eds), Flora Europaea, Vol. 1.
Richard, A. 1828. Nouveaux éléments de botanique et de physiologie végétale. Paris: Béchet Jeune.
Richard, A. & MacGillivray, W. 1831. Elements of botany and vegetable physiology: including the characters of the natural families of plants. Edinburgh: William Blackwood and Sons.
Ronquist, F. & Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12): 1572–1574.
Skvortsov, A.K. 1968. Willows of the USSR. Nauka, Moscow, USSR (In Russian).
Skvortsov, A.K. 1969. Salix. Pp. 12–43. In: K.H. Rechinger (ed.). Salicaceae, Flora Iranica, No. 65. Akademische Druck-u. Verlagsanstalt, Graz, Austria.
Skvortsov, A.K. 1999. Willows of Russia and adjacent countries, taxonomical and geographical revision. English edition/translated by I.N. Kadis. University of Joensuu, Finland.
Su, H., Li, Y., Lan, Z., Xu, H., Liu, W., Wang, B., Biswas, D.K. & Jiang, G. 2009. Leaf-level plasticity of Salix gordejevii in fixed dunes compared with lowlands in Hunshandake Sandland, North China. Journal of plant research 122(6): 611–622.
Thadeo, M., Azevedo, A.A. & Meira, R.M. 2014. Foliar anatomy of neotropical Salicaceae: potentially useful characters for taxonomy. Plant Systematics and Evolution 300: 2073–2089. doi: 10.1007/s00606-014-1037-5.
Wu, J., Nyman, T., Wang, D.C., Argus, G.W., Yang, Y.P. & Chen, J.H. 2015. Phylogeny of Salix subgenus Salix s.l. (Salicaceae): delimitation, biogeography, and reticulate evolution. BMC Evolutionary Biology 15: 31. doi: 10.1186/s12862-015-0311-7.