Acta Botanica 1-2015 - za web.indd ACTA BOT. CROAT. 74 (1), 2015 19 Acta Bot. Croat. 74 (1), 19–29, 2015 CODEN: ABCRA 25 ISSN 0365-0588 eISSN 1847-8476 Morphology and anatomy of Hedysarum pannosum (Boiss.) Boiss. (Fabaceae) HUSEYIN DURAL, BURCU YILMAZ CITAK* Selcuk University, Faculty of Science, Department of Biology, Kony a, Turkey Abstract – The aim of this paper is to investigate morphological, anatomical, palynological, fruit and seed micromorphological properties of Hedysarum pannosum (Boiss.) Boiss. A detailed description of the species is reported for the fi rst time in this study. The morpho- logical features of the species have been compared with the results of previous investiga- tions. Anatomical studies have been carried out on cross-sections of roots, stems, leafl ets and petioles. The anatomical results show that the plants have secondary growth roots, protruding stems, amphistomatic and equifacial leaves with tannin, triangular shaped peti- oles. Hedysarum pannosum pollen are tricolpate, prolate and pollen exine ornamentation is reticulate. Fruits have trichomes on their setae and tomentose trichomes have papillae. Seeds are reniform and they have rugolo-reticulate ornamentation. Keywords: anatomy, Fabaceae, fruit, Hedysarum, micromorphology, morphology, pollen, seed. Introduction Fabaceae, represented by 650 genera and 18000 species in the world, are a well-known family and have an economic value (POLHILL 1981). The genus Hedysarum, was established by LINNAEUS (1753). It belongs to the tribe Hedysareae of the family Fabaceae. The genus Hedysarum is represented by 154 species and the main origin of distribution of the genus is Central Asia. This genus has also an important distribution in the Anatolian-Iranian-Cauca- sian triangle. In Turkey, the genus Hedysarum is represented by 22 species (DAVIS 1970). Hedysarum pannosum was a synonym of Onobrychis pannosa (BOISSIER 1849). Later, PON- ERT (1973) reported H. pannosum as H. pogonocarpum Boiss. subsp. pannosum in Feddes Repertorium. However AKTOKLU (2012) determined Onobrychis pannosa and H. pogono- carpum subsp. pannosum as a synonym of H. pannosum. The genus Hedysarum is a legume plant which has photosynthetic metabolism and N2- fi xing ability. Accordingly, investigations about the genus Hedysarum are concentrated on photosynthetic metabolism and N2-fi xing but there are also studies based on various scien- * Corresponding author, e-mail: burcuyilmaz@selcuk.edu.tr Copyright® 2015 by Acta Botanica Croatica, the Faculty of Science, University of Zagreb. All rights reserved. DURAL H.,YILMAZ CITAK B. 20 ACTA BOT. CROAT. 74 (1), 2015 tifi c fi elds: molecular biology and karyology (ARSLAN and ERTUGRUL 2010, ARSLAN et al. 2012), palynology (CIVELEK et. al. 1999, PAVLOVA and MANOVA 2000, YILDIZ et al. 2009, GHANAVATI and AMIRABADIZADEH 2012) and nuclear DNA content (AKPINAR and YILDIZ 1999). However, anatomical and micromorphological studies are very limited (CIVELEK et al. 1999). Anatomical characters are not always as useful as morphological characters for plant identifi cations. However, they are well-established criteria and can offer signifi cant assistance in plant taxonomy (GUVENC and DUMAN 2010, RANJBAR et al. 2010, GUVENC et al. 2011). Furthermore, pollen exine ornamentation can also be used for plant taxonomy. The objectives of this investigation are to give a detailed account of the morphological, ana- tomical, pollen, fruit and seed micromorphological characteristics of H. pannosum and to evaluate their usefulness in the taxonomy of the genus. Material and methods The specimens of Hedysarum pannosum were collected from Konya, Obruk, Kızıltepe, low mountain steppe, 1250 m, 38°01’N 32°56’E, on 5th July 2011, and were deposited in KNYA herbarium (Dural-3500). Taxonomical description of the species was followed ac- cording to DAVIS (1970) and our observations. Anatomical investigations were performed using an average of 20 fresh specimens which were kept in FAA solution (5%, v/v formalin, 5%, v/v acetic acid, 50%, v/v ethanol). The paraffi n method was used for cross-sections. Sections were taken by a Thermo Scien- tifi c Shandon Finesse 325 Rotary microtome, stained with safranin-fast green and mounted with entellan. Only root cross-sections were taken with a razor blade and were stained with fl uoroglisin-HCl. Slides were observed by Leica DM 1000 light microscope. Measure- ments were made with Cameram 21 program and photos were taken with a Canon EOS 450D camera attached to the light microscope. For palynological investigations, pollen samples were obtained from herbarium materi- als. For light microscope investigations the pollen slides were prepared according to the WODEHOUSE technique (1935). Measurements and observations were made using a Leica DM 1000 light microscope with a Canon 450D camera and Cameram 21 program. The po- lar length (P), the equatorial length (E), the colpus length (CLG), the colpus width (CLT), thicknesses of exine and intine were examined for 30 pollen grains and P/E ratios were cal- culated. For scanning electron microscope investigations, unacetolyzed pollen grains were fi rst mounted on a double sided carbon tape affi xed to aluminum stubs, were covered with gold by a Cressington Auto 108 sputter coater and were photographed with ZEISS EVO LS10 SEM. Pollen terminology was followed according to PUNT et al. (2007). Size of fruits and seeds were screened with stereomicroscope and 30 mature fruits and seeds were measured. For SEM investigations, the mature fruits and seeds were placed on stubs directly and covered with gold and their diagnostic parts were photographed at sev- eral magnifi cations. Results Morphological characteristics Hedysarum pannosum is an erect and perennial plant, up to 65 cm, stems branched at the base, stems surface densely covered with pannose trichomes. Leaves are mostly basal THE MACRO AND MICROMORPHOLOGY OF HEDYSARUM PANNOSUM ACTA BOT. CROAT. 74 (1), 2015 21 with 4–10 pairs of ovate to elliptic or linear-lanceolate. Leafl ets have a pannose indumen- tum on both surfaces. The length of leafl et is 0.4–2 cm. Upper surface of leafl ets is greenish and more sparsely hairy than the lower surface, which is grayish-green. The apex of the leafl ets is acute. Petioles are 3–11 cm. Stipules are 4–5 mm, broad triangular, brownish, density and type of trichomes are the same as those of the stem. Peduncles are sturdy, 4–7 cm. Infl orescence is 9–16 cm, dense raceme. Bracts are c. 2–3 mm and bracteoles 2–2.25 mm. Calyx is 5–6 mm with subequal teeth ± same length and teeth are 2.5–3 mm. Corolla is yellow; standard size is 15–16 mm; wings are 8–9 mm; keel is 11–12 mm. Stamens are diadelphous, fi laments are 11–15 mm, anthers are approximately 1 mm length. Ovary is pilose. Lomentum has 1–2(–3) elliptic-ovate segments, 20–25 × 5–7 mm, fruit (juvenile) is pinkish-red setae, fruit (mature) is brownish-cream with densely 5–10 mm length setae. Anatomical characteristics Root anatomy Root anatomy shows that plants have a disintegrated periderm on the outermost layer as a protective tissue, which has 8–9 layers and is composed of disintegrating or squashed cells. Width of periderm cells is 81.16–128.59 μm (Tab. 1). Cortex, 7–8 layered, follows periderm towards to the center. There are sclerenchymatic cell groups in cortex and phloem (Fig. 1a). Phloem is well developed, phloem and xylem split up by 2–3 layered cambium. Vessels in xylem are irregular, according to METCALFE and CHALK (1957) classifi cation ves- sel grouping. The centre of roots in transverse sections was covered with xylem (Fig. 1b). Stem anatomy The shapes of the cross-sections of stem are oval but stem corners are protruding. It is evident on the transverse sections of stems that the one layered epidermis mainly consisted of rectangular, frequently arranged cells with a not thick cuticle (0.68–4.18 μm) (Tab. 1). The collenchyma is located below the epidermis; it has 6–7 layers at the corners of stem but it has 1–2 layers at the margins. The cortex which includes tannin is composed of 7–8 lay- ered oval parenchymatic cells and their dimensions are 4.5–18.4 × 7.6–30.3 μm (Fig. 2a, Tab. 1). Phloem and xylem are well developed. Above the phloem, sclerenchymatic cells are present. Diameters of the tracheas are 11.2–33.3 × 7.9–29.3 μm (Tab. 1). The pith re- gion of the stem consists of large parenchymatic cells and some of them include tannin (Fig. 2b). Leafl et anatomy The transverse sections of leafl ets show that the upper and lower epidermis are made up of oval, rectangular or isodiametric cells with adaxial and abaxial cuticles (adaxial cuticle thickness is 0.69–4.18 μm, abaxial cuticle thickness is 1.88–5.93 μm). Cells of the upper epidermis (8.63–50.45 μm wide × 6.75–22.74 μm long) are wider than those of the lower epidermis (5.70–42.68 μm wide × 5.0–16.6 μm long) (Tab. 1). The leafl et is amphistomatic and equifacial (Fig. 3a). The mesophyll thickness is 106.11–208.86 μm (Tab. 1). The pali- sade parenchyma is 1–3-layered above and 1–2-layered below the mesophyll. The spongy parenchyma cells which are 1–3-layered are present among the palisade parenchymatic cells with large intercellular spaces. Leafl ets of H. pannosum have hypodermis on the ab- axial side. Vascular bundles are collateral types (Fig. 3b). DURAL H.,YILMAZ CITAK B. 22 ACTA BOT. CROAT. 74 (1), 2015 Tab. 1. The anatomical characteristics of Hedysarum pannosum. Mean value ± standard deviation (SD), n = 20. Width (μm) Length (μm) Min–Max Mean ± SD Min–Max Mean ± SD Root Peridermis cell 81.16–128.59 105.0 ± 11.7 Parenchymatic cell 214.6–348.8 275.3 ± 49.9 Trachea cell 9.35–48.02 26.31 ± 8.74 Stem Cuticle Epidermis cell 0.68–4.18 5.9–25.9 2.35 ± 0.7 12.7 ± 3.9 7.5–17.1 12.2 ± 1.9 Cortex parenchyma cell 7.6–30.3 15.0 ± 5.0 4.5–18.4 12.8 ± 2.9 Trachea cell 7.9–29.3 18.3 ± 4.1 11.2–33.3 23.0 ± 4.3 Pith cell 16.03–79.70 39.3 ± 15.9 16.8–74.1 37.1 ± 14.1 Leafl et Adaxial cuticle 0.69–4.18 2.34 ± 0.7 Abaxial cuticle 1.88–5.93 3.48 ± 1.15 Adaxial epidermis 8.63–50.45 22.3 ± 8.2 6.75–22.74 12.51 ± 2.97 Abaxial epidermis 5.70–42.68 16.87 ± 7.80 5.0–16.6 9.8 ± 2.41 Mesophyll 106.11–208.86 161.39 ± 25.50 Palisade parenchyma 2.57–16.66 11.0 ± 2.8 11.66–77.31 44.3 ± 12.2 Spongy parenchyma 5.61–38.03 24.03 ± 6.85 Petiole Cuticle Adaxial epidermis 1.86–3.78 1.66–20.6 2.91 ± 0.52 7.7 ± 3.2 3.6–16.6 8.76 ± 2.0 Abaxial epidermis 2.7–18.0 8.23 ± 3.0 5.15–14.78 8.83 ± 1.9 Parenchymatic cell 22.9–95.4 55.7 ± 13.9 18.4–1020 58.1 ± 16.1 Trachea cell 4.8–29.88 19.71 ± 5.10 Fig. 1. The transverse sections of the root of H. pannosum: a) Pe – periderm, Sc – sclerenchyma, Co – cortex, X – xylem, Pi – pith region (scale bar = 250 μm); b) Ph – pholem, T – trachea, Ca – cambium (scale bar = 25 μm). THE MACRO AND MICROMORPHOLOGY OF HEDYSARUM PANNOSUM ACTA BOT. CROAT. 74 (1), 2015 23 Petiole anatomy The general view of petiole cross section is triangular especially in sections which have been taken from the midrib of the petiole. In petiole transverse sections, the epidermis is composed of one layer and epidermal cells of both surfaces are rectangular to oval and have trichomes (Fig. 4a). Cortex parenchymatic cells which are located under the epidermis are orbicular shaped and are composed of 8–9 layers. The dimensions of cortex cells are 18.4– Fig. 2. The transverse sections of the stem of H. pannosum: a) Eg – eglandular hair, Ep – epidermis, Co – cortex, X – xylem, Pi – p ith region (scale bar = 250 μm); b) Ta – tannin, Cu – cuticle, Sc – sclerenchyma, Ph – phloem, Cl – collenchyma (scale bar = 100 μm). Fig. 3. The transverse section of the leafl et of H. pannosum: a) Ue – upper epidermis, Pp – palisade parenchyma, Ta – tannin, Le – lower epidermis (scale bar = 100 μm); b) Sp – spongy paren- chyma, H – hypodermis, X – xylem, Ph – phloem, St – stomata (scale bar = 50 μm). Fig. 4. The transverse sections of petiole of H. pannosum: a) Ad – adaxial epidermis, Ab – abaxial epidermis, Co – cortex, X – xylem, Ph – phloem, Pi – pith region (scale bar = 250 μm); b) T – trachea, Ta – tannin, Sc – sclerenchyma (scale bar = 25 μm). DURAL H.,YILMAZ CITAK B. 24 ACTA BOT. CROAT. 74 (1), 2015 102 × 22.9–95.4 μm (Tab. 1). There are three large primary collateral vascular bundles in the corners of the petioles, with small secondary bundles among them. On the vascular bundles there is sclerenchyma shaped like an arc (Fig. 4a). The pith is composed of paren- chymatic cells which are orbicular shaped (Fig. 4b). Pollen characteristics The pollen grains of H. pannosum are tricolpate, prolate and isopolar. The shapes of pollen grains are elliptical in equatorial view (Fig. 5a) and orbicular in polar view (Fig. 5b). The dimensions of the polar axis (P) and equatorial axis (E) are 20.303–24.608 μm and 13.493–17.737 μm, respectively. The ratio of P/E is 1.350–1.792 μm. Colpus length is 15.072–21.275 μm and colpus width is 1.305–2.834 μm. Colpus membrane has large sculptural elements but some of them are fused especially in the middle of colpus (Fig. 5c). The exine thickness is 0.604–1.058 μm and the intine thickness is 0.447–0.84 μm. Exine ornamentation is reticulate in both of equatorial and polar view but pores in equatorial view are larger than those in polar view (Figs. 5d–e). Fruit and seed micromorphological characteristics Stereomicroscope investigations show that mature fruits (lomentum) of H. pannosum have 1–2(–3) segments, ovate, 20–25 × 5–7 mm, and its lomentum has setae. Lomentum surface is densely covered with tomentose trichomes. Juvenile fruit setae are pinkish-red, Fig. 5. SEM micrographs of the pollen of H. pannosum: a) equatorial view (scale bar = 2 μm); b) polar view (scale bar = 2 μm); c) colpus and colpus membrane view (scale bar = 2 μm); d) exine sculpturing in equatorial view (scale bar = 200 nm); e) exine sculpturing in polar view (scale bar = 200 nm) THE MACRO AND MICROMORPHOLOGY OF HEDYSARUM PANNOSUM ACTA BOT. CROAT. 74 (1), 2015 25 but mature fruits are brownish-cream and their length is 5–10 mm. The SEM investigations disclosed that both tomentose trichomes and setae are covered with papillae which are 1–2 μm long (Figs. 6a–b). Mature seeds are reniform (Fig. 6c), brownish-yellow, 6 × 4 mm, seed surface is rugolo-reticulate (Fig. 6d). Discussion The present study sought to provide useful information on the anatomy, pollen mor- phology, fruit and seed micromorphology of H. pannosum. This is the fi rst report on the examined characteristics of the species. The morphological results (e.g. leaves, bracts, stip- ules dimensions and corolla color) are mainly congruent with the description reported in Flora of Turkey (DAVIS 1970). However the dimensions of some characters of the plant such as stems, petioles and lomentum segments are seem to be variable than previously and measurements of some characters of H. pannosum are such as fi lament and anther length are presented here for the fi rst time (Tab. 2). Little work appears to have been done on the anatomy of vegetative organs of Hedy- sarum species (WATARI 1934, CIVELEK et al. 1999). In the root of H. pannosum periderm cells have 8–9 layers, but the root of H. aucheri comprises 14–15 layers (CIVELEK et al. 1999). H. pannosum cortex parenchyma and pith ray cells do not contain starch. However, the pith rays and cortex cells of H. aucheri do have starch in their parenchymatic cells. Also cambium cells of H. aucheri are composed of 3–4 layers (CIVELEK et al. 1999). However H. pannosum are composed of 2–3-layered rectangular cells. The number of layers of cambi- um, periderm and the presence/absence of starch in roots can appear to be a taxonomically signifi cant feature to distinguish the species. The transverse sections of stem of H. pannosum are made up of four main tissues from outside to inside and their names are epidermis, cortex, vascular bundles and pith region, respectively. We found that at the corners of stem of H. pannosum there are 6–7 layered Fig. 6. SEM micrographs of the fruit and seed of H. pannosum: a) the general view of fruits (scale bar = 1 mm); b) the setae of fruits (scale bar = 20 μm); c) the general view of seeds (scale bar = 200 μm); d) seed surface ornamentation (scale bar = 2 μm). DURAL H.,YILMAZ CITAK B. 26 ACTA BOT. CROAT. 74 (1), 2015 collenchyma. Although H. aucheri has 4–5 layered (CIVELEK et al. 1999). Vascular bundles of H. pannosum are collateral type and over them there are sclerenchymatic groups like an arc. Furthermore the pith cells of H. pannosum have tannin but there is no tannin in H. aucheri (CIVELEK et al. 1999). The number of layers of collenchyma at the corners of stem, the presence/absence of tannin in stem anatomy can be useful characters for distinguishing the species. Upper epidermis of H. pannosum is larger than lower epidermis in leafl et anatomy (Tab. 1). The leafl et of mesophyll of H. pannosum is equifacial that of H. aucheri is the same (CIVELEK et al. 1999). In leafl et anatomy of H. pannosum vascular bundles are of the col- Tab. 2. Comparison of morphological characters of Hedysarum pannosum based on the present study and ‘Flora of Turkey’ (DAVIS 1970). ‘Flora of Turkey’ Present study Stem Up to 30 cm Up to 65 cm Leaves 3–9 pairs ovate to elliptic on both surface pannose indumentum Ovate to elliptic on both surface pannose indumentum Leafl ets Not recorded 4–10 pairs of ovate to elliptic or ovate to linear-lanceolate. The biggest leafl et 0.4–2 cm. The both surfaces of leafl ets pannose. Upper surface of leafl ets is greenish and more sparsely hairy than lower surface, lower surface more hairy, grayish-green and leafl ets apex acute. Petiole Not recorded 3–11 cm Stipules c. 3 mm 4–5 mm Peduncles Sturdy, much longer than leaves 4–7 cm Infl orescence Not recorded 9–16 cm, dense racem Bracts and bracteoles Not recorded Bracts c. 2–3 mm; bracteoles c. 2–2.25 mm Calyx Calyx 4–5 mm with subequal teeth ± same length as tube Calyx c. 5–6 mm, teeth approximately the same length and teeth c. 2.5–3 mm length Corolla Corolla yellow; standard 10–14 mm; wings 7–9 mm; keel 10–15 mm Corolla yellow; standard 15–16 mm; wings 8–9 mm; keel 11–12 mm Filaments Not recorded Stamens diadelphous, fi laments 11–15 mm Anthers Not recorded c. 1 mm Ovary Ovary glabrous or slightly pilose Ovary pilose Fruits (lomentum) Lomentum with 1–2 ovate-orbicular segments, c. 8 × 8 mm, pubescent and densely covered with setae up to 5 mm long Lomentum with 1–2(–3) segments, 20–25 × 5–7 mm, ovate, when fruit is juvenile pinkish-red and is mature brownish-cream with densely 5–10 mm length setae THE MACRO AND MICROMORPHOLOGY OF HEDYSARUM PANNOSUM ACTA BOT. CROAT. 74 (1), 2015 27 lateral type and among the upper palisade parenchymatic cells there are cylindrical tannin cells in lysigenous secretory cells. Also tannins are present between abaxially palisade pa- renchyma in H. pannosum. CIVELEK et al. (1999) observed tannin in H. aucheri leafl ets. WATARI (1934) emphasized that ‘the petiolar base is one of the most important regions in the vascular course of foliar organs of Leguminosae.’ He classifi ed branching patterns of the vascular bundles at the petiolar bases into three types based on the number leaf traces and whether they are fused or free. In the present study leaf traces of H. pannosum are free. In petiole anatomy of H. pannosum there are three main median vascular bundles and also small secondary ones and they involve tannin. The shapes of petioles of H. pannosum show similarities with those of H. micropterum and H. falconeri (CHOI et al. 1999). METCALFE and CHALK (1957) pointed out that the stomata of Fabaceae is of the anizositic type and that those of H. pannosum and also H. aucheri (CIVELEK et al. 1999) are the same. The results of our investigation show that pollen morphology of H. pannosum is com- paratively homogenous and confi rms the general description presented by OHASHI (1971), FERGUSON and SKVARLA (1981), FAEGRI and IVERSEN (1989), MOORE et al. (1991), CHOI and OHASHI (1996), CIVELEK et. al. (1999), PAVLOVA and MANOVA (2000), and GHANAVATI and AMIRABADIZADEH (2012). H. pannosum pollen are tricolpate, prolate, circular in polar view and elliptical-elongated in equatorial view and ornamentation reticulate. While H. tauric- um, H. grandifl orum and H. aucheri pollen grains are prolate, triangular-obtuse in polar view, elongated, rectangular-obtuse to elliptic in equatorial view and their ornamentation is fi nely reticulate (CIVELEK et al. 1999, PAVLOVA and MANOVA 2000). The pollen grains of H. pannosum colpus membranes have large sculptural elements but some of them are united especially in the middle of the colpus. PAVLOVA and MANOVA (2000) declared that H. tauri- cum and H. grandifl orum colpus membrane was covered by differently sized sculptural ele- ments. Also GHANAVATI and AMIRABADIZADEH (2012) explained that H. kopetdaghi and H. damghanicum colpus membranes were covered by large and small sculptural elements. There has been no investigation about the fruit micromorphology of Hedysarum genus. In this study, the fruit micromorphology of H. pannosum is presented for the fi rst time. The fruits of the H. pannosum lomentum are oval shaped and have setae. The SEM investiga- tions show that on tomentose trichomes of lomentum and setae there are papillae 1–2 μm in diameter. The investigation of the fruits of Hedysarum genus will be a guide for future dis- cussions. The seeds of H. pannosum are reniform, hilum small and the seed surface is rugolo-re- ticulate. The surface of seed coat sculpture is arranged irregularly (Fig. 6d). SA (2007) showed that the seeds of H. jaxartucirdes were reniform, hilum small at upper part of seed and seed coat sculpture mainly cerebelloid, highly irregular, cell wall is sinuate and without ornamentation. Also the seeds of H. gmelinii, H. dahuricum and H. setigerum were reni- form, and their hilum region is grooved; the seed coat sculpture was irregular, the seed sur- face ornamentation was reticulate. Moreover H. brachypterum and H. dasycarpum seeds ornamentation were reticulate and seed coat cells were highly irregular. But H. splendens seeds coats were relatively smooth (SA et al. 2010). H. aucheri seeds were reniform and seed surface ornamentation was smooth (CIVELEK et al. 1999). Hence these features of seed surface micromorphology can suggest taxonomical diagnostic characters for distinguishing species. DURAL H.,YILMAZ CITAK B. 28 ACTA BOT. CROAT. 74 (1), 2015 Anatomical, palynological and micromorphological (pollen, fruit and seed) characteris- tics might be useful in the defi nition of the species investigated. Nevertheless, these charac- teristics will be more valuable if other species of Hedysarum are also examined. Acknowledgements We wish to thank Selcuk University Scientifi c Research Unit for fi nancial support (Proj- ect No: 11401072). References AKPINAR, N., YILDIZ, B., 1999: Nuclear DNA contents of some endemic Hedysarum L. Spe- cies. Turkish Journal of Botany 23, 229–232. AKTOKLU, E., 2012: Hedysarum. In: GÜNER, A., ASLAN, S., EKIM, T., VURAL, M., BABAÇ, M. T. (eds.), A checklist of fl ora of Turkey (vascular plants). Nezahat Gökyiğit Botanic Garden and Publication of Flora Researches Association, Istanbul. ARSLAN, E., ERTUGRUL, K., 2010: Genetic relationships of the genera Onobrychis, Hedysa- rum, and Sartoria using seed storage proteins. Turkish Journal of Biology 34, 67–73. ARSLAN, E., ERTUGRUL, K., TUGAY, O., DURAL, H., 2012: Karyological studies of the genus Onobrychis Mill. and the related genera Hedysarum L. and Sartoria Boiss. & Heldr. (Fabaceae, Hedysareae) from Turkey. Caryologia: International Journal of Cytology, Cytosystematics and Cytogenetics 65, 11–17. BOISSIER, P. E., 1849: Diagn. Pl. Orient., 1(9). Typis Marci Ducloux et Cons., Paris. CHOI, B. H., OHASHI, H., 1996: Pollen morphology and taxonomy of Hedysarum and its re- lated genera of the tribe Hedysareae (Leguminosae-Papilionaceae). Journal of Japanese Botany 71, 191–213. CHOI, B. H., NEMOTO, T., OHASHI, H., 1999: Anatomy of nodal regions and leaves in Hedys- arum L. and related genera (Leguminosae). Journal of Japanese Botany 74, 236–250. CIVELEK, S., YAMAN, A., SAHIN, A., GUR, N., 1999: The investigation in point of chromo- some number, morphological, anatomical and pollen characteristics of Hedysarum aucheri Boiss. Journal of Science and Engineering of Fırat University 11, 77–88. DAVIS, P. H. (ed.), 1970: Flora of Turkey and the East Aegean Islands. Vol. 3–10, Univ. Press, Edinburg. FAEGRI, K., IVERSEN, J., 1989: Textbook of pollen analysis. John Wiley & Sons, Chichester. FERGUSON, K., SKVARLA, J., 1981: The pollen morphology of the subfamily Papilionoideae (Leguminosae). In: POLHILL, R., RAVEN, P. (eds.), Advances in legume systematics, Part 2, 859–896. Royal Botanic Gardens, Kew. GHANAVATI, F., AMIRABADIZADEH, H., 2012: Pollen grain morphology in Iranian Hedysareae (Fabaceae). Crop Breeding Journal 2, 25–33. GUVENC, A., DUMAN, H., 2010: Morphological and anatomical studies of annual species of Sideritis L. (Lamiaceae), with notes on chorology in Turkey. Turkish Journal of Botany 34, 83–104. GUVENC, A, HURKUL, M. M., ERDEM, A., 2011: The leaf anatomy of naturally distributed Ju- niperus L. (Cupressaceae) species in Turkey. Turkish Journal of Botany 35, 251–260. THE MACRO AND MICROMORPHOLOGY OF HEDYSARUM PANNOSUM ACTA BOT. CROAT. 74 (1), 2015 29 LINNAEUS, C., 1753: Species Plantarum. pp 745–756. METCALFE, C. R., CHALK, L., 1957: Anatomy of the Dicotyledons I. Clarendon Press, Ox- ford 504–516. MOORE, P., WEBB, J., COLLINSON, M., 1991: Pollen analysis (2 ed.). Blackwell Sci. Publ. Oxford. OHASHI, H., 1971: A taxonomic study of the tribe Coronilleae (Leguminosae) with special reference to pollen morphology. Journal of the Faculty of Science, University of Tokyo, Section III Botany 11, 25–92. PAVLOVA, D. K., MANOVA, V. I., 2000: Pollen morphology of the genera Onbrychis and He- dysarum (Hedysareae, Fabaceae) in Bulgaria. Annales Botanici Fennici 37, 207–217. POLHILL, R. M., 1981: Papilionoideae. In: POLHILL, R. M., RAVEN, P. H. (eds.), Advances in legume systematics, part 1, 367–370. Kew: Royal Botanic Gardens. PONERT, J., 1973: Neue taxonomische Kombinationen, Kategorien und Taxa vor allem der türkischen Arten. Feddes Repertorium 83, 621. PUNT, W., HOEN, P. P., BLACKMORE, S., NILSSON, S., LE THOMAS, A., 2007: Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology 143, 1–81. RANJBAR, M., HAJMORADI, Z., KARAMIAN, R., 2010: The taxonomic importance of leaf epi- dermis morphology and peduncle anatomy in Trigonella disperma Bornm. ex. Vassilcz. Taxonomy and Biosystematics 1, 15–26. SA, R., 2007: Hedysarum jaxartucirdes (Fabaceae), a new species from Xinjiang. China. Annales Botanici Fennici 44, 157–159. SA, R., SU, D., DEBRECZY, Z., 2010: Taxonomic notes on the Hedysarum gmelinii complex (Fabaceae). Annales Botanici Fennici 47, 51–58. YILDIZ, K., GUCEL, S., DADANDI, M. Y., 2009: A palynological investigation of endemic taxa from Northern Cyprus. Pakistan Journal of Botany 4, 991–1007. WATARI, S., 1934: Anatomical studies on some leguminous leaves with special reference to the vascular system in petioles and rachises. Journal of the Faculty of Science, Univer- sity of Tokyo, Section III Botany 4, 225–365. WODEHOUSE, R. P., 1935: Pollen Grains, McGraw-Hill Book Company Inc. New York and London.