Research Paper

Pollen morphology of the Galium L. (Rubieae-Rubiaceae) from Pakistan and evaluation of its systematic significance

Tariq Ullah, Amjad Khan, Raees Khan, Amir Sultan, Shahab Ali, Mohsin Kazi

Published on: 19 March 2025

Page: 207 - 218

DOI: 10.6165/tai.2025.70.207

Abstract

Galium is a typical member of the tribe Rubieae, characterized by its 3 or 4-lobed corolla, rudimentary corolla tubes, corolla tube length and dry mericarps and has a ubiquitous distribution. In this study pollen morphology of 20 species of Galium from Pakistani highland was investigated and documented in detail using light and scanning electron microscopy. The genus Galium itself is a delimited natural group and its taxa are poorly explored for pollen morphology. Among the investigated species, pollen grains are small to large (P=13.05–21.75 μm, E=17.00–24.20 μm), oblate–spheroidal, suboblate, subprolate and prolate–spheroidal (P/E=0.84–1.16) in shape and 5–10 colpate. Exine sculpturing under SEM showing different ornamentations, including microechinate–scabrate, scabrate–punctate, microreticulate–scabrate, microspine–scabrate, microechinate–punctate, microspine–verrucate, microechinate–verrucate, microspine–perforate, scabrate–verrucate and microechinate–perforate among the investigated taxa. In addition, based on pollen morphometric traits, hierarchical clustering (UPGMA) analysis is performed for correlation between the species. However, pollen traits alone or with the combination of morphological characters are used in the infrageneric relationships and also provide useful information for its evolutionary history.

Keyword: Galium, Pakistan, Palynotaxonomy, SEM, UPGMA

Literature Cited

Abdel Khalik, K., Abd El-Ghani, M.M., Elkordy, A. 2007 A palynological study of Galium L. (Rubiaceae) in Egypt and its systematic implication. Feddes Repert. 118(7-8): 311–326.
DOI: 10.1002/fedr.200711137View Article Google Scholar

Abdel Khalik, K., El-Ghani, M. A., El Kordy, A. 2008a Fruit and seed morphology in Galium L. (Rubiaceae) and its importance for taxonomic identification. Acta Bot. Croat. 67(1): 1–20.

Abdel Khalik, K.N., Abd El-Ghani, M.M., El Kordy, A. 2008b Numerical taxonomy of Galium (Rubiaceae) in Egypt. Hytologia Balcacia 14(2): 245–253.

Al-Taie, T.A., Sadek, A.A. 2023 Palynological Study for some Species of Rubiaceae in Iraq.Biol. Appl. Environ. Res 7(1): 58–64.

Ba?er, B., Akdeniz, S., Kur?at, M. 2020 Palynomorphological studies on some Asperula and Galium (Rubiaceae) taxa. Bitlis Eren ?niversitesi Fen Bilimleri Dergisi 9(2): 689–696.
DOI: 10.17798/bitlisfen.652353View Article Google Scholar

Boissier, E. 1881 Galium L., Calyciflorae gamopetalae, Basileae. (H. Georg) In: Flora Orientalis. 3:1881–1033.

Chen, T., Ehrendorfer, F. 2011 Galium L. Flora of China 19: 104–141.

Chouhan, A., Dintu, K. P., Kumar, A., Jha, A., Bedi, M. 2022 Palynological Diversity In Selected Medicinal Plant Species Of Rubiaceae From Flora Of India. J. Pharm. Negat. Results 13(10): 6109–6122.

De Block, P., Robbrecht, E. 1998 Pollen morphology of the Pavetteae (Rubiaceae, Ixoroideae) and its taxonomic significance. Grana 37(5): 260–275.
DOI: 10.1080/00173139809362678View Article Google Scholar

De Toni, K.L., Mariath, J.E. 2011 Developmental Anatomy and Morphology of the Flowers and Fruits of Species from Galium and Relbunium (Rubieae, Rubiaceae) 1. Ann. Missouri Bot. Gard. 98(2): 206–225.
DOI: 10.3417/2008016View Article Google Scholar

Dessein, S., Ochoterena, H., De Block, P., Lens, F., Robbrecht, E., Schols, P., Huysmans, S. 2005 Palynological characters and their phylogenetic signal in Rubiaceae. Bot. Rev. 71(3):354–414.
DOI: 10.1663/0006-8101(2005)071[0354:PCATPS]2.0.CO;2View Article Google Scholar

Ehrendorfer, F. 2010 New and critical taxa of Rubia and Galium (Rubiaceae, Rubieae) for the Flora of China. Novon 20(3): 268–277.
DOI: 10.3417/2009087View Article Google Scholar

Ehrendorfer, F., Barfuss, M.H. 2014 Paraphyly and Polyphyly in the Worldwide Tribe Rubieae (Rubiaceae): Challenges for Generic Delimitation1, 2. Ann. Missouri Bot. Gard. 100(1-2):79–88.
DOI: 10.3417/2012088View Article Google Scholar

Ehrendorfer, F., Barfuss, M.H., Manen, J.F., Schneeweiss, G.M. 2018 Phylogeny, character evolution and spatiotemporal diversification of the species-rich and world-wide distributed tribe Rubieae (Rubiaceae). PLoS One 13(12): e0207615.
DOI: 10.1371/journal.pone.0207615View Article Google Scholar

Ehrendorfer, F., Schonbeck-Temesy, E., Puff, C., Rechinger, W. 2005 Rubiaceae. In: Rechinger KH eds. Flora Iranica. Vienna: Ann. Naturhist. Mus. Wien, Bot 176:47–72.

Elkordy, A.M., Schanzer, I.A. 2015 Fruit morphology in Galium section Platygalium (Rubiaceae) and its potential taxonomic significance. Turczaninowia 18(1):82–89.
DOI: 10.14258/turczaninowia.18.1.9View Article Google Scholar

Erdtman, G. 1960 The acetolysis method. Seven Bot. Tidskr 54: 561–564.

Faegri, K., Iversen, J. 1964 Textbook of Pollen Analysis of Rubiaceae. In: Nasir, E., Ali, S.I. (Eds.) Flora of Pakistan. Karachi University, Pakistan 76: 1–35.

Ferrer-Gallego, P.P. 2020 Typification of Linnaean specific names in the genus Galium (Rubiaceae). Taxon 69(5): 1062–1071.
DOI: 10.1002/tax.12243View Article Google Scholar

Govaerts, R., Ruhsam, M., Andersson, L., Robbrecht, E., Bridson, D.M., Davis, A.P., Schanzer, I., Sonk?, B. 2011. World Checklist of Rubiaceae, R.B.G Kew.

Halbritter, H., Ulrich, S., Gr?msson, F., Weber, M., Zetter, R., Hesse, M., Svojtka, M., Frosch-Radivo, A. 2018 Illustrated Pllen Terminology. Springer.
DOI: 10.1007/978-3-319-71365-6View Article

Hesse, M., Halbritter, H., Weber, M. 2009 Beschorneria yuccoides and Asimina triloba (L.) Dun: examples for proximal polar germinating pollen in angiosperms. Grana 48(3): 151–159.
DOI: 10.1080/00173130903024343View Article Google Scholar

Huysmans, S., Dessein, S., Smets, E., Robbrecht, E. 2003 Pollen morphology of NW European representatives confirms monophyly of Rubieae (Rubiaceae). Rev. Palaeobot. Palynol 127(3-4): 219–240.
DOI: 10.1016/S0034-6667(03)00121-0View Article Google Scholar

Johansson, J.T. 1987 Pollen morphology of the tribe Morindeae (Rubiaceae). Grana 26(2): 134–150.
DOI: 10.1080/00173138709429943View Article Google Scholar

Khan, A., Ahmad, M., Sultan, A., Ullah, Z., Majeed, K., Ullah, T., Zafar, M. 2024 Contribution to the pollen morphology of Astragalus L. section Aegacantha Bunge (Galegeae-Fabaceae) and its systematic significance. Palynology 48(1): 1–14.
DOI: 10.1080/01916122.2023.2264352View Article Google Scholar

Khan, R., Abidin, S.Z.U., Ahmad, M., Zafar, M., Liu, J., Amina, H. 2018 Palyno-morphological characteristics of gymnosperm flora of Pakistan and its taxonomic implications with LM and SEM methods. Microsc. Res. Tech. 81(1): 74–87.
DOI: 10.1002/jemt.22958View Article Google Scholar

Khan, R., Abidin, S.Z.U., Mumtaz, A.S., Jamsheed, S., Ullah, H. 2017 Comparative leaf and pollen micromorphology on some Grasses taxa (Poaceae) distributed in Pakistan. Int. J. Nat. Sci. 1(2): 72–82

Kirpicznikov, M.E. 1969 The flora of the USSR. Taxon 18(6): 685–708.
DOI: 10.2307/1218928View Article Google Scholar

Kliphuis, E. 1986 Cytotaxonomic investigations on some species of the genus Galium (Rubiaceae) from the Balkans. Nord. J. Bot. 6(1): 15–20.
DOI: 10.1111/j.1756-1051.1986.tb00854.xView Article Google Scholar

Kumar, A., Ranjan, V., Srivastava, S. 2013 Galium kulluense (Rubiaceae) - A new species from Kullu, Himachal Pradesh, India. J. Jpn. Bot. 88: 163–165.

Mill, R.R. 1996 The Galium acutum and G. asperifolium species complexes in the eastern Himalaya. Edinb. J. Bot. 53(2): 193–213.
DOI: 10.1017/S0960428600002857View Article Google Scholar

Minareci, E., Y?ld?z, K., ??rp?c?, A. 2010 Comparative morphological and palynological study on poorly known Asperula serotina and its closest relative A. purpurea subsp. apiculata. Sci. Res. Essays. 5(17): 2472–2479.

Natali, A., Manen, J.F., Ehrendorfer, F. 1995 Phylogeny of the Rubiaceae-Rubioideae, in particular the tribe Rubieae: evidence from a non-coding chloroplast DNA sequence. Ann. Missouri Bot. Gard. 82(3): 428–439.
DOI: 10.2307/2399892View Article Google Scholar

Nazimuddin, S., Ehrendorfer, F. 1987 Three new species of Galium (Rubiaceae) from Pakistan. Pl. Syst. Evol. 155(1-4): 71-75.
DOI: 10.1007/BF00936290View Article Google Scholar

Nazimuddin, S., Qaiser, M. 1989 Rubiaceae. In: Flora of Pakistan. (Eds.): S.I. Ali & E. Nasir.190: 1–145.

Parsapanah, S., Faghir, M.B. 2021 Pollen morphology and its taxonomic significance of the genus Crucianella L. (Rubiaceae) in Iran. Feddes Repert. 132(3): 287–300.
DOI: 10.1002/fedr.202000037View Article Google Scholar

Perveen, A., Qaiser, M. 2007 Pollen flora of Pakistan - Liv. Rubiaceae. Pak. J. Bot. 39(4): 999.

Pobedimova, E.G. 1958 The genus Galium L. Flora of the USSR. Moscow; Ler ningrad: 23: 100–115.

Puff, C. 1977 The Galium obtusum group (Galium sect. Aparinoides, Rubiaceae). Bull. Torrey Bot. Club. 104(3): 202–208.
DOI: 10.2307/2484299View Article Google Scholar

Punt, W., Blackmore, S., Nilsson, S., Le Thomas, A. 1994 Glossary of pollen and spore terminology: LPP Contributions series No. 1. International Federation of Palinological Societies, (IFPS)71.

Robbrecht, E. 1982 Pollen morphology of the tribes Anthospermeae and Paederieae (Rubiaceae) in relation to taxonomy. Bull. Jard. Bot. Nat. Belg. 52(3-4): 349–366.
DOI: 10.2307/3667888View Article Google Scholar

Schanzer, I.A., Elkordy, A.A.R. 2014 On the correlation of pollen grain size and ploidy levels of genus Galium sect. platygalium. RUDN Journal of Agronomy and Animal Industries 3: 5–17.
DOI: 10.22363/2312-797X-2014-3-5-17View Article Google Scholar

Son, D.C., Chang, K.S. 2019 Effective typification of Galium verum var. hallaensis, a replacement name for the Korean G. pusillum (Rubiaceae). Phytotaxa 423(5): 289–292.
DOI: 10.11646/phytotaxa.423.5.3View Article Google Scholar

Soza, V.L., Olmstead, R.G. 2010 Molecular systematics of tribe Rubieae (Rubiaceae): Evolution of major clades, development of leaf–like whorls, and biogeography. Taxon 59(3): 755–771.
DOI: 10.1002/tax.593008View Article Google Scholar

Tao, C., Ehrendorfer, F. 2011 28. Galium L., Sp. Pl. 1: 105. Flora of China 19: 104–141.

Vinckier, S., Huysmans, S., Smets, E. 2000 Morphology and ultrastructure of orbicules in the subfamily Ixoroideae (Rubiaceae). Rev. Palaeobot. Palynol. 108(3-4): 151–174.
DOI: 10.1016/S0034-6667(99)00036-6View Article Google Scholar

Wikstr?m, N., Kainulainen, K., Razafimandimbison, S.G., Smedmark, J.E., Bremer, B. 2015 A revised time tree of the asterids: establishing a temporal framework for evolutionary studies of the coffee family (Rubiaceae). PloS one 10(5): e0126690.
DOI: 10.1371/journal.pone.0126690View Article Google Scholar

Yang, L.E., Meng, Y., Peng, D.L., Nie, Z.L., Sun, H. 2018 Molecular phylogeny of Galium L. of the tribe Rubieae (Rubiaceae)–Emphasis on Chinese species and recognition of a new genus Pseudogalium. Mol. Phylogenetics Evol. 126: 221–232.
DOI: 10.1016/j.ympev.2018.04.004View Article Google Scholar