contribution to the anatomy of some angiosperms flower … in curs/21 2/8 popoviciu dan...the bark...

Annals of R.S.C.B., Vol. XXI, Issue 2, 2017, pp. 51 – 58 doi: 10.ANN/RSCB-2017-0009:RSCB Received 1o May 2017; accepted 19 July 2017.

The Romanian Society for Cell Biology ©, Annals of R. S. C. B., Vol. XXI, Issue 2, 2017, Dan Razvan Popoviciu, pp. 51 – 58 51

Contribution to the anatomy of some angiosperms flower parts with therapeutic value

R. BERCU (1), A. BAVARU (1), R. POPOVICIU (1)* 1 Faculty of Natural and Agricultural Sciences,

”Ovidius” University, Constantza, Romania

*Corresponding author

Dan Rǎzvan Popoviciu, Ph.D.

Faculty of Natural and Agricultural Sciences, “Ovidius” University, Campus, Aleea Universitǎţii, nr. 1, Corp B,

900525, Constanţa, Romania

Phone: +40(0)761.178.785

e-mail: e-mail: [email protected]

Key words: angiosperms, anatomy, flower parts, medicinal use, secretory elements

Summary

The paper presents some histological and

anatomical aspects of the floral elements

(petals or tepals, bract, bract peduncle and

female flower style, respectively), of some

medicinal herbs: Althaea officinalis L.,

Calendula officinalis L., Lavandula

angustifolia Mill., Lilium candidum L.,

Robinia pseudacacia L., Tilia tomentosa

Moench, Verbascum phlomoides L. and Zea

mays L.

Even though the structure organization is

almost the same for petal or tepals,

differences occur concerning the

conformation of epidermal cells, the cuticle

thickness, the presence or absence of the

secretive elements. Non-glandular hairs and

the mechanical tissue are present as well.

The bract of Tilia tomentosa has a foliar

structure and the bract peduncle a partial

secondary structure of conductive elements.

Zea mays style has a simple structure with

ground tissue and two vascular bundles. Introduction

Angiosperm flowers are extremely

specialized organs for sexual reproduction.

The paper deals with histological and

anatomical aspects of the floral elements

(petals, tepals, bract, bract peduncle or

style, as the case) of nine angiosperms

Althaea officinalis L., Calendula officinalis

L., Lavandula angustifolia Mill., Lilium

candidum L., Robinia pseudacacia L., Tilia

tomentosa Scop., Verbascum phlomoides L.

and Zea mays L.

Althaea officinalis L. (fam. Malvaceae),

commonly known as marshmallow, is a

perennial herb, native to North Africa, but

widespread today throughout Europe. It has

an erect, hairy stem up to 1-1.5 m. The

petiolate leaves are large, long-lobed, light

green-white and covered with stellate hairs.

The flowers with white-pink corolla are

large, located axillary below the leaves,

grouped in terminal racemes. The leaves

and flowers have a characteristic odor and a

mucilaginous taste (Bojor & Alexan, 1981).

Calendula officinalis L. (common

marigold) is an annual herb belonging to

Asteraceae family, native to Southern

Europe and the Mediterranean region

except for Greece and Italy. It has sparsely

branched, lax or strong, erect stems,

growing up to 30-80 cm. The flowers are

grouped in flower heads, with central

tubular and on marginal yellow or yellow-

orange ligulate flowers (Preda, 1989).

Lavandula angustifolia Mill. (fam.

Lamiaceae), commonly known as lavender,

is native to calcareous and mountainous



areas in the Western Mediterranean. It is a

strong aromatic shrub with square, lignified

stems. The leaves (2–6 cm long) are

opposite, linear, with right margins and a

sharp tip. (Bojor & Alexan, 1981). The

gamopetal, bilabiate bluish-purple flowers

are zygomorphic, almost sessile, arranged

in spikes at the top of the branches

(Ecaterina & Răducanu, 1992).

Lilium candidum L. (Liliaceae family).

Lilies are spread in all temperate regions of

the Northern Hemisphere but also in the

Mediterranean region, throughout Asia, so

far as Japan and India, in the US, Canada,

as well as in Balkans and western Asia. The

genus Lilium comprises over 100 species,

distributed worldwide. Lilies are perennial

ornamental herbaceous plants, with large,

fragrant flowers. Lilium candidum known

as white lily is the most popular. It has scaly

bulbs, a foliate stem up to 1.5 m, bearing 3-

20 terminal large white flowers that open in

early summer.

The leaves are linear or reverse-

lanceolate, hairless and grow opposite. The

flowers are large, funnel-shaped, white and

strongly odorant (Barneby, 1986).

The black locust or false acacia - Robinia

pseudoacacia L. – (fam. Fabaceae) is a tree

growing spontaneously on almost any type

of soil. It is native to the North American

continent, being introduced in Europe

(France) in 1601. In many European

countries, including Romania, it is

considered an invasive species (Călinescu,

1941; Pârvu, 2000).

The stem is straight, up to 25-30 m high,

with a wide, rare, light crown, developed up

on the trunk. The trunk can grow up to 1 m

in diameter. The bark is smooth in young

individuals, forming a thick, longitudinally

cracked rhytidome successively. The leaves

are even-pinnately compound, long

(approx. 25 cm), with 7-15 elliptic leaflets.

The papilionaceus, zygomorphic flowers

are white, fragrant and have a campanulate

calyx. They are grouped in 25-50 simple

racemes (Ciocârlan, 2000).

Tilia tomentosa Moench (fam.

Tiliaceae), known as silver linden or silver

lime, occurs at moderate altitudes in

Southwest Asia and Southeast Europe, from

Hungary to Western Turkey. Tilia

tomentosa is a tree, up to 40 m tall, with a

dense globular crown. The petiolate leaves

are ovate, asymmetrical at their base, green

and mostly hairless above, densely white

tomentose with white hairs below, with a

pointed tip and serrated margin. The

flowers are yellowish-white and fragrant,

protected by a pedunculated green bract.

The flower stalk has a glabrous pale

green to yellow lanceolate bract. Flowers

are grouped in inflorescences (3-15 flowers;

Ciocârlan, 2000).

Verbascum phlomoides L., (mullein,

fam. Scrophulariaceae) is a biannual/

perennial plant widespread in Romania,

which grows on rocky or cultivated and

uncultivated lands. In the first year the plant

forms a basal rosette of petiolate and hairy

leaves. In the second year, it develops a

straight, cylindrical stalk (20 cm long) with

multiseriate grey hairs. The leaves are large

and soft, covered with yellow hairs.

Flowers are large, golden-yellow, grouped

in racemes, with honey-like odor and sweet

taste. They bloom from June to October

(Ciocârlan, 2000; Pârvu, 2000).

Zea mays L. (fam. Poaceae), known as

maize, is grown in Romania on large

surfaces and has many varieties. Zea mays

is a monoecious plant cultivated today in

many regions of the world as a food and

forage plant. It has thick, unbranched stems

with obvious nodes and internodes.

The leaves are long, rough, with a sharp

tip. Male flowers are grouped in pairs

(spikelets) enclosed by two bracts; spikelets

form a terminal panicle. The female

inflorescence (spadix) is completely

wrapped in a small number of leaves and

forms the ‘cob’. Each flower is enclosed by

thin transparent bracts and consists of an

ovary with a single ovule, and a long style

which protrudes from the top of the cob

(Weatherwax, 1916; Zanovschi & Toma,

1985).

The anatomical studies on angiosperms

floral elements, especially those with



therapeutic value, is a field being

sporadically addressed in Romanian and

foreign scientific literature (e.g. Bowes,

2004; Fahn, 1990; Metcalfe & Chalk, 1965;

Özkan & Uzunhisarcikli, 2009; Shaheen et

al., 2010; Sulborska et al., 2012; Souza,

2003; Souza et al., 2004; Toma & Rugină,

1998). Most works concern morphological

and pharmaceutical aspects (e.g.

Batanouny, 1999; Capek et al., 1987;

Elmastas et al., 2004; Fakhari et al., 2005;

Hajhashemi et al., 2003; Rouhi & Ganji,

2007; Wali et al., 2007; Weberling, 1992

etc.). For this reason our research brings an

information surplus to the knowledge of the

selected species.

The active products of the studied

species flower parts are used for therapeutic

purposes, in the treatment of various

diseases such as digestive, respiratory, renal

and reproductive diseases, circulatory

system disorders, nervous system diseases,

rheumatism, skin diseases etc.

Material and methods

Small pieces of petals (tepals), bract

peduncle, bract and style, respectively, of

the studied medicinal herbs were fixed in

FAA (formalin: glacial acetic acid: alcohol

5:5:90). The cross sections were performed

by freehand technique (Bercu & Jianu,

2003). The samples were stained with alum-

carmine and iodine green. Anatomical

observations and micrographs were

performed with a Biorom–T bright-field

microscope, equipped with a Topica 6001A

video camera.

Results and discussion

Cross section of Althaea officinalis petal

had an elongate shape with slightly

narrowly curved margins. Externally, it has

a single-layered upper and lower epidermis

with rectangular, narrow, small cells

covered by a fine cuticle, followed by the

mesophyll. Remarkable are the stellate non-

glandular hairs with long one-celled

branches, more abundant to the petal

margins (Fig. 1, a, b) as reported by Toma

& Rugină (1998) and Özkan &

Uzunhisarcikli (2009).

The mesophyll shows numerous large air

spaces. Some of the mesophyll cells are

mucilaginous. The vascular system is

fascicular with a large number of small

collateral bundles (Fig. 1, c).

Ligula of Calendula officinalis, in cross

section made through its base, exhibits,

externally, a single-layered upper epidermis

and a lower epidermis. The upper epidermal

cells are rectangular and slightly elongated

whereas those of the lower epidermis are

more or less rounded. Such as Toma &

Rugină observed in1998, lower epidermis

exhibited glandular and non-glandular hairs

with uniseriate and biseriate stalk. The

glandular hairs possessed multiple-cell

glands. The many-layered mesophyll is

homogenous and consists of

parenchymatous and oxaliferous (small

calcium oxalate crystals) cells. Small

collateral bundles (5-6 vascular bundles)

consisting of few xylem and phloem

elements are embedded in the mesophyll.

The central bundle is larger than the rest.

Fig. 1. Cross sections of Althaea officinalis L.

Ensemble (a, x 50). Portion with mesophyll and

vascular bundles (b, x 145). Non-glandular hairs (c,

c b

a

http://www.sciencedirect.com/science/article/pii/0008621587801477

http://www.sciencedirect.com/science/article/pii/S036725300700028X



x 60): as- air space, m- mesophyll, h- hairs, le- lower

epidermis, mc- mucilaginous cells, ue- upper

epidermis, vb- vascular bundle.

The yellow-orange color is due to the

presence of chromoplasts in the epidermal

and mesophyll cells (Fig. 2, a, b).

The cross section, of the tubular part of

Lavandula angustifolia corolla showed an

upper and lower epidermis covered by thin

cuticle. The upper epidermal cells are

rectangular and in the distal part papillose

whereas those of the lower epidermis have

a papillose aspect, particularly between the

glandular, unicellular, bi- or even

multicellular hairs stalks. All of them have

a unicellular gland head (Fig. 3, b). Long,

uneven stalks and unicellular heads may

occur. Some hairs showed small spheroid

protuberances just below the insertion point

of the intermediary cell on the stalk (Fig. 3,

d)

The upper epidermis possesses numerous

non-glandular many-celled branched hairs.

The mesophyll is homogenous, reduced to

2-3 layers of small cells and wide

intercellular spaces. The vascular system is

represented by poorly developed small

collateral bundles, the central one being

larger than the others (Fig. 3, a, b, c).

Cross sections of Lilium candidum tepal

disclose the usual succesion of tissues:

upper epidermis, mesophyll and lower

epidermis. Both epidermises are single-

layered and have rectangular cells covered

by a relatively thick cuticle (Fig. 4, a, b).

The lower epidermis forms a large proemi-

nence and have smaller cells and rare

inactive stomata (Fig. 4, c). The mesophyll

is homogenous and composed of round-

shaped cells, some of them secreting

essential oils, such as in other angiosperms

petals (Sulborska et al., 2012; Souza, 2003;

Souza et al., 2004) and small intercellular

spaces.

Fig. 3. Cross sections of Lavandula angustifolia

tubular corolla. Ensemble (a, x 70). Portions with

mesophyll and glandular and non-glandular hairs (b,

c x 300; d- x 280): gh- glandular hear, le- lower

epidermis, m- mesophyll, ngh- non-glandular hairs,

vb- vascular bundle.

In the mesophyll, a large number (23-24

bundles) of randomly arranged, well-

b

c

a

a

b

d

Fig. 2. Cross section of

Calendula officinalis L. petal.

Ensemble (a, x 70). Detail of

the mid rib zone (b, x 200):

gh- glandular hair, le- lower

epidermis, m- mesophyll,

ngh- non-glandular hairs, ph-

phloem, ue- upper epidermis,

vb- vascular bundle, x- xylem

(the arrow indicate air

spaces).



developed collateral bundles are present.

The vascular bundles consist of few xylem

and phloem elements (Fig. 4, a).

Robinia pseudoacacia L. petal showed

single-layered upper and lower epidermis,

with rectangular cells. The cells are

cutinized, covered by a thick cuticle. The

homogenous mesophyll has a number of

large parenchyma cells, some of them with

mucilage. Small vascular bundles with few

xylem elements and some more phloem

elements are embedded in the mesophyll

(Fig. 5).

Fig. 4. Cross sections of Lilium candidum tepal.

Ensemble (a, x 90). Portions with upper and lower

epidermis (b, c). A vascular bundle (d) (b-d x 350):

cu-cuticle, ph- phloem, m- mesophyll, le- lower

epidermis, s- stoma, ue- upper epidermis, vb-

vascular bundle, x- xylem.

Tilia tomentosa bract peduncle has a

single-layered epidermis with a thick

cuticle. Some of the epidermal cells are

transformed into non-glandular hairs,

grouped in clumps (three hairs/clump) such

as Toma & Rugină (1998) reported (Fig. 7,

a). Bellow the epidermis, there is a

hypodermis with 5-6 layers of collenchyma

cells, followed by few layers of

parenchyma, with numerous large

mucilaginous cells and oxaliferous cells.

The vascular system is represented by

xylem and phloem, with compact layout

tendency, separated by medullary rays, with

some of their cells being slightly lignified.

Xylem is better developed than phloem.

The periphloemic sclerenchyma fibers are

close creating the impression of a

continuous ring (Fig. 6. a, b).

Fig. 5. Cross section of Robinia pseudoacacia petal

(x 225): cu- cuticle, le- lower epidermis, m-

mesophyll, mc- mucilage cell, ue- upper epidermis,

vb- vascular bundle.

The bract, in cross section, has one-

layered upper and lower epidermises, with

more or less isodiametric cells covered by a

thick cuticle. Remarkable is the presence of

non-glandular hairs grouped in clumps (5-8

hairs/clump) denser than those of the

peduncle (Fig. 7, a, b). In the midrib zone,

bellow the upper epidermis and above the

lower there is a region of collenchyma

tissue, followed by a basic tissue.

The mesophyll is narrow and

homogenous with large intercellular spaces

(Fig. 7, a). The midrib consists of 5 vascular

bundles surrounded by periphloemic fibers

with thick, lignified walls. Compared to

other authors (Toma & Rugină, 1998; Fahn,

1990), mechanical fibers were observed

between the vascular bundles of the bract

(Fig. 7, c). In the midrib, mucilaginous cells

occur (Fig. 7, c).

a

b c

d



Unlike other plant species petals

structure (e.g. Sulborska et al., 2004), Tilia

tomentosa flower petal, in cross section,

discloses that the outer cells walls of upper

and lower epidermial cells are slightly

convex and form small papillae, whereas

the anticlinal walls are straight. The upper

part of papillae is covered by a striate

cuticle covering at the apex. Stomata are

present. The mesophyll is homogenous,

with isodiametric parenchymatous cells.

Large mucilaginous cells are present in the

mesophyll. On the analyzed material there

were no oxaliferous cells (mentioned by

Toma & Rugină, 1998; Fig. 8).

Fig. 6. Cross section of the bract peduncle of Tilia

tomentosa. Ensemble (a, x 100). Portion with

epidermis, cortex and stele (b, x 220): e- epidermis,

c- cortex, co- collenchyma, d- druse, h- hypodermis,

mc- mucilaginous cell, pf- periphloemic fibers, ph-

phloem, st- stele, x- xylem.

Verbascum phlomoides petal shows, in

transection, the usual tissue succession:

upper epidermis, a lower epidermis and the

mesophyll. Epidermal cells are slightly

convex and form small papillae, especially

those of the upper epidermis, covered by a

thin cuticle. Remarkable are the large,

multicellular, branched, non-glandular hairs

of candelabra type (Payne, 1978), mostly

placed on the lower epidermis. The

mesophyll is homogenous (spongy tissue

type), some of its cells containing mucilage.

The vascular bundles are poor lydeveloped

with few xylem and phloem elements (Fig.

9).

Zea mays gynoecium style of the female

flower, in cross section, exhibits a more or

less flat contour, slightly dimpled (adaxial)

and convex (abaxial). Externally, the

epidermis consists of single-layered

epidermal cells, covered by a thin cuticle.

Most of the style consists of ground tissue,

with two vascular bundles embedded.

Fig. 7. Cross section of Tilia tomentosa bract.

Portion with mesophyll (a, x 175). Non-glandular

hairs (b, x 300). The mid rib (c, x 175): is-

intercellular space, le- lower epidermis, m-

mesophyll, mc- mucilage cell, ngh- non-glandular

hair, sv- secondary vein, vb- vascular bundle, ue-

upper epidermis.

Centrally, a number of collenchyma cells

are present, both in adaxial and abaxial

position.

The vascular bundles are poorly

developed, with few xylem and phloem

a b

c

a

b



elements, with foliar arrangement (Fig.

10, a, b).

Fig. 8. Cross section of Tilia tomentosa petal (x

200): le- lower epidermis, m- mesophyll, mc-

mucilaginous cell, ue- upper epidermis, vb- vascular

bundle.

Fig. 9. Cross section of Verbascum phlomoydes petal

(x 90): le- lower epidermis, m- mesophyll, mc-

mucilaginous cell, ngh- non-glandular hairs, ue-

upper epidermis, vb- vascular bundle.

Fig. 10. Cross section of Zea mays gynoecium style

(female flower). Ensamble (a, x 100). Portion with a

vascular bundle (b, x 250): co- collenchma, e-

epidermis, gt- ground tissue, ph- phloem, vb-

vascular bundle, x- xylem.

Conclusions

The flower petals or tepals, respectively, of

all studied species have the same plan of

structural organization. Differences occur

concerning the shape of epidermal cells,

cuticle thickness, number of mesophyll cell

layers, the presence or absence of non-

glandular hairs and inactive stomata, as well

as the degree of vascular bundles

development (mainly of the midrib). The

secretive elements are glandular hairs

(Calendula officinalis and Lavandula

angustifolia), mucilaginous cells (Althaea

officinalis, Robinia pseudoacacia, Tilia

tomentosa and Verbascum phlomoides),

oxaliferous cells and cells with essential

oils (almost all studied species).

Tilia tomentosa bract has a foliar

structure with three vascular bundles and an

incipient secondary structure of xylem and

phloem in the bract peduncle.

Zea mays style has a simple structure

with two poorly developed vascular

bundles.

Non-glandular, multicellular, branched

hairs were found on the petals of Lavandula

angustifolia and Verbascum phlomoides

and simple single-cell hairs, on the petal of

Althaea officinalis, Verbascum phlomoides

and Tilia tomentosa bract peduncle, bract

and petal. The mechanical tissue is

represented by mechanical fibers (Tilia

tomentosa peduncle and bract) and

collenchymatous tissue (Althaea officinalis,

Tilia tomentosa bract and peduncle and Zea

mays style).

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contribution to the anatomy of some angiosperms flower … in curs/21 2/8 popoviciu dan...the bark...

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