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Pollen Morphology and Anatomical Features of Lilium (Liliaceae) Taxa from Turkey

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Pollen Morphology and Anatomical Features of Lilium (Liliaceae) Taxa from Turkey Biologia 69/9: 1122—1133, 2014 Section Botany DOI: 10.2478/s11756-014-0416-2 Pollen morphology and anatomical features of Lilium (Liliaceae) taxa from Turkey Seher Guven¨ 1,SedaOkur1*, Mine Sezen Dem˙irel2,KamilCoskuncelebi2, Serdar Makbul1 &OsmanBeyazoglu˘ 3 1Department of Biology, Faculty of Sciences and Arts, Recep Tayyip Erdo˘gan University, Rize, Turkey, [email protected] 2Department of Biology, Science Faculty, Karadeniz Technical Universty, Trabzon, Turkey 3Department of Biomedical Engineering, Faculty of Engineering and Architecture, Yeni Y¨uzyıl University, Istanbul,˙ Turkey Abstract: In this study, pollen grains and anatomical features of Turkish lilies were investigated under the electron (SEM) and light (LM) microscope. LM and SEM observations showed that the pollen grains are monosulcate, heteropolar, elliptical in polar view and oblate. Numerical results based on combined palynological and anatomical characters were discussed and compared with traditional taxonomic treatments. It was found that the midrib shape, mesophyll type, P/E (polar/equatorial), sulcus length, and lumina width are the most valuable traits in separating the examined taxa. The numerical analysis showed that Lilium candidum L. differs from the rest Turkish Lilium and also confirmed a close relationship between L. szovitsianum Fisch. & Avé-Lall. and L. armenum Miscz. ex Grossh. Also this study is the first report dealing with anatomical and palynological features of all Turkish lilies. Key words: Lilium; anatomy; pollen; systematics; Turkey Introduction tion of different genera (Troia et al. 2012; Ceter et al. 2013) and also closely related Liliaceae taxa (Tek¸sen et The genus Lilium L. (Liliaceae) includes about 100 al. 2010; Kameshwari 2011; Masoumi 2012). Addition- species distributed throughout the cold and temperate ally, palynological studies showed that several features regions of Northen Hemisphere (McRae 1998). Most of (Kosenko 1999; Muratovi´cet al. 2010a; Pupuleku et al. the Lilium species consisting of fragrant, bulbous and 2010) and carbohydrate content of pollens in the genus perennial herbs, form an important group of flowering Lilium (Clement & Audran 1995) provide important in- garden plants. The long-standing popularity of Lilium formation, but to our knowledge there are no records as ornamental plants is due to their large, showy flowers on pollen morphology and contents of lilies distribution that often have a strong fragrance (Woodcock & Stearn in Turkey. Similarly, as stated by Kim & Lee (1990), 1950). Kaviani et al. (2008), Dhyani et al. (2009) and Mura- Recently, many taxonomic viewpoints regarding tovi´c et al. (2010a), the features related to stem and the members and infrageneric classification of genus Lil- leaf anatomy have considerable taxonomic value in the ium have been put forward. Traditionally, it has been systematic of Lilium. The first taxonomic treatment of subdivided into 5–11 sections (Endlicher 1840; Baker Turkish Lilium was made by Davis & Henderson (1984), 1871; Wilson 1925; Baranova 1988) based on the mor- who recognized four species and four varieties. Since phological characters such as flower shape and position. then, L. akkusianum R. G¨amperle has been recorded as But a more detailed and acceptable classification was a new species from Turkey (G¨amperle 1998). Recently proposed by Comber (1949) with seven sections based the most comprehensive phylogenetic study on Turk- on combination of 13 morphological characteristics and ish lilies based on phenetic and molecular data pub- two germination types. The infrageneric treatment of lished (Ikinci˙ 2005). The recent study reveals, genus Comber (1949) has been supported by some molecular Lilium is represented by 7 species and 8 taxa in Turkey studies of Nishikawa et al. (2001), Ikinci (2005, 2011), (Ikinci˙ 2012). Inceer et al. (2002) and Coskuncelebi Ikinci et al. (2006), Rønsted et al. (2005), Resetnik et et al. (2005) reported the caryological properties of al. (2007), Muratovic et al. (2010b), Lee et al. (2011) some lily taxa (L. candidum, L. martagon L., L. pon- and Gao et al. (2012). ticum K. Koch (= L. carniolicum subsp. ponticum It is well known that pollen features have a great (C.Koch) Davis & Henderson), L. ciliatum P.H. Davis) taxonomic value, and have been used in the classifica- distributed in Turkey. Additionally, some anatomical * Corresponding author c 2014 Institute of Botany, Slovak Academy of SciencesUnauthenticated Download Date | 11/24/15 3:00 PM Pollen morphology and anatomical features of Lilium taxa from Turkey 1123 Fig. 1. Distribution map of the examined taxa. Table 1. Locality information of Turkish lilies. No Taxon Locality Altitude (m) Collection numbers 1 Lilium candidum L. Mu˘gla, Fethiye-Dalaman eski yolu, G¨o¸cek Ge¸cidi 298 Makbul 203 2 Lilium martagon L. Kastamonu-K¨ure-Akdivan k¨oy¨u 1990 Makbul 164 3 Lilium ponticum K. Koch Trabzon-C¸ aykara-Kabata¸sk¨oy¨u 1250 Makbul 161 4 Lilium ciliatum P. H. Davis Trabzon-Ma¸cka-Hamsik¨oyust¨ ¨ u 1400 Makbul 152 5 Lilium szovitsianum Fisch. & Avé-Lall. Artvin, Karabel-Ercan kayalı˘gıustleri, ¨ Aksaz G¨ol¨u 1912 Makbul 163 6 Lilium armenum Miscz. ex Grossh. Trabzon-Zigana Da˘gı-G¨um¨u¸shane b¨ol¨um¨u 1643 Makbul 154 7 Lilium kesselringianum Miscz. Artvin-Bor¸cka-Karag¨ol ¨ustleri 1848 Makbul 162 8 Lilium akkusianum R. G¨amperle Ordu, Akku¸s-G¨ok¸cebayır arası 1200 Makbul 208 features of L. ciliatum (Coskuncelebi & Beyazoglu 1999; from permanent slides. All measurements and observations Ozdemir¨ 2003), L. ponticum (= L. carniolicum Bernh. were performed on 5 species for each population. ex W.Koch var. artvinense (Miscz.) Davis & Hender- son) (Akta¸s et al. 2009) and L. candidum (Ozen¨ et Palynological studies al. 2012) have been recorded from Turkey. These all Polleniferous materials were removed from living specimens preliminary studies do not provide detailed anatomical in the field. The pollen grains were prepared for light mi- croscope (LM) by standard methods described by Erdtman information for all Turkish Lilium species. Thus, the (1952). All measurements were based on at least 30 pollen present study aims; (1) to explore the anatomical and grains per taxa. After pollen grains were coated with a thin palynological properties and (2) contribute systematic layer of gold for 3 min with a Poloron SC502 Sputter Coater, position of eight Lilium taxa from Turkey. they were examined and photographed with a JEOL-JSM 5600 scanning electron microscopy (SEM) at The Scientific and Technical Research Laboratories of Kırıkkale Univer- Material and methods sity (Turkey). Pollen terminology mainly follows Punt et al. (2007). Specimens Both polleniferous and anatomical materials (stem and leaf) Numerical analysis were collected from the natural habitats in Turkey during Two types of multivariate analyses were performed by Syn- 2009 and 2010 (Fig. 1). The collection data for the exam- Tax PC 5.0 (Podani 1993): Cluster analysis (CA) and princi- ined taxa are given in Table 1. The voucher specimens were pal components analysis (PCA). For CA (UPGMA), a pair- stored in the Herbarium of Recep Tayyip Erdo˘gan Univer- wise matrix of resemblance values was calculated from raw sity, Department of Biology (RUB). standardized data matrix, using Gower’s coefficient of re- semblance designed for mixed data sets (Sneath & Sokal Anatomical studies 1973). A dendrogram was generated by the unweighted The anatomical materials were fixed in FAA (formalde- pair-group method by using arithmetic averages (UPGMA). hyde : acetic acid : alcohol) for 24 h and then preserved in Also, cophenetic correlation coefficient (rcs) was calculated ethanol (70%). Cross section of stem and leaf were taken (Sneath & Sokal 1973). For PCA, firstly the raw data were with the microtome of Shandon Cryotome SME at 25– used to create a correlation matrix and then two eigenvec- 30 µm thickness. Surface sections of the leaves were cut by tors (a set of coordinates) wereextractedbyEigenanalysis free hand. All sections except for surface ones were stained from this correlation matrix. Two coordinates (axes) were with hematoxylen for 30 minutes and mounted with aqua projected to give a two-dimensional plot of the taxa and witrexia in order to obtain permanent slides (Vardar 1987). the characters. Thirteen anatomical and eleven palynolog- The sections were photographed with an Olympus BX51 ical characters were assessed by numerical analysis: Three Unauthenticated Download Date | 11/24/15 3:00 PM 1124 S. Guven¨ et al. Table 2. Anatomical and palynological characters used in numerical analysis. Symbol Characters X1 Width/length of epidermal cells of stem (µm/µm) X2 Width/length of collenchyma cells of stem (µm/µm) X3 Width of cortex tissue / Width of scleranchymatic tissue (µm/µm) X4 Width of phloem / Width of xylem (µm/µm) X5 Plant; glabrous or simple hairy:0, strigose hairy:1 X6 Midrib; triangular-shaped or semicircular:0, circular:1 X7 Mesophyll; unifasial:0, bifasial:1 X8 Width of mesophyll (µm) X9 Width/length of lower epidermal cells of leaf (µm/µm) X10 Width/length of lower stomata (µm/µm) X11 Stomata index of lower epidermis X12 Width/length of upper epidermal cells of leaf (µm/µm) 2 X13 Average number of upper epidermal cells of leaf (mm ) X14 Polar axis (P) (µm) X15 Equatorial axis (E) (µm) X16 P/E rate X17 Muri (µm) X18 Lumina (µm) X19 Sulcus length (Slg) (µm) X20 Sulcus width (Slt) (µm) X21 Length/width of sulcus (Slg/Slt) (µm/µm) X22 Exine (µm) X23 Sexine (µm) X24 Nexine (µm) characters were nominally scored as 0 or 1 and the remain- arm-shaped palisade cells and 6–7 layers of isodiametric ing twenty one characters were quantitative including linear spongy parenchymatic cells, there is homogenous meso- measurements and numbers (Table 2). All anatomical and phyll in the unifacial leaves. All leaves are hypostomatic palynological measurements used in the numerical analysis leaves with anomocytic stomata. are given in the Appendix as a raw data matrix. Palynological results Results The color of the pollen grains of the examined taxa were determined from the polleniferous materials collected in Anatomical results the field, however it was not used in numerical analysis The general anatomical properties of stem and leaves in the present study.
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