Research Article |
Corresponding author: Tuncay Dirmenci ( dirmenci@balikesir.edu.tr ) Academic editor: Eberhard Fischer
© 2018 Gülay Ecevit-Genç, Betül Büyükkılıç-Altınbaşak, Taner Özcan, Tuncay Dirmenci.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ecevit-Genç G, Büyükkılıç-Altınbaşak B, Özcan T, Dirmenci T (2018) Comparative anatomical studies of some Teucrium sect. Teucrium species: Teucrium alyssifolium Stapf, Teucrium brevifolium Schreb. and Teucrium pestalozzae Boiss. (Lamiaceae). PhytoKeys 96: 63-77. https://doi.org/10.3897/phytokeys.96.24498
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Teucrium alyssifolium Stapf (endemic), Teucrium pestalozzae Boiss. (endemic) and Teucrium brevifolium Schreb. are three closely related taxa in Teucrium sect. Teucrium. The obtained data from the anatomical studies revealed that these three taxa represent the general anatomical characteristics of the Lamiaceae family. Leaves, anatomical features such as thick cuticle, abundant trichomes, rich palisade parenchyma layer in the mesophyll provide evidence that these three species are xeromorphic structures. Leaf and stem anatomy showed that the taxa have generally similar anatomical features. However, cuticle layers, epidermis cells size, indumentum density, mesophyll types, palisade parenchyma occupied in the mesophyll, presence of spherocrystals in leaves and parenchyma, collenchyma and sclerenchyma layers in stems show differences amongst the taxa. Anatomical characters of leaf and stem of these taxa are examined for the first time in this study.
Lamiaceae , Teucrium, leaf anatomy, stem anatomy
The genus Teucrium L. has approximately 300 species all over the world. Teucrium’s cosmopolitan distribution is mainly concentrated in Europe, North Africa and in the temperate parts of Asia (
Teucrium species have traditionally been used in Turkey for abdominal pain, stomach-ache, common cold, high fever, antipyretic, rheumatic pain and as an antidiabetic (
T. alyssifolium is a narrowly distributed endemic species. It is classified as a ‘Conservation Dependent (LR/cd)’ category of IUCN and it is a source of polyphenols and flavonoids and has confirmed antioxidant activities (
The chromosome numbers are reported as 2n = 10, 14, 16, 18, 22, 26, 28, 30, 32, 36, 39, 48, 52, 56, 58, 60, 62, 64, 78, 80, 86, 90, 96 and 104 in the genus Teucrium (http://www.tropicos.org/Project/IPCN). The chromosome number of T. brevifolium examined in this study was determined as 2n = 30. Another member of the sect. Teucrium, T. sandrasicum, was studied and it was determined that the chromosome number is the same as T. brevifolium (
Pollen morphology supplies useful data at the taxonomic level in Teucrium (
There are several studies on Teucrium anatomy (
T. pestalozzae samples were collected from Antalya, T. brevifolium and T. alyssifolium samples were collected from Muğla provinces in Turkey (Figures
The anatomy of the collected specimens were assessed by examination of leaf and stem cross sections (Figures
Leaf anatomy
The epidermis at the both surfaces of the leaves is single layered. The epidermis consists of single-layer, ovoid or rectangular cells which are covered by thick cuticula. The upper epidermis cells are larger than the lower ones. Both leaf surfaces are covered by glandular and non-glandular trichomes. Also, the upper epidermis is covered with lower-density trichomes than the lower epidermis. The spherocrystals occur in the upper epidermis cells of the leaf in T. allysifolium. Leaves are isolateral. The mesophyll is differentiated into 1 layered palisade and 2–3-layered spongy parenchyma. The palisade parenchyma cells are under the upper and lower epidermis.
Their shapes are cylindrical in transverse section. The palisade parenchyma occupies about 60–65% of the mesophyll. The spongy parenchyma cells, ovoid or circular, are located between the palisade tissues. Both parenchyma tissues contain starch grains. The midrib has 3–4 layered collenchyma and 1–2 layered parenchyma below the lower epidermis. The vascular bundle is located in the central part of the midvein. Vascular bundles are collateral. The xylem layer is just below the collenchyma. 1–2 layered parenchyma and 5–6 layered collenchyma are located under the phloem (Figure
Stem anatomy
The stem is quadrangular shaped. The epidermis consists of single-layer, ovoid or rectangular cells which are covered by thick cuticula. There are glandular and non-glandular trichomes on the epidermis. Collenchyma with a single layer of cells between the corners but 4–5 layers of collenchyma at the corner of the stem. The cortex, consisting of 3–4 layered ovoidal parenchymatous cells, is located under the collenchyma. The endodermis is conspicuous as a single layer. The vascular tissue is surrounded by 1–2 layers of sclerenchyma fibres. The cambium is indistinguishable. Phloem and xylem members are conspicuous. The pith is present at the middle of the stem and it is completely filled by orbicular parenchymatic cells (Figure
Leaf anatomy
The epidermis in both surfaces of the leaves is single layered. It is consists of single-layer, ovoid or rectangular cells which are covered by cuticula. Both surfaces are covered by a thick cuticula layer, with dense indumentum built of glandular and non-glandular trichomes. The upper epidermal cells are as large as the lower ones. Spherocrystals are observed in both epidermis cells. Leaves are dorsiventral. Palisade parenchyma has two layers and palisade parenchyma cells shapes are cylindrical in transverse section. The palisade parenchyma occupies about 60% of the mesophyll. Spongy parenchyma consists of four or five layers and their cells are ovoid or circular.
Starch accumulated in both spongy and palisade parenchyma. Midrib has 5–6 layered collenchyma and 1–2 layered parenchyma below the lower epidermis. The collateral vascular bundle is located in the central part of the midvein. The xylem layer is found under the collenchyma. 1–2 layered parenchyma and 2–3 layered collenchyma are located under the phloem (Figure
Stem anatomy
The stem is rectangular shaped. The epidermis consists of single-layer, ovoid or rectangular cells which are covered by thick cuticula. It is covered by glandular and non-glandular trichomes. Underneath the epidermis, 6–7 layers of collenchyma are located at the corners, 3–4 layered collenchyma is located between the corners. Beneath the collenchyma, 5–6 layered rectangle shaped parenchymatous cells are located. Starch grains are also present in the parenchymatous cells. Endodermis and cambium are inconspicuous. 2–3 sclerenchymatic cell clusters are situated at the corners above the phloem. The pith is present in the middle of the stem and is completely filled by orbicular parenchymatic cells (Figure
Leaf anatomy
The epidermis in both surfaces of the leaves is single layered. It is consists of single-layer, ovoid or rectangular cells which are covered by cuticula. The upper epidermis cells are larger than the lower ones. The upper cuticle layer is slightly thicker than the lower ones.
Both surfaces are covered by glandular and non-glandular trichomes. Also, trichomes are abundant on the lower epidermis of leaves and sparse on the upper epidermis of leaves. Leaves are dorsiventral. The spherocrystals occur in the upper epidermis of the mesophyll. Mesophyll is differentiated into 2-layered palisade and 5–6-layered spongy parenchyma. Palisade parenchyma cells are cylindrical shaped in transverse section. The palisade parenchyma occupies about 50–55% of the mesophyll.
The spongy parenchyma cells are ovoid or circular. Both parenchyma tissues densely contain starch grains. Midrib has 5–6 layered collenchyma and 1 layer of parenchyma below the lower epidermis. The collateral vascular bundle is located in the central part of the midvein. The xylem layer is found under the collenchyma. 1–2 layered parenchyma and 4–5 layered collenchyma are located under the phloem (Figure
Stem anatomy
The stem is rectangular shaped. The epidermis consists of single-layer, rectangular cells which are covered by cuticula. There are glandular and non-glandular trichomes on the epidermis. Underneath the epidermis, there is collenchyma with 1–2 layers between the corners but 7–8 layers of collenchyma at the corner of the stem. The cortex, consisting of 5–6 layers of ovoid shaped parenchymatous cells, is located under the collenchyma. 1–2 layers of sclerenchyma fibres are located above the phloem. The cambium is indistinguishable. Phloem and xylem members are conspicuous. The pith is present in the middle of the stem and is completely composed of orbicular parenchymatic cells (Figure
Taxon |
Locality, Voucher number ( |
T. brevifolium | Muğla: Marmaris-Knidos, Datça peninsula, 30–100 m elev., 16 May 2012, T. Özcan, T. Dirmenci, O. Yıldırım, |
T. pestalozzae | Antalya: Between Antalya and Burdur, Çubuk Beli gateway, 950–1000 m elev., 17 May 2012, T. Özcan, T. Dirmenci, O. Yıldırım, |
T. alyssifolium | Muğla: Fethiye-Çameli road, Tuzla Beli gateway, 1440 m elev., 14 April 2011,T. Özcan, T. Dirmenci, E. Akçiçek, |
T. alyssifolium, cross-section of the leaf (A), stem (B, C); cl: collenchyma; en: endodermis; gt: glandular trichomes; le: lower epidermis; p: parenchyma; ph: phloem; pp: palisade parenchyma; sc: sclerenchyma; scr: sphaerocrystal, sg: starch grains; sp: spongy parenchyma; t: trichome; ue: upper epidermis; xy: xylem; Scale bars: 50 mµ.
T. brevifolium, cross-section of the leaf (A), stem (B, C); cl: collenchyma; cu: cuticle; gt: glandular trichomes; le: lower epidermis; ph: phloem; pp: palisade parenchyma; sc: sclerenchyma; scr: sphaerocrystal, sg: starch grains; sp: spongy parenchyma; t: trichome; ue: upper epidermis; xy: xylem; Scale bars: 50 mµ.
T. pestalozzae, cross-section of the leaf (A), stem (B, C); cl: collenchyma; cu: cuticle; e: epidermis; gt: glandular trichomes; le: lower epidermis; p: parenchyma; ph: phloem; pp: palisade parenchyma; sc: sclerenchyma; scr: sphaerocrystal, sg: starch grains; sp: spongy parenchyma; t: trichome; ue: upper epidermis; xy: xylem; Scale bars: 50 mµ.
T. alyssifolium | T. brevifolium | T. pestalozzae | ||
Flowers | Pedicellate | Pedicellate | Pedicellate | |
Pedicels | 2.0–4.0 mm | 2.0–12 mm | 3.0–5.0 mm | |
Bracts | Orbicular-ovate, oblanceolate | Linear, linear-oblanceolate | Linear-lanceolate | |
Bract size | 2.0–20 × 1.5–5.0 mm | 3.0–9.0 × 1.0 mm | 10–12 mm | |
Calyces | Campanulate | Campanulate | Campanulate | |
Calyx size | 6.0–13 × 4.0–5.0 mm | (3.0-) 4.0–5.0 × 2.0–3.5 mm | 5.0–6.0 × 3.0–4.0 mm | |
Calyx teeth | 4.0–5.0 mm | 1.0–2.0 × 1.0 mm | 2.5–3.0 mm | |
Corolla | Lilac, light pinkish | White-pinkish | Bluish | |
Corolla size | 20–25 mm | 6.5–7.0 mm | 9.0–9.5 mm | |
Filaments | 18– 22 mm | 8.0–9.0 mm | 7.0–8.0 mm | |
Style | 20–22 mm | 9.0–10 mm | 8.0–9.0 mm | |
Leaf | Shape | Orbicular-ovate, oblanceolate | Linear or oblanceolate | Linear, obtuse or oblanceolate |
Size | 4.0–28 × 2.5–7.0 mm | 6.0–17 × 1.0–4.0 mm | 11–24 × 2.0–4.0 mm | |
Leaf apex | Acute or obtuse at apex | Acute or obtuse at apex | Acute or obtuse at apex | |
Cuticular thickness | Cuticular thickness | Equal | Equal | |
Epidermal cells | Upper epidermis cells are larger than the lower ones. | Upper epidermal cells are as large as the lower ones | Upper epidermis cells are larger than the lower ones | |
Indumentum density | Lower surface is denser than upper ones | Same density on both surface | Lower surface is denser than upper ones | |
Mesophyll type | Isolatheral | Dorsiventral | Dorsiventral | |
Mesophyll | 60–65 % palisade parenchyma | 60% palisade parenchyma | 60–65 % palisade parenchyma | |
Location of spherocrystals | Upper epidermis | Both epidermis | Upper epidermis | |
Collenchyma cells layers of midrib | 3–4 layered on the lower surface, 5–6 layered on the upper surface | 5–6 layered on the lower surface, 2–3 layered on the upper surface | 5–6 layered on the lower surface, 4–5 layered on the upper surface | |
Stem | Length | 3.5–9.0 cm | 30–110 cm | 15–18 cm |
Collenchyma cells layers | 1 layer between the corners, 4–5 layered at the corners | 3–4 layers between the corners, 6–7 layers at the corners | 1–2 layered between the corners, 7–8 layers at the corners | |
Cortex parenchyma | 3–4 layered | 5–6 layered | 5–6 layered | |
Endodermis | Conspicuous | Inconspicuous | Inconspicuous | |
Sclerenchyma | 1–2 layered | 2–3 cell clusters | 1–2 layered |
Sect. Teucrium is one of the eight Teucrium sections distributing in Turkey. The members of this section are perennial and shrubs or subshrubs. Leaves are entire to deeply dissected (in T. orientale subspecies, T. parviflorum, T. pruinosum) and revolute at the lower surface.
Flowers borne in racemes or spreading panicles or axillary in upper leaves. Peduncles/pedicels are 1–3-flowered. Calyx not gibbous, obconical-campanulate, teeth ± equal and triangular (
Three species showing the characteristic features of the section Teucrium, investigated in the present study, have some significant distinguishing characters. Especially the size of parts of the flowers are very distinctive. T. alyssifolium easily differs with its leaf and bract shape, flower, filament and calyx size from T. brevifolium and T. pestalozzae in their natural habitats (Table
In this study, morphologically related three taxa belonging to the sect. Teucrium have been investigated. Moreover anatomical features of these three species have been reported for the first time. Our results showed the general anatomical characteristics of three Teucrium species as well those reported by
The results of the present study revealed that there were differences amongst the leaf anatomy of these three taxa (Table
The palisade parenchyma shows a slight difference in mesophyll amongst the studied taxa. However, these differences can be based on different ecological conditions. Collenchyma layers are different in midrib amongst these studied taxa. The spherocrystals occur in the upper epidermis of the leaf in T. alyssifolium and T. pestalozzae and both epidermis of the leaf in T. brevifolium. According to
Some characteristics of the leaf anatomy which indicates of xeromorphy have been reported before in previous studies (Metcalfe and Chalk 1983,
In conclusion, this study shows that leaf and stem anatomy have a diagnostic value in the distinction of these three closely related Teucrium sect. Teucrium. Anatomical characters contribute to the separation of three species with the morphological characters.
The stem is rectangle shaped in all species. In general, the stems of the family Lamiaceae species are rectangular (
This work was supported by the Research Fund of İstanbul University (Project number 31081) and Research Fund of Balıkesir University (Project number 2012/8). We are grateful to Jessica Romero as a native speaker for her valuable contributions and language control of this manuscript.