Revista Brasileira de Farmacognosia 27 (2017) 143–152
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Original Article
Pharmacobotanical study of Hypericum thymopsis
Mehmet Tekin
Department of Pharmaceutical Botany, Faculty of Pharmacy, Cumhuriyet University, Sivas, Turkey
a b s t r a c t
a r t i c l e i n f o
Article history: Hypericum thymopsis Boiss., Hypericaceae, is an endemic herb which generally grows at the calcareous
Received 16 June 2016
steppe regions of Central Turkey. In flowering stage, the aerial parts of this species are used for wound-
Accepted 19 September 2016
healing and sedation, and its infusions are used against stomach diseases and throat infections by local
Available online 21 October 2016
people. The aim of this study, to examine and to reveal of the morphology, anatomy and histology of
the aerial vegetative and reproductive organs of the H. thymopsis, which are used in popular medicine
Keywords:
and thus contributing to the pharmacognostic evaluation of the species. In comparison with previous
Anatomy
published morphological description of the species, some different findings about plant height and leaf
Clusiaceae
length were found. In addition, some morphological characteristics such as dimensions of sepals and
Hypericum thymopsis
ovaries, length of filaments, anthers, pistils and pedicels were examined here for the first time. The
Medicinal plant
Morphology anatomical characteristics of stem, leaf, sepal, filament and pistil were studied using light microscopy
Turkey and additionally for stem and leaf using scanning electron microscopy. The stem has the secondary
growth, and circular shape. The leaves are amphistomatic and the mesophyll is dorsiventral. Stomata are
anisocytic and sunken. The glandiferous emergences are present on stem and translucent glands exist in
leaf mesophyll. Type A secretory canals are present in stem, leaf, sepal and petal cross section. While type
B secretory canals are observed in sepal and petal, type C secretory canals are observed solely in ovary
cross section. All the structural features herein found can assist the diagnosis of H. thymopsis.
© 2016 Sociedade Brasileira de Farmacognosia. Published by Elsevier Editora Ltda. This is an open
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction and diabetes in Turkish folk medicine (Bingol et al., 2011; Özkan
and Mat, 2013). The taxa of Hypericum characterized by having
Hypericaceae is a small cosmopolite dicot family represented extensively secretory structure such as translucent glands, black
by nine genera and about 500 species of tree, shrub and herb in nodules and secretory canals which synthesizing and accumulating
the world (Simpson, 2006; APG III, 2009; Carine and Christenhusz, biologically active substances, so they have great phytochem-
2010). Hypericum is the largest genus of Hypericaceae by com- ical potential and composition (Siersch, 1927; Metcalfe et al.,
prising about 400 species throughout the world except the poles, 1950; Curtis and Lersten, 1990; Ciccarelli et al., 2001a, 2001b;
deserts and low altitude areas of tropical regions (Lewis, 2003; Onelli et al., 2002). Some of these phytochemical compositions of
Meseguer and Sanmartín, 2012). In Turkey, Hypericum is repre- the Hypericaceae are naphthodianthrones (notedly hypericin and
sented by 96 species, 104 taxa in which 45 of them are endemic pseudohypericin), acylphloroglucinol derivatives (notedly hyper-
with the endemism ratio 43% (Güner et al., 2012). The genus forin and adhyperforin), flavonoids (notedly quercetin, quercitrin,
Hypericum characterized by possess generally pale to dark yellow hyperoside and biapigenin), tannins, n-alkanes, xanthones and
flowers and transparently dotted leaves with red or black col- essential oils (Bombardelli and Morazzoni, 1995; Bruneton, 1995;
ored glands (Davis, 1966, 1988; Güner et al., 2000). The genus Kitanov, 2001; Maggi et al., 2004). Due to their phytochemical
Hypericum is known worldwide with its wide folk medicinal composition and waste usage in traditional folk medicine, many
usage (Avato, 2005; Assadi et al., 2011). Hypericum species are studies were made on biological activities of different species
known under the names “binbirdelik otu”, “kanotu”, “peygamber extracts of Hypericum in Turkey and in the world. For exam-
c¸ ic¸ egi”˘ and by a majority “sarı kantaron”, and have been used as ple, analgesic activity (Öztürk, 2001), wound healing activity
sedatives, antiseptics, anti-inflammatory, anti-astmatic, antispas- (Öztürk et al., 2007), hepatoprotective activity (Öztürk et al., 1992),
modics, wound-healing and to against stomach diseases, ulcers anti-inflammatory activity (Öztürk et al., 2002), anti-Helicobacter
pylori activity (Yes¸ ilada et al., 1999) and antidepressant activity
(Öztürk, 1997) of well-known Hypericum, H. perforatum L. were
studied by different researchers. In addition, antioxidant activ-
E-mail: [email protected] ity of H. venustum Fenzl was studied by Spiteller et al. (2008),
http://dx.doi.org/10.1016/j.bjp.2016.09.004
0102-695X/© 2016 Sociedade Brasileira de Farmacognosia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).
144 M. Tekin / Revista Brasileira de Farmacognosia 27 (2017) 143–152
antimicrobial activity of H. hyssopifolium Chaix var. microcalycinum University, Faculty of Science Herbarium (CUFH), Department
(Boiss. & Heldr.) Boiss. was studied by Toker et al. (2006), and of Biology, Sivas, Turkey. Taxonomical identification was made
myeloperoxidase activity of H. empetrifolium Willd. was studied by according to Flora of Turkey (Davis, 1966) by author.
Kültür (2007). In addition there are some studies focused morphol-
ogy, anatomy and secretory structure of some Hypericum species
(Metcalfe et al., 1950; Toma and Rugina,˘ 1998; Hong-Fei and Zheng- Structural analysis
Hai, 2001; Yaylacı et al., 2013; Perrone et al., 2013a, 2013b).
Hypericum thymopsis Boiss. is an endemic species for Turkey Morphological description of H. thymopsis was made using both
Flora and naturally growing in Sivas, Kayseri, Malatya and fresh and herbarium samples collected from different localities.
Kahramanmaras¸ provinces (Davis, 1966). Essential oil composition Parts of the some fresh material were stored in 70% alcohol–water
of H. thymopsis was studied by Özkan et al. (2009, 2013). Özkan et al. solution for later histo-anatomical procedures. For this reason,
(2013) studied composition of essential oils of five endemic Hyper- hand-made transverse sections of stem, leaf, sepal, petal, filament,
icum species for Turkey (H. uniglandulosum Hausskn. ex Bornm., ovary and style were taken. Also superficial hand-made sections
H. scabroides Robson and Poulter, H. kotschyanum Boiss., H. sal- of adaxial and abaxial surface of the leaf blade were taken with
sugineum Robson and Hub.-Mor. and H. thymopsis). According to razor blade. The sections were stained in 1% Alcian blue (Sigma)
their study, ␣-pinene, baeckeol, limonene and spathulenol were and 1% Safranine O (Sigma), in a ratio 3/2 (Davis and Barnett, 1997).
identified as major components of H. thymopsis. Furthermore, H. The sections were kept about 5 min in the dye. Semi-permanent
thymopsis has greatest potential by having so much more ␣-pinene, slides were mounded using glycerin-gelatine (Jensen, 1962). The
within these five species. ␣-Pinene is one of the active substance structural investigations of vegetative and reproductive parts of H.
which has bronchodilator and anti-inflammatory activity (Russo, thymopsis were made using Olympus BX22 light microscopy. Pho-
2011) and has bacteriostatic and bactericide effect against espe- tomicrographs were taken using Olympus BX51 light microscopy
cially gram (+) and gram (−) bacteria with broad spectrum (Nissen coupled with Olympus DP70 digital camera. The anatomical ter-
et al., 2010). In addition, it has acetylcholinesterase inhibitor activ- minology used is that according to Esau (1965). For secretarial
ity, thus it has effect that strengthens the memory of human (Russo, analyses, the study of Ciccarelli et al. (2001b) was carried out:
2011). ␣-Pinene is also reported as one of the main components (a) Translucent glands. These are pale glands or glandular pockets
of the essential oils of other some Hypericum species (Joulain and (Robson, 1981) and are spherical or oblong glands delimited by two
König, 1998; Santos et al., 1999; Zeng and Zhou, 2001; Gudziˇ c´ et al., layers. (b) Three types of secretory canals. Type A: the lumen of the
2002, 2004). canals is usually surrounded by four (or more in especially flow-
In the field works, by interviewing local peoples under an ers parts) polygonal cells which have very thin wall toward canal
ethnobotanical studies, it was learned that above ground parts lumen. Type B: they have a same structure with translucent glands
of H. thymopsis are used for wound-healing and sedation, and its with their wide lumen, but they seem elongated and pale which
infusions and decoctions as tea are used also against stomach dis- differ from the translucent glands. Type C: type C canals composed
eases and throat infections. By considering great usage of various of wide cavity surrounded by one or more cell layers which have
Hypericum taxa in folk medicine, their anatomical features are densely stained and thin walls.
not well-known except H. perforatum. In Turkey, there are some For scanning electron microscopy (SEM) analyses, the some
anatomical studies on other Turkish Hypericum taxa (Yaylacı et al., plant parts were mounted on aluminum stubs and coated with gold.
2013; Altıntas¸ and Akc¸ in, 2015). The morphological characteristics The micromorphological and anatomical observations were made,
of all Turkish Hypericum taxa are more or less known. But there and micrographs were taken at different magnifications by using
is some deficiency on some endemic species such as H. thymop- LEO 440 SEM.
sis. For example, in Flora of Turkey (Davis, 1966), dimensions of
sepals and ovaries, length of filaments, anthers, pistils and pedicels
Results
of H. thymopsis are not reported. Despite of some essential oil stud-
ies on H. thymopsis (Özkan et al., 2009, 2013), there is no report
Morphological aspects
on anatomical and histological structure of the species. The aim
of this study, revealed entirely morphological characteristics, and
Perennial herbs. Stems 3–14 cm, erect, numerous, glabrous,
anatomical and histological structure in all above ground parts and
scabrid with glandiferous emergences (Fig. 1B). Leaves
their secretory structures which make up biologically active sub-
5–18 × 0.6–1.6 mm, linear, revolute with obtuse or rounded
stances of H. thymopsis.
apex, glabrous, usually papillose at adaxial surface and especially
at margins. Black glands present at the margins of small leaves
which positioned at the base of pedicel on stem. Inflorescence
Materials and methods
corybose, up to 17 cm in fruiting time, soliter or 20 flowered. Sepals
1.9–2.8 × 0.8–1.1 mm, united at base, lanceolate to lanseolate-
Plant material
elliptic with sessile or subsessile black glands at margins and
acute apex (Fig. 1D). Sepals reddish when flowers in bud stage,
The specimens of Hypericum thymopsis Boiss., Hypericaceae,
green in flowering time (Fig. 1A, D). Petals 4.5–7.5 × 2–3.8 mm,
were collected during the flowering and fruiting time from differ-
pentamerous, elliptic-oblanceolate to obovate and without black
ent natural populations in Sivas province of Turkey. Field works
glands (Fig. 1C, E). Filaments 4–5.5 mm, thin and numerous.
were carried out in between the years 2012–2014. Locality 1: B6
◦ ◦
Anthers 0.35–0.45 mm, dorsifixed and longitudinal dehiscence
Sivas: Ulas¸ district, Ziyarettepe, 1444 m, 39 33 06.7 N; 37 01 11.9
(Fig. 1F). Pistils 4–5 mm, ovaries 1.5–2.2 × 0.9–1.4 mm, 3 loculed
E, 26.06.2013; Locality 2: B6 Sivas: Ulas¸ district, Kurtlukaya vil-
◦ ◦
and ovoidal shaped. Style 3, free and selender, 2.5–3.2 mm (Fig. 1G).
lage to Bogazdere˘ village, 1458 m, 39 23 02.1 N; 36 55 48.3 E,
Placentation axillar, ovules anatropous. Pedicels 2–8 mm. Fruit
05.06.2014; Locality 3: B6 Sivas: Sivas-Kangal-Gürün road inter-
◦ ◦
4.5–5.5 × 2.7–3.1 mm, ovoid, reddish-brown, septicidal capsule
section, 1560 m, 39 07 53.1 N; 37 14 32.9 E, 06.08.2012, ibid.
rostrate and with 3 locule, each locule bear usually 2, occasionally
05.06.2014, ibid. 05.07.2014.
1 seed. Seeds 2–2.3 × 0.7–1 mm, light brown, oblong-cylindrical
These were registered under collector numbers M. Tekin 1309,
and covered by densely short thick white hairs (Fig. 1).
1470, 1562, 1566, 1625 and are conserved at the Cumhuriyet
M. Tekin / Revista Brasileira de Farmacognosia 27 (2017) 143–152 145
A
B
100 μm
1 cm
C D E F G
1 mm
2 mm 1 mm 1 mm 1 mm
Fig. 1. Morphology of Hypericum thymopsis. In natural habitat at flowering stage (A); stem under SEM, arrows indicate glandiferous emergences (B); flower (C); calyx, arrow
indicate black glands (D); petal (E); stamen (F); pistil (G).
Anatomical and histological aspects Leaf
Leaf is “3” shaped in transverse section. There are uniseriate epi-
Stem dermises on both surfaces of the leaves. Adaxial epidermis cells are
The stem is in the secondary growth stage and circular shaped very large, oval or rectangular shaped and usually papillose espe-
in transverse section (Fig. 2A, E). The epidermis is uniseriate and cially near lamina margins, conversely, abaxial epidermis cells are
its cells are small, oval or usually irregular shaped, and are sur- small, rectangular or occasionally squarish shaped and are all non-
rounded by thick cutinized wall at all around the cell. Cuticle layer papillose (Fig. 3A, D). Epidermal cells have a smooth cuticle on both
is thick. There are two small wings and glandiferous emergences sides. There is conspicuous epicuticular wax on abaxial epidermis
on stem (Fig. 2A). Cortex consists of 3–7 parenchymatous cell lay- while it is lack of on adaxial surface (Fig. 4C–F). The cell wall of
ers. Cortex cells are oval or circular-shaped and there are some adaxial epidermis is very thick, despite that it is thin in abaxial epi-
intercellular spaces between them. There is a thin collenchyma dermis cells (Fig. 3D). In addition, margins of adaxial epidermis cells
which compose a ring in cortex. Endodermis is uniseriate and cells are distinct and slightly wavy, while margins of abaxial epidermis
are dorsoventrally depressed. The pericycle is conspicuous with cells are obscure. Stomata are anisocytic and sunken, occurring in
thickened laterally cell walls, just beneath the endodermis (Fig. 2B, both on the adaxial and predominantly abaxial sides of the leaf lam-
F). Vascular bundles are located in the major portion of the stem ina (Figs. 3F and 4). The mesophyll is dorsiventral and is formed
transverse section. In phloem, there are lots of type A secretory by 2–3 layers of palisade parenchyma and 2–3 layers of spongy
canals which are composed of four secretory cells. Cambium is parenchyma. While, the palisade parenchyma cells are gener-
indistinguishable. Secondary xylem is ring-porous. Pith rays are ally cylindrical, occasionally rectangular, squarish or ovoid-shaped,
parenchymatous and uniseriate, occasionally biseriate (Fig. 2C, G). the spongy parenchyma cells are usually cylindrical occasionally
Pith cells are parenchymatous and are oval or circular shaped. Size ovoid or irregular-shaped (Fig. 3B, D). There are large translucent
of pith cells enlarge toward center and the cell walls are lignified glands that positioned between just beneath the adaxial epider-
and prominently thickened in this region (Fig. 2D, H). mis and the middle area of spongy parenchyma (Fig. 3A, D). Small
146 M. Tekin / Revista Brasileira de Farmacognosia 27 (2017) 143–152
Fig. 2. Photomicrographs of stem transverse section of Hypericum thymopsis. Under light microscopy (LM) (A–D); under scanning electron microscopy (SEM) (E–H). General
view (A, E), red arrows indicate small wings in A; detail of cortex region (B, F); detail of vascular bundles (C, G); detail of pith region (D, H). Abbreviations: cl, collenchyma;
cx, cortex; ep, epidermis; en, endodermis; ge, glandiferous emergence; pe, pericycle; ph, phloem; pt, pith; pt-lg, pith cells-lignified; pt-nlg, pith cells-nonlignified; pr, pith
ray; sc, secretory canal-type A; sl, secretory cell; ve, vessel element; xy, xylem.
collateral vascular bundles are observed immersed into the meso- collenchyma cap which cells are usually ovoid or circular-shaped
phyll, associated with one or a few type A secretory canals and which make the midrib even more prominent and conspicuous
in the phloem (Fig. 3E). The midrib is oval-shaped, particularly (Fig. 3B). The cambium is clearly distinguishable between xylem
large and protrude from the abaxial surface. The midrib sur- and phloem, so vascular bundle type is open collateral. In vascu-
rounded by a uniseriate parenchymatous bundle sheath. There are a lar bundle, there are numerous type A secretory canals which are
M. Tekin / Revista Brasileira de Farmacognosia 27 (2017) 143–152 147
Fig. 3. Photomicrographs of the leaf trasnverse sections of Hypericum thymopsis. General view (A); detail of midrib region (B); detail of vascular bundle in midrib (C); detail
of lamina with translucent gland (D); detail of small vascular bundle with a type A secretory canal in mesophyll (E); detail of sunken stomata in adaxial epidermis (F).
Abbreviations: ab, abaxial epidermis; ad, adaxial epidermis; as, air space; bs, bundle sheath; ca, cambium; cx, cortex; gc, guard cells; ph, phloem; pp, palisade parenchyma;
sc, secretory canal-type A; sl, secretory cell; sp, spongy parenchyma; st, stoma; tg, translucent gland; vb, vascular bundle; xy, xylem.
composed of four secretory cells and are immersed the phloem Petal
(Fig. 3C). Adaxial and abaxial epidermises are uniseriate in petal trans-
verse section. While abaxial epidermis cells are rectangular or
squarish-shaped, adaxial epidermis cells are usually irregular
Sepal
shaped. The mesophyll consists of 5–8 layered parenchymatous
The transverse section of sepal was taken from calyx tube.
cells which are usually oval-shaped and have intercellular spaces
Epidermis is uniseriate in both sides. Adaxial epidermis cells are
between them (Fig. 6A, C). Vascularization is made by a few small
rectangular or rectangular ovoid-shaped, but they are larger and
vascular bundles in the center of mesophyll. Type A and type B
irregular shaped especially above the main vascular bundles region.
secretory canals may occur in same section, as they can be seen in
Abaxial epidermis cells are rectangular, squarish or oval shaped and
separate sections as in Fig. 6A and C. Type A secretory canals are
are usually larger than adaxial epidermis cells (Fig. 5A). Mesophyll
present in vascular bundles and they consist of four or more secre-
consists of 7–12 parenchymatous cell layers. These cells are usually
tory cells (Fig. 6B). Type B secretory canals occur just beneath the
oval, rarely circular-shaped and they have intercellular spaces. The
abaxial epidermis and they alternate with the veins (Fig. 6C, D).
midrib is almost circular-shaped and lacks bundle sheath (Fig. 5B).
There are type A secretory canals in phloem of vascular bundles and
these canals consist of 4–6 secretory cells (Fig. 5C). Beneath the Filament
abaxial epidermis, there are large type B secretory canals which
Filaments are very thin and triangular-shaped in transverse
alternate with the vascular bundles and immersed in mesophyll
section. Uniseriate epidermal cells are large and usually irregular-
(Fig. 5D).
shaped. Cuticle is thick and rugose. There is small single vascular
148 M. Tekin / Revista Brasileira de Farmacognosia 27 (2017) 143–152
Fig. 4. Photomicrographs of the leaf blade superficial sections on light microscopy (A and B); micrographs of the leaf blade surface on scanning electron microscopy (C–F)
of Hypericum thymopsis; general view of adaxial surface (A, C); detail of adaxial surface (B, D); general view of abaxial surface (E); detail of abaxial surface (F). Abbreviations:
wx, epicuticular wax; adc, adaxial epidermis cell; gc, guard cell; st, stoma; tg, leaf surface view of translucent gland.
bundle in the center of transverse section. Between epidermis and Discussion
vascular bundle, there are irregular-shaped parenchymatous cells.
The members of secretory structure are absent (Fig. 7A). Despite of its usage in folk medicine, the morphology of H. thy-
mopsis is not entirely known. There are some general knowledge
on morphology of the species in Flora of Turkey (Davis, 1966), but
Pistil there are no report on the shape of petals, dimensions of sepals and
The style is rectangular-shaped in transverse section. Epidermis ovaries, length of filaments, anthers, pistils, styles and pedicels of
is uniseriate, with rectangular, squarish or irregular-shaped cells. the species. These features are examined in present study. In Flora
Outer walls of epidermal cells are thick. Cuticle is rugose and thick. of Turkey (Davis, 1966), stems height and petals length of H. thy-
There is single vascular bundle which positioned close to epider- mopsis are given as 3–11 cm and 5–7 mm, respectively. In present
mis. There is pollen tube transmitting tract (PTTT) in the center of study, stems height and petals length of H. thymopsis were found
transverse section. Between the region of epidermis and PTTT are as 3–14 cm and 4.5–7.5 mm, respectively. In addition, black glands
filled by oval, circular or irregular shaped parenchymatous cells. were observed at the margins of small leaves which are positioned
The members of secretory structure are absent in transverse section at the base of pedicel on stem. It is not reported in Flora of Turkey
of style (Fig. 7B). The ovaries have 3 locules (Fig. 7C). Adaxial epider- (Davis, 1966) (Fig. 1).
mis cells of carpels are usually irregular, occasionally rectangular According to Metcalfe et al. (1950), pith rays are uniseriate, the
or squarish shaped. Abaxial epidermis cells of carpels are rectan- xylem and phloem are relatively narrow, whilst there is a greater
gular or squarish shaped. The mesophyll cells are parenchymatous development of pith in stem of herbaceous Hypericum. Conversely,
and usually irregular-shaped. Just beneath the adaxial epidermis, in H. thymopsis stem, phloem and especially xylem fill major part
there are numerous type C secretory canals which immersed in the of the transverse section, pith located in the small region of the
parenchymatic mesophyll of each locules (Fig. 7D). transverse section center (Fig. 2A, E). Pith rays of H. thymopsis are
M. Tekin / Revista Brasileira de Farmacognosia 27 (2017) 143–152 149
Fig. 5. Photomicrographs of calyx tube transverse section of Hypericum thymopsis. General view (A); detail of sepal midrib region with type A and type B secretory canals
(B); detail of vascular bundle and type A secretory canal in sepal (C); detail of type B secretory canal (D). Abbreviations: ab, abaxial epidermis; abw, abaxial epidermis cell; ad,
adaxial epidermis; cu, cuticle; pc, parenchymatous cell; ph, phloem; scA, secretory canal-type A; scB, secretory canal-type B; sl, secretory cell; st, stoma; vb, vascular bundle;
xy, xylem.
Fig. 6. Photomicrographs of petal transverse section of Hypericum thymopsis. General view with type A secretory canals (A) and detail view of vascular bundle and type A
secretory canal (B). General view with type B secretory canals (C) and detail view of type B secretory canal (D). Abbreviations: ab, abaxial epidermis; ad, adaxial epidermis;
cu, cuticle; pc, parenchymatous cell; ph, phloem; scA, secretory canal-type A; scB, secretory canal-type B; sl, secretory cell; vb, vascular bundle; xy, xylem.
150 M. Tekin / Revista Brasileira de Farmacognosia 27 (2017) 143–152
Fig. 7. Photomicrographs of the reproductive parts transverse section of flower of Hypericum thymopsis. General view of filament (A); general view of style (B); general view
of ovary (C); detail of carpel (D). Abbreviations: ab, abaxial epidermis; ad, adaxial epidermis; cp, carpel wall; cu, cuticle; ep, epidermis; pc, parenchymatous cell; ph, phloem;
pt, pollen-tube transmitting tract; scC, secretory canal-type C; sl, secretory cell; vb, vascular bundle; xy, xylem.
commonly uniseriate, occasionally biseriate. In addition, pith ray are absent in H. maculatum and H. hirsutum. In stem of H. thymop-
cells of H. thymopsis are upright and usually oval or rectangular- sis, type A canals and glandiferous emergences are present, but type
shaped, whereas the examined Hypericum species of Metcalfe et al. B canals are absent as well as H. maculatum and H. hirsurum (Fig. 2).
(1950), they are upright and entirely square-shaped (Fig. 2C, G). The However, there are no reports on presence of glandiferous emer-
outlines of stem transverse section are circular-shaped, vascular gences, in stems of their studied four Hypericum species. According
bundles of the H. thymopsis stems always formed a circle which to Gîtea et al. (2011), all examined species have 1–2 layered palisade
is reported for some other Hypericum species by Arda (1989) and parenchyma in leaf mesophyll, whereas it was observed as 2–3 lay-
Tokur and Mısırdalı (1989) (Fig. 2A, E). ered in H. thymopsis (Fig. 3B, D). According to Shields (1950), having
According to Metcalfe et al. (1950), the leaves of Hypericaceae more strongly developed palisade tissue is one of the characteris-
are dorsiventral with hypoderm in certain species of Hypericum and tic of the xerophytic plants, due to being the xeromophic plant, H.
stomata of Hypericum species are commonly surrounded by three thymopsis has similar feature of mentioned literature.
or more cells. The leaves of H. thymopsis are dorsiventral, with- Recently, Perrone et al. (2013a) were studied the leaf and stem
out hypodermis and stomata are anisocytic (Figs. 3B, D and 4A, B). anatomy of eight Hypericum species (H. aegypticum L., H. androsae-
The level of stomatal guard cells is lower than epidermis cells, so mum L., H. hircinum L., H. perfoliatum L., H. perforatum, H. pubescens
stomata are sunken type which is known as a special feature of Boiss., H. tetrapterum Fr. and H. triquetrifolium Turra) which grow
the xerophytes (Fig. 3F). Prominent epicuticular waxes are present heterogeneous environments of Sicily Island. General anatomical
on abaxial side of the leaf and thus, the capacity of reduce the characteristics of H. thymopsis are similar with those in their study.
water loss is increase (Fig. 4E, F). Furthermore, presence of the At the same time, there are some evident different characteristics
wax reduces mechanical damage and prevents from fungal and for H. thymopsis especially in leaf anatomy. In stem anatomy, there
insect attack (Eglinton and Hamilton, 1967). In addition, accord- are numerous glandiferous emergences outer of the H. thymopsis
ing to Briquet (1919) leaves of certain species of Hypericum growing stem (Figs. 1B and 2A, E). There is no report on the presence of this
arid regions in Brasil have thickened margins consisting of enlarged characteristic in stems of their studied eight species. Transverse
epidermal cells or collenchyma. The margin epidermal cells of H. section shape of the stem and presence of slightly two wings in
thymopsis leaves are enlarged, the cuticle and outer cell walls of H. thymopsis are common characteristics with some species stud-
these cells are more thickened than other epidermal cells (Fig. 3A, ied by Perrone et al. (2013a). Secondary xylem of H. thymopsis is
D) so, the leaves of H. thymopsis show the same feature of men- ring-porous (Fig. 2C, G) such as their studied six species, except H.
tioned knowledge. pubescens and H. aegypticum which have diffuse-porous secondary
Gîtea et al. (2011) were studied four Hypericum (H. perfora- xylem. The leaves of H. thymopsis are dorsiventral (Fig. 3A, B, D) as
tum, H. tetrapterum Fries, H. maculatum Crantz and H. hirsutum with H. perforatum, H. perfoliatum, H. tetrapterum, H. androsaemum
L.) in point of secretory structure of some vegetative organs. In and H. hircinum, but the leaves of H. pubescens, H. triquetrifolium
their study, while type A canals are present in the phloem of all and H. aegypticum are isobilateral (Perrone et al., 2013a). The leaves
four species stems, type B secretory canals are present solely, in of H. thymopsis are amphistomatic (Fig. 4) as with H. pubescens, H.
subepidermic area of H. perforatum and H. tetrapterum, and they tetrapterum, H. triquetrifolium and H. aegypticum while the leaves of
M. Tekin / Revista Brasileira de Farmacognosia 27 (2017) 143–152 151
the H. perforatum, H. perfoliatum, H. androsaemum and H. hircinum glands, type A, type B and type C secretory canals which produce
are hypostomatic. All stomatal complexes are anisocytic in the biologically active substances were shown anatomically and his-
studied eight species by Perrone et al. (2013a), and this feature is tologically in vegetative and reproductive organs of H. thymopsis.
the same for H. thymopsis (Fig. 4A, B). Among their studied eight Therefore, some results given in this research were compared with
species, solely H. triquetrifolium is xerophyte as H. thymopsis and the results of other members of Hypericum in the literature records
they have many common characteristics, such as possess two small and differences between them were stated in detail. All this results
wings on stem, amphistomatic leaves and ring-porous secondary can be used to evaluate of the diagnostic features of H. thymopsis
xylem. One of the prominent differences between two species is as well as the genus Hypericum.
the leaf mesophyll which is dorsiventral in H. thymopsis while it is
isobilateral in H. triquetrifolium.
Conflicts of interest
There are some studies on morphology and anatomy of the Turk-
ish Hypericum (Arda, 1989; Tokur and Mısırdalı, 1989; Erkaya and
The authors declare no conflicts of interest.
Tokur, 2004; Altıntas¸ and Akc¸ in, 2015). Erkaya and Tokur (2004)
were studied morphology and anatomy of H. montbretii Spach.,
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