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Molecular Phylogeny of Artemisia (Asteraceae-Anthemideae)

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Molecular Phylogeny of Artemisia (Asteraceae-Anthemideae) Plant Ecology and Evolution 152 (3): 507–520, 2019 https://doi.org/10.5091/plecevo.2019.1583 REGULAR PAPER Molecular phylogeny of Artemisia (Asteraceae-Anthemideae) with emphasis on undescribed taxa from Gilgit-Baltistan (Pakistan) based on nrDNA (ITS and ETS) and cpDNA (psbA-trnH) sequences Adil Hussain1,*, Daniel Potter2, Sangtae Kim3, Muhammad Q. Hayat4 & Syed A.I. Bokhari1 1Department of Biological Sciences, International Islamic University Islamabad, 44000 Pakistan 2Department of Plant Sciences, College of Agricultural and Environmental Sciences, University of California Davis, 95616 USA 3School of Biological Sciences and Chemistry, Sungshin Women’s University, Korea 4Department of Plant Biotechnology, Atta-ur-Rahman School of Applied Biosciences, National University of Sciences and Technology Islamabad, 44000 Pakistan *Corresponding author: [email protected] Background – Gilgit-Baltistan, the Northeast region of Pakistan, is well known for its floristic diversity, including members of the genus Artemisia. Artemisia is a large, taxonomically complex genus including ~500 species of both herbs and shrubs. This study was conducted to determine the phylogenetic position of ten undescribed Artemisia taxa from northern Pakistan, using nrDNA internal transcribed spacer (ITS), external transcribed spacer (ETS) and cpDNA intergenic spacer (psbA-trnH) regions. Methods – The phylogenetic relationships of 28 taxa of Artemisia using separate and combined data sets of sequences of three markers (ITS, ETS and psbA-trnH) were analysed with maximum parsimony, maximum likelihood, and Bayesian approaches. Key results – The results resolve northeastern Pakistani Artemisia, which represent five morphologically defined subgenera, into ten major clades. Subgenera Artemisia and Absinthium are shown to be polyphyletic, while Dracunculus, Pacifica and Tridentatae appear monophyletic. All species of subgenus Seriphidium are retrieved in a single clade that also includes annual species from subgenus Artemisia. In the Flora of Pakistan, Seriphidium is described as a separate genus but in this study, Seriphidium fell within the genus Artemisia. In addition, on the basis of phylogenetic analysis, we present evidence that ten as-yet undescribed taxa are present in northeastern Pakistan based on newly recognized three groups (Groups I, II and III) of taxa within the genus Artemisia. One undescribed taxon from group I was placed within the subgenus Dracunculus clade and the remaining nine taxa from groups II and III were placed in the subgenus Absinthium clade. Morphological studies coupled with modern molecular techniques may lead to a new infrageneric classification of the genusArtemisia. It will also clarify and characterize the undescribed taxa reported in this study. Keywords – Artemisia; Asteraceae; nrDNA; cpDNA; molecular phylogeny; undescribed taxa; Gilgit- Baltistan; Pakistan. INTRODUCTION species of both herbs and shrubs (Martin et al. 2003). Several species from this genus have a noteworthy economic status The genus Artemisia (family Asteraceae; tribe Anthemideae) because they exhibit antispasmodic, antiseptic, antitumor is a large taxonomically challenging group that includes ~500 antimicrobial, antimalarial, antirheumatic and hepato-protec- © 2019 The Authors. This article is published and distributed in Open Access under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original work (author and source) is properly cited. Plant Ecology and Evolution is published by Meise Botanic Garden and Royal Botanical Society of Belgium ISSN: 2032-3913 (print) – 2032-3921 (online) Pl. Ecol. Evol. 152 (3), 2019 tive properties (Terra et al. 2007; Hussain et al. 2017). The as a subgenus of Artemisia. Mahmood et al. (2011) carried genus is distributed primarily in the northern hemisphere’s out a molecular phylogenetic study of Artemisia species col- temperate zones; a few Artemisia species are also found in lected from different localities of Pakistan based on restric- the southern hemisphere (Oberprieler et al. 2009). The centre tion fragment length polymorphism of the chloroplast rps11 of diversity for Artemisia is Central Asia. The earliest micro- gene. They provided evidence that hybridization occurred at fossils of the genus are known from the Miocene radiation an infrageneric level during the evolutionary process, due to (Wang 2004) and the Eocene end (Zaklinskaja 1957). which the natural classification of the genus is still a chal- Since many years, the infrageneric classification of Ar- lenging problem. temisia has offered a challenge for researchers dealing with Here, we determine the phylogenetic position of ten unde- taxonomy. These historical studies were well acknowledged scribed Artemisia taxa from northern Pakistan, using nrDNA in the previous revelations of Torrell et al. (1999) and Vallès internal transcribed spacer (ITS), external transcribed spacer & McArthur (2001). From the studies of Tournefort (1700) (ETS) and cpDNA intergenic spacer (psbA-trnH) regions. to Bremer (1994) and Ghafoor (2002), all investigations re- garding the classification and taxonomy of Artemisia were MATERIALS AND METHODS based on capitulum morphology. They documented four subgenera in the genus Artemisia (s. lat.) i.e. Artemisia, Ab- Study area sinthium, Seriphidium and Dracunculus as shown in table 1. During the course of this period, the position of Seriphidium Gilgit-Baltistan is a northeastern region of Pakistan situated between 74°–77.5°E and 34.6°–37.4°N, covering an area of as a separate genus or a subgenus of Artemisia (s. lat.) per- 2 sisted and was a subject of discussion among taxonomists. about 45 224 km . The altitude of this region ranges from For example, the generic recognition was implemented by ±1400 m to 8611 m. The area is divided into seven main Ling (1982), Bremer & Humphries (1993), Bremer (1994), districts, i.e. Gilgit, Skardu, Hunza-Nagar, Astore, Diamer, Ling (1995) and Ghafoor (2002), whereas subgeneric status Ghizer and Ghanche. This region includes world-renowned was followed by Kornkven et al. (1998, 1999), Torell et al. mountain ranges like the Karakorum, Hindu Kush and the (1999), Watson et al. (2002) and D’Andrea et al. (2003). Himalayas. There are several peaks with heights above 7000 m, including Godwin Austin (K-2, 8611 m), Rakaposhi Kornkven et al. (1998) provided a pioneering molecular (7788 m) and Deran peak (7268 m). The world’s largest phylogenetic study of Artemisia based on nrDNA internally glaciers are also found in this region, such as Baltoro Gla- transcribed spacer (ITS) with the aim of resolving its inter- cier, which extends for about 62 km with an area of 529 km2 specific associations. In their study, they supported the North (Anonymous 2003). This area is well known for a great di- American origin of Tridentatae. They concluded that Triden- versity of plants (Shinwari 2010) and is a centre for tradi- tatae could be restricted as a monophyletic group with the tional medicinal herbs (Shinwari & Gilani 2003). omission of A. palmeri A.Gray and A. bigelovii A.Gray. Sub- sequently, Torrell et al. (1999) revealed the phylogeny of ge- nus based on ITS sequences, in which they found support for Plant collection and sampling five subgenera of Artemisia: Artemisia, Seriphidium, Absin- The plant samples employed for molecular phylogenetic thium, Dracunculus and Tridentatae. These results were ad- analysis were taken from both herbarium specimens and sil- ditionally confirmed by Watson et al. (2002) and followed by ica gel dried samples collected during expeditions to various numerous other molecular phylogenetic revisions. The de- parts of Gilgit-Baltistan region of Pakistan as already given tailed history of molecular phylogenetic efforts on the genus in our preceding paper (Hussain et al. 2019). Provenance of is provided in table 2. These works here surveyed proposed the different populations of Artemisia studied from Northern numerous taxonomic reorganizations for the subgeneric clas- Pakistan, with their collection details are listed in table 3. sification based on molecular data and related the latter’s Thus, covering all the Northeastern Pakistani endemic Arte- outcomes with the traditional morphology-based classifica- misia taxa representing five subgenera of the genus Artemi- tions (table 1). However, the infrageneric classification has sia, including Artemisia, Absinthium, Dracunculus, Pacifica not yet been entirely fixed. This is because of the inconsist- and Seriphidium, were included, except the North American ent assignments of some taxa during phylogenetic examina- endemic A. tridentata Nutt. of which we could not get the tions with respect to the classification based on morphology. material. In the flora of Pakistan, Ghafoor (2002) treatedArtemisia Voucher specimens were deposited in the herbarium of (s. lat.) by two separate genera, Artemisia, with 25 species, Pakistan Museum of Natural History (PMNH) and the de- and Seriphidium, with 13 species. All these 38 species are tails are given in table 3. Earlier published ITS (Internal tran- recorded from the arid and semi-arid areas of Baluchistan, scribed spacer), ETS (External transcribed spacer) of nrDNA Khyber Pakhtunkhwa, North Punjab and the temperate areas and psbA-trnH (Intergenic spacer) of cpDNA sequences rep- of Gilgit-Baltistan and Kashmir territory (Ghafoor 2002). resenting all subgenera of the genus Artemisia were retrieved Within Pakistan, the
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