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Caryophyllaceae, Sagineae) and Related Genera

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Caryophyllaceae, Sagineae) and Related Genera Phytotaxa 394 (2): 148–160 ISSN 1179-3155 (print edition) https://www.mapress.com/j/pt/ PHYTOTAXA Copyright © 2019 Magnolia Press Article ISSN 1179-3163 (online edition) https://doi.org/10.11646/phytotaxa.394.2.3 Stem anatomy and its systematic implication in Bufonia (Caryophyllaceae, Sagineae) and related genera SABEREH MOUSAVI1, ATEFEH PIRANI2 & SHAHIN ZARRE1,* 1Center of Excellence in Phylogeny of Living Organism, School of Biology, College of Science, University of Tehran, P.O. Box 14155- 6455, Tehran, Iran; email: [email protected] 2Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, P.O. Box 91775-1436, Mashhad, Iran *Corresponding author Abstract Stem anatomy of Bufonia and nine allied genera was studied in order to investigate the systematic value of anatomical characters in generic delimitation. Cross-sections of stems of 31 accessions representing 14 species and 3 subspecies of Bufonia, and 17 additional species of the genera Arenaria, Cerastium, Eremogone, Minuartia, Minuartiella, Odontostemma, Sabulina, Sagina, and Shivparvatia were examined using light microscopy. The characteristic features of stem anatomy in Bufonia are: 1) presence of one to four layers of parenchyma in cortex, 2) calcium oxalate crystals mostly in the endodermis, 3) presence of inner and outer sclerenchymatous pericycle, and 4) a large central pith rupturing in a linear to boat-shape mode and forming a central continuous slit. Characters such as arrangement and continuity of xylem along with the number, and arrangement of different tissues (or layers) discriminate Bufonia from the other studied genera. Stem anatomy of Eremogone, Minuartia, and Bufonia showed some degree of similarity reflecting a level of convergence in the stem anatomy that might explain the taxonomic confusion associated with this group. The present study supports previous exclusion of Bufonia koelzii and B. caespitosa from Bufonia and their inclusion in Eremogone. Keywords: Eremogone, evolution, phylogeny, taxonomy Introduction Bufonia Linnaeus (1753: 123) [subfam. Alsinoideae Beilschmied (1833: 92) or subfam. Minuartioideae (Candolle, 1828: 379) Beilschmied (1833: 92) following Reveal (2007), tribe Alsineae Lamarck & Candolle (1806: 392)] includes ca. 30 annual or perennial herbaceous to small subshrubby species growing mostly on dry gravely slopes in mountainous regions (Bittrich 1993, Chrtek & Křísa 1999) and is distributed in the Mediterranean and the Irano-Turanian regions (see Bittrich 1993). The genera of Caryophyllaceae are under partial rearrangements and several genera need further study from both taxonomical and nomenclatural points of view (see e.g., Dillenberger & Kadereit 2014, Iamonico 2015, 2016a, 2016b, 2018, Iamonico & Domina 2015, Iamonico et al. 2015). A subfamilial classification of Caryophyllaceae is rejected by the molecular phylogenetic investigations and a tribal system is currently followed (Harbaugh et al. 2010, Greenberg & Donoghue 2011, Hernández-Ledesma et al. 2015). The molecular phylogenetic studies place Bufonia in tribe Sagineae (Harbaugh et al. 2010, Greenberg & Donoghue 2011, Hernández-Ledesma et al. 2015). The first taxonomic treatment of Bufonia was made by Boissier (1867) who divided the genus into two main unranked groups based on the number of stamens. He further classified one of these main groups into a few smaller ones using characters such as habit and the number of the ovules. Other main taxonomic studies of the genus covered taxa distributed in certain geographical regions, and no comprehensive monograph of the genus has been accomplished yet. Some of the important studies of Bufonia are made in regional floras such as Flora of Turkey and the East Aegean Islands (Davis 1965), Flora Iranica (Rechinger 1988), Flora Europaea (Tutin et al. 1993), and Flora of North Africa (Maire 1952). An infrageneric classification of Bufonia has not been carried out by these regional works, but a taxonomic investigation of the genus by Chrtek & Křísa (1999) classified 17 Asian species of Bufonia into seven sections. Although major efforts have been done to resolve the phylogeny of Caryophyllaceae, only four species of Bufonia have been included in previous molecular investigations depicting the genus as monophyletic (Fior et al. 2006, 148 Accepted by Duilio Iamonico: 23 Jan. 2019; published: 26 Feb. 2019 Harbaugh et al. 2010, Greenberg & Donoghue 2011). Therefore, the monophyly of the whole genus and its proposed sections have not been addressed sufficiently yet. Cerastium Linnaeus (1753: 437) and Sagina Linnaeus (1753: 128) have traditionally been considered as close relatives of Bufonia (Chrtek & Křísa 1999). However, molecular phylogenetic studies suggested Sabulina Reichenbach (1832: 24) and Sagina as the closest allies of Bufonia (Dillenberger & Kadereit 2014, Greenberg & Donoghue 2011). In addition, major morphological similarities between Bufonia and Eremogone Fenzl (1833: 13) species were reported by Sadegian et al. (2015). A taxonomic treatment of Bufonia revealed that B. koelzii Rechinger (1961: 44) should be reduced under the synonymy of Eremogone polycnemifolia Boissier (1843: 48) rendering close relationships between these genera (Chrtek & Křísa 1999). Moreover, B. caespitosa Haussknecht ex Bornmüller (1910: 22) was treated as a synonymy of Eremogone pseudacantholimon Bornmüller (1910: 22). Wood anatomy of the family Caryophyllaceae has been appreciated due to its potential importance in systematics at various taxonomic ranks, and provides informative data for understanding the reasons behind the habit changes in different ecosystems (see e.g., Carlquist 1995, Schweingruber 2007). Anatomical features of Caryophyllaceae were summarized by Metcalfe & Chalk (1950), while Carlquist (1995) investigated wood anatomy of 16 woody species of Caryophyllaceae, and showed their xeromorphic feature. Schweingruber (2007) studied the stem anatomy of 88 species of Caryophyllaceae, and indicated that members of the traditional subfamily Alsinoideae have a homogeneous stem anatomy where the libriform fibers, crystal druses and sclereids are absent in the cortex. Anatomical features of stem have been investigated within certain genera of the subfamily Alsinoideae, e.g., Minuartia Linnaeus (1753: 89) (Al- Saadi & Al-Taie 2014) and Stellaria Linnaeus (1753: 421) (Keshavarzi et al. 2014a), and subfamily Caryophylloideae, e.g., Silene Linnaeus (1753: 416) (Keshavarzi et al. 2014b), Acanthophyllum C.A.Meyer (1831: 210) (Mahmoudi Shamsabad et al. 2013) and Gypsophila Linnaeus (1753: 406) (Ataşlar & Ocak 2017). These studies suggested that anatomical features such as the outline of stem cross-section, and number of the sclerenchymatous cell layers surrounding the vascular cylinder can be used to discriminate closely related species. Stem anatomy and its potential application in delimitation of Bufonia from its related genera have not been investigated. In the present study, we perform a comparative study of stem anatomy in Bufonia and its nine related genera based on the recent molecular phylogenetic findings (Harbaugh et al. 2010; Greenberg & Donoghue 2011, Dillenberger & Kadereit 2014, Hernandez-Ledesma et al. 2015, Sadeghian et al. 2015), i.e., Arenaria, Cerastium, Eremogone, Minuarta, Minuartiella Dillenberger & Kadereit (2014: 84), Odontostemma Bentham ex Don (1831: 449), Shivparvatia Pusalkar & D.K.Singh (2015: 81), Sabulina, and Sagina. The aims of this study are: 1) to evaluate the usefulness of stem anatomy in generic delimitation of Bufonia, 2) to elucidate potential implication of anatomical characters in infrageneric classification of Bufonia, and 3) to find evidence supporting the suggestecd phylogenetic placement of taxa related to or assigned once to Bufonia. Material and methods Herbarium specimens of 17 taxa of Bufonia, representing 14 species and 3 subspecies from the whole distribution area of this genus (Table 1), four species of Eremogone, three species of each Minuartia and Sabulina, two species of Cerastium, one species of each genera Arenaria, Minuartiella, Odontostemma, Sagina, and Shivparvatia were used for stem anatomical studies. The voucher specimens (Table 2) of the sampled taxa are deposited at M, MSB and TUH (acronyms according to Thiers 2019+). Mature stems were removed from the studied specimens and fixed in alcohol/glycerin (1:1) in 55˚C for 16 hrs. The second and third lower internodes of the stems were used for sectioning. The cross-sections were made from the median part of the internodes using commercial razor blades by hand. The tissue ingredients were removed by 20% solution of Sodium Hypochlorite (NaClO) for 20 minutes. We used Safranin O (KGaA, Darmstadt, Germany) and Fast Green (KGaA, Darmstadt, Germany) to stain the cross-sections (Gerlach 1977). The cross-sections were maintained 30 minutes in Safranin and about 1 second in Fast Green. After each step the cross-sections were washed with distilled water and then they were dehydrated through ethanol and xylol (xylene) gradient, and finally fixed on the slides using Canada balsam. We used an Olympus VANOX AHBS3 light microscope to study the cross-sections. A total of 19 anatomical characters were studied on the cross-sections. The selected characters include (Fig. 1): the size of the long and short axis of the cross-sections (μm), the outline of the cross-section (elliptic to circular), thickness of epidermis (μm), thickness of parenchymatous cortex (number of layers), thickness of outer sclerenchymatous pericycle (μm), thickness
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