Фенотипічна мінливість структури епідермісу та кремнієві включення у листках Quercus robur у парку “Феофанія”
The micromorphology of the leaf epidermis, localization, and silicon content in the epidermal cells of Quercus robur leaves growing in the shade and under direct sunlight in the Feofaniya Park (Kyiv, Ukraine) were studied using scanning electron microscopy and laser confocal microscopy. Silicon incl...
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M.M. Gryshko National Botanical Garden of the NAS of Ukraine
2023
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Plant Introduction| _version_ | 1860145138121048064 |
|---|---|
| author | Nedukha, Olena Zolotareva, Olena Netsvetov, Maksym |
| author_facet | Nedukha, Olena Zolotareva, Olena Netsvetov, Maksym |
| author_sort | Nedukha, Olena |
| baseUrl_str | https://www.plantintroduction.org/index.php/pi/oai |
| collection | OJS |
| datestamp_date | 2023-08-26T20:36:09Z |
| description | The micromorphology of the leaf epidermis, localization, and silicon content in the epidermal cells of Quercus robur leaves growing in the shade and under direct sunlight in the Feofaniya Park (Kyiv, Ukraine) were studied using scanning electron microscopy and laser confocal microscopy. Silicon inclusions were found in the anticlinal and periclinal walls of adaxial epidermal cells, trichomes, guard cells of stomata, and walls of regular epidermal cells on the abaxial leaf surface, the amount of which varied according to the conditions of growth. Natural shading and the intensity of solar irradiation were found affecting the size of leaf blades, the ultrastructure of the leaf epidermis, and changes in the silicon content of oak leaves. Studies have shown that the anticlinal walls of the adaxial epidermis and the trichomes and stomata of the abaxial epidermis of leaves are the main silicon accumulators. The findings suggest that changes in leaf microstructure and silicon content contribute to maintaining optimal water balance in plants and can be regarded as signs of phenotypic plasticity in plants and an adaptive marker depending on the sunlight conditions of oak growth. |
| doi_str_mv | 10.46341/PI2023001 |
| first_indexed | 2025-07-17T12:54:12Z |
| format | Article |
| fulltext |
© The Authors. This content is provided under CC BY 4.0 license.
Plant Introduction, 97/98, 18–32 (2023)
RESEARCH ARTICLE
Phenotypic variability of epidermis structure and silicon inclusions in the
leaves of Quercus robur in the Feofaniya Park
Оlena Nedukha 1, *, Olena Zolotareva 2, Maksym Netsvetov 3
1 Department of Cell Biology and Anatomy, M.G. Kholodny Institute of Botany of the National Academy of Sciences of Ukraine,
Tereschenkivska str. 2, 01601 Kyiv, Ukraine, * o.nedukha@hotmail.com
2 Department of Membranology and Phytochemistry, M.G. Kholodny Institute of Botany of the National Academy of Sciences of
Ukraine, Tereschenkivska str. 2, 01601 Kyiv, Ukraine
3 Department of Phytoecology, Institute for Evolution Ecology of the National Academy of Sciences of Ukraine, Acad. Lebedev str. 37,
03143 Kyiv, Ukraine
Received: 21.02.2023 | Accepted: 01.04.2023 | Published online: 30.04.2023
Abstract
The micromorphology of the leaf epidermis, localization, and silicon content in the epidermal cells of
Quercus robur leaves growing in the shade and under direct sunlight in the Feofaniya Park (Kyiv, Ukraine)
were studied using scanning electron microscopy and laser confocal microscopy. Silicon inclusions were
found in the anticlinal and periclinal walls of adaxial epidermal cells, trichomes, guard cells of stomata, and
walls of regular epidermal cells on the abaxial leaf surface, the amount of which varied according to the
conditions of growth. Natural shading and the intensity of solar irradiation were found affecting the size
of leaf blades, the ultrastructure of the leaf epidermis, and changes in the silicon content of oak leaves.
Studies have shown that the anticlinal walls of the adaxial epidermis and the trichomes and stomata of
the abaxial epidermis of leaves are the main silicon accumulators. The findings suggest that changes in
leaf microstructure and silicon content contribute to maintaining optimal water balance in plants and can
be regarded as signs of phenotypic plasticity in plants and an adaptive marker depending on the sunlight
conditions of oak growth.
Keywords: Quercus robur, leaf micromorphology, silicon, laser confocal microscopy, scanning electron microscopy, shade influence
https://doi.org/10.46341/PI2023001
UDC 581.45
Authors’ contributions: Dr. Olena Nedukha sampled and processed the plant material, conducted microscopic studies, described
the results, and wrote the text of the article. Dr. Olena Zolotareva – sampled the plant material, took photos of the collected material,
discussed the data, and edited the text of the article. Dr. Maksym Netsvetov – selected oak trees for research, provided geographical
characteristics of trees, and examined the data.
Funding: The study was financially supported by the National Academy of Science of Ukraine and performed at the Department of
Cell Biology and Anatomy of the Institute of Botany of the National Academy of Sciences of Ukraine (state registration Nr 8–22 of
January 04, 2022) within the project “Determination of structural-functional and molecular features of resistance of common oak
(Quercus robur L.) to aridization of the Ukrainian climate”.
Competing Interests: The authors declares that they have no conflict of interest.
Introduction
The study of the structural and functional
organization of organs and tissues of ancient
oak groves attracts the attention of many
researchers due to the stable mechanisms of
resistance against biotic and abiotic stresses
that the species have developed (Werker,
https://creativecommons.org/licenses/by/4.0/
https://orcid.org/0000-0001-8405-453X
https://orcid.org/0000-0001-9037-3588
Plant Introduction • 97/98 19
Phenotypic variability of epidermis and silicon inclusions in the leaves of Quercus robur
2000). The resilience of forest ecosystems to
extreme environmental conditions depends
mainly on the sensitivity of certain species
that form the forest. In Ukraine and Europe,
one of these species is the common oak
(Quercus robur L.). The problem of preserving
oak forests in Ukraine is warned by climate
changes causing the increased frequency
of windstorms and droughts. For oaks and
other tree species, the leaf epidermis is a
principal protective structure that reacts
to climate changes, especially to intensified
drought and solar activity. The leaf epidermis
is the first barrier between the plant and the
environment, protecting the plant from various
environmental factors, including soil drought,
windstorms, and intense solar radiation (Dietz
& Hartung, 1996). Epidermal structures, such
as stomata and trichomes, play an essential
role in the cell water balance regulation and
plant adaptation to extreme environmental
conditions.
The first stage of photosynthesis is the
capture and absorption of photons by
chloroplasts, followed by their utilization
and scattering. Plants have adapted to light
capture by regulating leaf and chloroplast
sizes, the location and orientation of leaves,
and modifying their photosynthetic apparatus
(Björkman, 1981; Björkman & Powles, 1981;
Brugnoli & Björkman, 1992; Mathur et al., 2018).
In addition, plants have developed several
mechanisms of protection against excessive
light, including the formation of trichomes and
the formation of wax on the leaf surface (Soares
et al., 2012; LoPresti, 2015). The developed wax
cover causes the increased light-reflectance
of the leaf surface and assures the plant’s
resistance to intense radiation (Hansen et al.,
2007; Custódio et al., 2015).
Investigating the structural and functional
organization of oak leaves is important for
fundamental and applied botany and forestry
because these plants (in particular, their
leaves, bark, seeds, and acorns) are actively
used in phytochemistry, pharmacology,
and agriculture. Due to the presence of
phenolic acid, terpenoids, and tannins in
oak tissues, which have a positive effect
on anti-inflammatory, anti-diabetic, and
anti-tumor effects, they can be considered
promising candidates for the development of
new pharmaceuticals for various infectious
diseases (Moon et al., 2013; Taib et al., 2020).
The presence of flavonoid compounds
(terpenoids) in leaf trichomes and parenchyma
was confirmed for two oak species (Quercus
ilex L. and Q. coccifera L.). Moreover, the
content of terpenoids in these two species
depended on the leaf growth stage and the
illumination level (Liakoura et al., 1999).
The aboveground organs and roots of oaks
contain, in addition to terpenoids, silicon
and are also used in medicine (Aseeva et al.,
1985). In agriculture, it was recently proposed
to use an extract from young oak leaves as a
natural resource of biofertilizer, which actively
influences tomatoes’ growth and biological
activity (Tahir et al., 2022).
Considering the role of silicon in absorbing
and reflecting sunlight, we decided to stress
the idea that silicon should be present in
the epidermis of oak leaves and that its
content will vary depending on the intensity
of sunlight and shade level. We also suppose
that the growth of oaks in conditions of
variable light and water supply is possible due
to their tolerance related to the peculiarities
in leaf morphology, in particular, the
ultrastructure of the epidermis. This study
aimed to investigate the stable and plastic
features of the leaf epidermal structure and
silicon content for oak trees of different ages
growing in Feofaniya Park (Ukraine), related to
both species characteristics and phenotypic
plasticity under different light intensities.
Material and methods
The object of the study was the leaves of
common oak trees (Quercus robur, Fagaceae)
growing in Feofaniya Park on the outskirts of
Kyiv, Ukraine (50°26’ N, 30°34’ E). Oak leaves for
the study were collected on May 31, 2022. The
material was collected from the trees growing
in both of the Feofaniya tracts in the territory
of Holosiivskyi district in the recreational
area of Kyiv. Four trees were selected for the
study, two growing on the Feofaniya hill and
two growing much lower, in the hollow. Tree
Nr 1 grow on a hill on the territory of the St.
Panteleimon Monastery, in the shade, on the
lawn next to other trees. Tree Nr 2 grow on the
highest point of Feofaniya hill, in the shade,
in a dense forest belt near the road, close to
Feofaniyiv lakes. Tree Nr 3 grow between the
hill and the depression, in the shade, alongside
20 Plant Introduction • 97/98
Nedukha et al.
other trees at the edge of Feofaniya Park. Tree
Nr 4 grow in the depression alone on the lawn
near the lakes of Feofaniya Park without shade,
50 m far from the lakeshore. Trees Nrs 1–3
grow under the shade of other trees (oaks and
maples), while tree Nr 4 grow separately on a
lawn, without shade from other trees (Table 1).
In a sampling day, the weather was rainy
and overcast. Photosynthetic photon fluency
rate (PPFR) was measured using the light
meter Li-Cor LI-250 (USA). PPFR on the
adaxial surface of the leaves of oak trees on
the sampling day ranged from 75 to 120 μmol
quantum m−2 · s−1. The mean daytime PPFR on
the next day (a sunny day) ranged from 850
to 1850 μmol quantum m−2 · s−1. PPFR data and
other measured oak parameters are provided
in Table 1.
The lowest branches (at the height of 2–2.5 m
above the ground) were taken for the study.
From these branches, 12–15 leaves of nearly the
same size were selected, photographed and
measured. For cytological studies, the middle
part of every second (upper) lobe in four leaves
was cut out. Leaves from 12–15 plants of each
ecotype were used for the microscopic and
cytochemical investigations.
The middle part of each second lobe
(upper) of the leaf blade was fixed for scanning
electron microscopy. The specimens were
fixed immediately in the field in the solution of
2 % paraformaldehyde and 1% glutaraldehyde
(1 : 1, vol.) in 0.5 M phosphate buffer (pH 7.2)
for 3 h at ± 4 °C (in a thermos). Then in the
laboratory, the samples were washed in the
identical buffer, and dehydrated in a series of
alcohols (70 %, 80 %, and 100 % ethanol; twice,
every 30 min) according to Talbot & White
(2013) protocol. After dehydration, the samples
were mounted on aluminum tables, sputtered
with carbon and gold, and examined using
JSM 6060 LA scanning electron microscope at
30 kV. To determine cell sizes, 30–40 regular
epidermal cells, 30–35 stomata, and 20–25
trichomes were used in three samples from
each leaf. Statistical significance of the cell size
and the stomata density was determined using
Origin 6.1 software, including the standard
error (± SE), and Student’s test (P ≤ 0.05).
The cytochemical study of the presence
and content of silicon with laser confocal
microscopy has been conducted following
Dabney et al. (2016). The samples of the middle
part of the second (upper) lobe of leaf blades
(10 × 20 mm) from four common oak trees were
exposed to high temperatures in an oven at
250 °C for three to four hours until the samples
darkened to gray. The prepared leaf samples
were examined using a laser scanning confocal
microscope Zeiss LSM5 (Germany) using
an excitation wavelength of 480 nm and an
emission wavelength of 530 nm, respectively.
Four leaves from each tree were taken for the
study. The average fluorescence intensity in
30–40 epidermal cells (stomata, trichome, and
regular epidermal cells) has been calculated.
Values of results expressed at the mean and
standard errors using Student’s test (P < 0.05).
The fluorescence intensity of silicon and other
chemical elements was measured using the
Pascal software.
Results
Micromorphology of Quercus robur leaves
The leaves of the four selected trees of the
common oak, regardless of the place of growth
and regardless of age, were characterized by
a similar morphology of leaf blades: leaves are
short-petiolate; the shape of the leaf blade
is elongated-obovate, narrowed downward,
Tree number Approximate
age, years
Trunk
perimeter at
a height of
1.5 m from the
ground, cm
Photosynthetic photon fluency
rate (PPFR), µmol·m-2·s-1
Shadiness
at the level
of lower
branches, %
Elevation,
m a.s.l.
cloudy day sunny day
Nr 1 ~200–250 353 110 1200 33.0 186
Nr 2 ~80 145 75 850 52.8 186
Nr 3 ~200 324 80 1000 45.0 154
Nr 4 ~50–70 158 120 1800 0.0 128
Table 1. Basic parameters of investigated Quercus robur trees and their habitat.
Plant Introduction • 97/98 21
Phenotypic variability of epidermis and silicon inclusions in the leaves of Quercus robur
and pinnately lobed (Fig. 1). The leaf blades
are blunt, rounded, and have shallow notches
between them. Some differences in the leaf
size, surface area, and ultrastructure of the
epidermis were found.
It was found that the leaves of the first three
investigated trees (Nrs 1–3) were quite large
and characterized by a significant leaf blade
area (Table 2). In contrast, the smallest sizes
characterized the leaves of tree Nr 4. The leaf
area in tree Nr 4 was 2.5 times smaller than in
tree Nr 1, three times smaller than in tree Nr 2,
and almost two times than in tree Nr 3. Leaves
of all studied Q. robur trees, regardless of the
place of growth, were hypostomatic.
Scanning electron microscopy
Tree Nr 1
The adaxial surface of leaf blades showed
precise contours of the regular epidermal cells
and the absence of stomata and trichomes
(Fig. 2 A). The cells of the upper surface are
small, almost square, or rectangular in shape.
The anticlinal walls are thick, protruding
above the cell surface. The anticlinal and
periclinal walls of the regular epidermal cells
are covered with solitary lamellar and needle-
like waxy structures.
The abaxial epidermis of a leaf is
characterized by the presence of trichomes
and stomata, which are irregularly arranged
(Fig. 2 B, C). The density of stomata is high
– 406 ± 31 stomata per 1 mm2 (Table 2).
Stomatal guard cells are covered with lamellar
crystalline waxy structures, but the stomatal
slit is smooth and free of wax. The surface
of the guard cells of the stomata is covered
with a continuous layer of needle-like wax
structures. The boundaries of the regular
epidermal cells are not visible. The density of
trichomes is low compared to other studied
trees (Table 2). Trichomes are slightly raised,
simple, comma-like, with a drop-shaped base
and elongated head part.
Tree Nr 2
The adaxial surface of the leaf blade has clear
contours of the regular epidermal cells and
has no stomata or trichomes (Fig. 2 D). The
cells of the upper leaf surface are small and
similar in shape to those in the tree Nr 1. The
cells of the upper surface are almost square
or rectangular in shape. The anticlinal walls
are as thick as in the tree Nr 1; they protrude
above the cell surface. The periclinal walls
are depressed. The anticlinal and periclinal
walls of regular epidermal cells are covered
with solitary waxy structures of various
shapes.
The abaxial leaf surface is characterized by
an increased density of trichomes and stomata
Figure 1. Common view of leaf blades from four Quercus robur trees growing in Feofaniya Park, on the
outskirts of Kyiv, Ukraine. Trees Nrs 1–3 grow among other trees in the shade; tree Nr 4 grow separately
from other trees without shade.
5 cm
Nr 1 Nr 2 Nr 3
Nr 4
22 Plant Introduction • 97/98
Nedukha et al.
compared to the tree Nr 1 (Fig. 2 E, F; Table 2).
Stomata are slightly elongated. The average
size of stomata guard cells is represented in
Table 2. Guard cells of stomata are covered
with needle-like waxy structures, which are
about 2 µm long. The stomatal slit is smooth
and free of wax. Trichromes are slightly
elevated above the regular epidermal cells.
Trichomes are simple, unbranched, with a
drop-shaped base and a stick-shaped head
part. The sizes of trichomes are represented
in Table 2. The bases of the trichomes are
covered with needle-like crystalline waxy
structures (Fig. 2 F). The surface of the regular
epidermal cells surrounding the stomata is
covered with a continuous layer of needle-like
waxy structures, due to which the boundaries
of the regular epidermal cells are not visible.
Tree Nr 3
The laminar adaxial surface has the same
epidermal cells as in previously described
trees, with relatively wide anticlinal walls
(Fig. 2 G), which protrude above the periclinal
walls. Stomata and trichomes are absent
on this surface. The epidermal cells of the
upper surface are small; most of the cells are
rectangular. The walls are covered with a layer
of convex, rounded-plated wax structures.
The abaxial epidermis is characterized by
the presence of irregularly arranged stomata
and trichomes (Fig. 2 H, I). The density of
stomata and trichomes in the leaves of tree Nr 3
is higher than in trees Nr 1 and Nr 2 (Table 2).
The surface of the guard cells of the stomata
is covered with thin needle-like waxy crystal
structures ranging in size from 1 to 4 µm. The
stomata slit is free of crystals. The surface of
the regular epidermal cells surrounding the
stomata is also covered with crystalline wax
structures. The boundaries of the regular
epidermal cells between the stomata are not
visible. Simple, unbranched trichomes, with a
drop-shaped base and a stick-shaped head are
Parameter Tree Nr 1 Tree Nr 2 Tree Nr 3 Tree Nr 4
Leaf size, cm
Long axis 170 ± 19 210 ± 15 105 ± 8.9 100 ± 7.8 a, b
Short axis (at the level of the second lobe) 110 ± 11 115 ± 10 82 ± 7.5 52 ± 3.9 a, b, c
Leaf area, cm2 104 ± 7.7 134 ± 5.7 74 ± 15.7 38 ± 0.5 a, b, c
Adaxial epidermis
Long axis of regular epidermal cells, µm 30 ± 1.4 32 ± 1.1 30 ± 1.1 33 ± 1.1
Short axis of regular epidermal cell, µm 25 ± 1.1 25 ± 1.2 18 ± 1.6 25 ± 1.2
Width of anticlinal walls, µm 8 ± 0.4 8 ± 0.2 8 ± 1.7 8 ± 0.2
Abaxial epidermis
Stomata
Density, number per 1 mm2 406 ± 21 434 ± 27 470 ± 33 483 ± 47 а, b
Long axis of guard cells, µm 15 ± 1.1 25 ± 1.3 27 ± 1.1 30 ± 1.1
Short axis of guard cells, µm 7 ± 0.3 11 ± 0.5 11 ± 0.4 11 ± 0.3
Trichomes
Density, number per 1 mm2 18 ± 1.9 56 ± 3.9 22 ± 1.3 130 ± 12 a, b, c
Long axis, µm 70 ± 7.9 100 ± 11.0 95 ± 10.9 90 ± 9.7 a
Short axis (at the base), µm 15 ± 1.2 19 ± 1.3 15 ± 1.3 19 ± 1.3
Width of middle elongated part, µm 7 ± 0.2 8 ± 0.5 9 ± 0.4 8 ± 0.4
Table 2. The parameters of sampled Quercus robur leaves. a denotes significant differences between the
parameters in the tree Nr 1 (shaded) from the tree Nr 4 (without shade) (P ≤ 0.05); b denotes significant
differences between the parameters in the tree Nr 2 (shaded) from the tree Nr 4 (without shade) (P ≤ 0.05);
c denotes significant differences between the parameters in the tree Nr 3 (shaded) from the tree Nr 4
(without shade) (P ≤ 0.05).
Plant Introduction • 97/98 23
Phenotypic variability of epidermis and silicon inclusions in the leaves of Quercus robur
Figure 2. SEM images of the leaf epidermis of four studied Quercus robur trees: A–C – tree Nr 1; D–F – tree
Nr 2; G–I – tree Nr 3; J–L – tree Nr 4. The adaxial (A, D, G, J) and abaxial (B, C, E, F, H, I, K, L) surfaces of oak
leaves. Abbreviations: st – stomata; tr – trichrome; w – wax deposits.
B CA
E
H
F
I
D
G
K LJ
w
tr st w st
w tr
st
tr
w
w tr
st
tr
st
st
w
tr
st
tr
tr ww
tr
st
located near the cells of protruding veins and
sporadically occur close to regular epidermal
cells. They are slightly elevated above the
epidermal surface. The base of trichomes is
covered with needle-like crystalline waxy
structures (Fig. 2 I). The sizes of trichomes
are represented in Table 2. The surface of
the regular epidermal cells surrounding the
stomata is covered with a continuous layer
of needle-like waxy structures. Due to the
24 Plant Introduction • 97/98
Nedukha et al.
developed cuticular coating, the boundaries
between the epidermal cells are not visible.
Tree Nr 4
The upper epidermis has no stomata
or trichomes (Fig. 2 J). Some cells are
characterized by clear contours of the
anticlinal walls of the epidermis, while in
other cells, the periclinal walls are located at
the same level as the anticlinal walls, forming
a continuous surface layer. The adaxial
epidermal cells are small and similar in shape
to those in previously discussed trees. They
are almost square or rectangular in shape.
The anticlinal walls of adaxial epidermal cells
are thick and protrude above the surface.
The periclinal walls are depressed. Nearly the
entire surface of the anticlinal walls of the
epidermis is covered with a layer of small waxy
structures of various shapes protruding above
the epidermal surface.
The abaxial surface is characterized by an
increased density of trichomes and stomata
compared to the leaves of other studied
trees grown in the shade (Fig. 2 K, L; Table 2).
Stomata are slightly elongated; the average
size of guard cells is somewhat higher than
in other studied trees. Guard cells of stomata
are covered with needle-like waxy structures;
the stomatal slit is smooth and free of wax.
Trichomes are located above the regular
epidermal cells and along small veins that are
slightly raised. The trichomes are simple and
unbranched, with a spoon-shaped base and
a stick-shaped head. The apical part of the
trichomes is slightly curved. Trichomes have
needle-like crystalline waxy structures at their
bases. The sizes of trichomes are represented
in Table 2. The surface of the regular epidermal
cells surrounding the stomata is also covered
with a continuous layer of needle-like waxy
structures, and therefore the boundaries of
the regular epidermal cells are not visible.
Localization of silicon inclusions
It is shown that silicon inclusions fluoresce
brightly in green in the epidermal cells in
the leaves of investigated Q. robur plants
(Fig. 3 A–C).
Tree Nr 1
In the adaxial epidermis, silicon inclusions
fluorescence was detected in the periclinal
and anticlinal walls of regular epidermal cells
and on the surface of small veins. Silicon
inclusions are densely spaced in the anticlinal
walls, forming almost continuous layers. In
the periclinal walls, individual large silicon
inclusions were visible (Fig. 3 B), or only a
thin layer of amorphous silicon inclusions
was present, which was visible at low
magnifications (Fig. 3 A). The intensity profile
of silicon in the anticlinal and periclinal walls
differed (Table 3). In the abaxial epidermis
of tree Nr 1 leaves, silicon fluorescence was
detected in the guard cells of stomata, in the
cells surrounding the stomata, and at the base
of trichomes (Fig. 3 C). The intensity of the
silicon fluorescence profile was different in
these cells and differed from that of the upper
epidermis cells (Table 3; Fig. 3 D–G).
Tree Nr 2
In the leaves of oak Nr 2, which grew in
the shade at the highest site in Feofaniya,
green silicon fluorescence was detected in
the epidermal cells of the upper and lower
epidermis (Fig. 3 H, I). Silicon fluorescence was
detected in the periclinal and anticlinal walls
of epidermal cells on the adaxial leaf surface.
In the abaxial epidermis, silicon fluorescence
was detected in stomata, cells around stomata,
and trichomes. The intensity of the silicon
profile depended on the leaf surface and the
cell type (Table 3). The highest intensity of
the profile was on the adaxial surface, in the
anticlinal walls of the epidermal cells. The
highest profile intensity was found on the
abaxial surface at the base of trichomes and
the anticlinal walls of the regular epidermal
cells. It was much lower in the periclinal walls
of regular epidermal cells and guard cells of
stomata (Table 3).
Tree Nr 3
Green silicon fluorescence in the epidermal
cells of the upper (Fig. 3 J) and lower epidermis,
similar to the two previous specimens, has
been detected. Silicon fluorescence was
detected in the periclinal and anticlinal walls
of adaxial epidermal cells. In the abaxial
epidermis, silicon fluorescence was detected
in stomata, stomatal surrounding cells, and
at the base of trichomes. The intensity of the
silicon profile differed in the studied cells of
the upper and lower epidermal leaf surfaces
(Table 3). The high intensity of the profile was
Plant Introduction • 97/98 25
Phenotypic variability of epidermis and silicon inclusions in the leaves of Quercus robur
Figure 3. Fluorescence of silicon inclusions visualized with confocal laser scanning microscopy for the
adaxial (A, B, D, E, H, J, K, L) and abaxial (C, F, G, I, M) leaf surfaces in Quercus robur trees from Feofaniya,
Kyiv. A–J – trees grown in the group, in the shade (trees Nrs 1–3); K–M – a tree grown separately, in the sun
(tree Nr 4). D′–G′, L′, and M′ – histograms of the intensity profile of silicon (green line) resulted from D–G, L,
and M, respectively, where the scanned direction is shown as a white arrow. Abbreviations: st – stomata;
tr – trichrome; incl – inclusions of Si in the periclinal wall.
50 µm
incl st
A B C
D
F
E
G
H I J K
L M
D’ E’
F’ G’
L’ M’
tr
26 Plant Introduction • 97/98
Nedukha et al.
on the adaxial surface in the anticlinal walls
of the epidermal cells. The highest profile
intensity on the abaxial surface was in the
anticlinal walls of the regular epidermal cells
and at the base of trichomes.
Tree Nr 4
In the leaves of tree Nr 4 growing under
direct sunlight, green silicon fluorescence
was detected in the epidermal cells of the
upper and lower epidermis (Fig. 3 K–M). On the
adaxial leaf surface, silicon fluorescence was
detected in the periclinal and anticlinal walls
of epidermal cells. In the abaxial epidermis,
silicon fluorescence was detected in stomata,
stomatal surrounding cells, and trichomes.
The intensity of the silicon profile depended
on the leaf surface and the cell type (Table 3;
Fig. 3 L, M). The intensity of the silicon
profile on the adaxial surface in the anticlinal
walls of the epidermal cells was nearly twice
higher compared to the periclinal walls. On
the abaxial surface, the profile intensity was
relatively high in all studied cells and highest
in the anticlinal and periclinal walls of the
regular epidermal cells and the guard cells of
the stomata (Table 3).
Discussion
Leaf micromorphology
The results obtained in this study indicate that
the oak growing separately from other trees
(without shade) had significantly smaller leaf
sizes and, respectively, leaf areas than the oaks
growing in groups and surrounded by other
trees (in shade). Obtained results regarding
the effect of light on leaf size are consistent
with the results of studies conducted on
other plant species (Terashima et al., 2006;
Wu et al., 2017). Thus, Granier & Tardieu
(1999) studied the effect of illumination on the
growth of sunflower leaves and demonstrated
that cell division and elongation directly
depend on the illumination intensity. Granier
& Tardieu (1999) proved that the cell division
rate and elongation decreased with increased
illumination.
The leaf is the most flexible organ
responding to environmental conditions
(Nevo et al., 2013). Its structure reflects the
environmental influence more clearly than
the stem and root. Smaller leaf sizes result in
less water loss, particularly from the adaxial
surface. Such phenomenon has been described
for leaves of Olea europaea L. trees growing
in hot and dry conditions (Bacelar et al.,
2004) and grasses (Liu et al., 2016). As shown
in succulents and mesophytes, minimizing
water loss during drought is achieved by
increasing both the density of vascular
bundles and stomata (Bolhar-Nordenkampf,
1987; Richardson & Berlyn, 2002), thickening
the cuticle and epicuticular wax layer (Leon &
Bukovac, 1978; Liakoura et al., 1999; Richardson
& Berlyn, 2002). Plants usually respond
strongly to shading by producing leaves with
a larger area and less mass per unit area
(Niinemets & Sack, 2006), which results in
Source Tree Nr 1 Tree Nr 2 Tree Nr 3 Tree Nr 4
Adaxial epidermis
Anticlinal wall of regular cells 138 ± 11.0 143 ± 14.0 143 ± 12.0 153 ± 11.0
Periclinal wall of regular cells 62 ± 3.2 56 ± 4.0 61 ± 7.0 82 ± 4.5
Abaxial epidermis
Anticlinal wall of regular cells 100 ± 12.0 100 ± 9.3 177 ± 13.0 180 ± 13.0 a, b, c
Periclinal wall of regular cells 45 ± 4.3 40 ± 3.5 77 ± 5.3 170 ± 12.0 a, b, c
Trichomes 155 ± 13.0 130 ± 11.0 222 ± 11.0 192 ± 10.0 a, b
Stomata 106 ± 10.0 67 ± 5.9 152 ± 13.0 138 ± 11.0 a, b, c
Table 3. The intensity profile of silicon inclusions (in relative units) in cell walls of the leaf epidermis of
studied Quercus robur. a denotes significant differences in the parameters in the tree Nr 1 (shaded) from
the tree Nr 4 (without shade) (P ≤ 0.05); b denotes significant differences in the parameters in the tree Nr 2
(shaded) from the tree Nr 4 (without shade) (P ≤ 0.05); c denotes significant differences the parameters in
the tree Nr 3 (shaded) from the tree Nr 4 (without shade) (P ≤ 0.05).
Plant Introduction • 97/98 27
Phenotypic variability of epidermis and silicon inclusions in the leaves of Quercus robur
more effective light capture per unit mass. The
leaves of trees growing in more sunny areas, in
addition to their smaller size, are characterized
by increased mechanical strength and impact
force (Sanson et al., 2001; Onoda et al., 2008)
compared to shaded ones.
In the leaves of the oak trees we studied,
stomata are located on the abaxial side
(hypostomate leaf type). Using the scanning
electron microscopy method, we found both
common structural features of stomata and
apparent differences in their density. In
particular, an oak tree Nr 4, growing openly
near a lake in a lowland (without shade), showed
increased stomatal density compared to the
leaves of other oaks (Nrs 1–3) that grew in semi-
shaded conditions. It is known that stomatal
density can be influenced by several factors,
including changes in plant water balance
and soil moisture, as well as the intensity of
sunlight (Hetherington & Woodward, 2003).
Leaves of plants growing under soil drought
conditions usually have smaller and more
numerous stomata than leaves developing
under well-moisturized conditions (Larcher,
2003). The effects of direct sunlight and
shading on stomatal density and function have
been described by many researchers (Bolhar-
Nordenkampf, 1987; Onwueme & Johnston,
2000; Hansen et al., 2007; Matos et al., 2009).
Kardiman & Ræbild (2018) investigated 11
species of trees in tropical forests and showed
a certain correlation between the density of
stomata in their leaves and the intensity of
tree illumination: comparing the leaves of
trees growing in full sunlight with the leaves of
trees growing in 70 % shade. Their assessment
of stomatal density and size and working
maximum stomatal conductance showed that
the anatomical parameters of stomata and gas
exchange differed between species. Shading
significantly affected the size and density
of stomata and the rate of their opening.
The researchers suggest that the change
in stomatal micromorphology is, to some
extent, due to the biochemistry of stomatal
functioning in response to light conditions, in
particular, changes in the activity of enzymes
responsible for creating and maintaining a
high level of osmotic potential (Raven, 2014).
Early studies also revealed that soil moisture
affects the morphological characteristics of
tree stomata; specifically, during drought,
plants were characterized by an increase in the
density of stomata, which were characterized
by small sizes compared to leaves of plants
developing under well-moistured conditions,
which had few large stomata (Larcher, 1960,
2003).
Taking into account the above literature
data and our data on differences in stomatal
density in the four studied oak trees, we
can suggest that not only the increased
illumination around the unshaded oak tree Nr 4
but also changes in soil moisture, also affects
stomatal formation and flexible regulation
of leaf water balance in the studied oak
samples. High air temperatures can damage
pigments, cytochromes, and membrane
proteins (Vatnick & Bruce, 2004; Bashir, 2022).
Stomatal transpiration may help oaks regulate
the temperature on the leaf surface, cooling it
and allowing normal physiological functioning.
It is the high illumination of plants, including
the studied oaks, that promotes optimal
photochemical activity and, consequently,
activates gas exchange, which is due to the
increased density of stomata in trees growing
in direct sunlight.
When studying the ultrastructure of leaf
samples from four oaks, we found the presence
of simple needle-like trichomes with a pointed
apex and an expanded spoon-shaped base
on the abaxial surface of the leaves. Similar
localization of trichomes has been described
for many other oaks, particularly Quercus
laevis Walter and Q. rubra L. (Coder, 2010).
Simple, unbranched trichomes characterize
the leaves of many tree species, including
Quercus (Hardin, 1976; Llamas et al., 1995;
Nicolić et al., 2003; Leandro et al., 2016). We
also found a significant difference in the
density of trichomes in the studied oaks
depending on the growing conditions. The
highest density of trichomes was in the leaves
of oak Nr 4, which grew in direct sunlight
rather than in the trees in the shade. The
increase in the density of trichomes in the
leaves of tree Nr 4 may be mediated by their
function since trichomes protect the leaf from
environmental influences.
As a plant defense barrier, trichomes
counteract ultraviolet light, irradiation,
pathogen attacks, and excessive transpiration,
playing a pivotal role in plant development
(Werker, 2000) under extreme temperatures
and ultraviolet irradiation (Yamasaki &
Murakami, 2014). Trichome density can
28 Plant Introduction • 97/98
Nedukha et al.
modulate leaf heat balance and light photon
interception and thus affect plant gas
exchange. Trichomes can not only reflect but
also absorb ultraviolet radiation, reducing the
damaging effect of UV-B on photochemical
activity and preventing stomatal clogging.
This is due to the accumulation of phenolic
substances (flavonoids) in the trichomes, which
can effectively absorb UV radiation from 250
to 350 nm (Bickford, 2016). The accumulation
of phenolic substances in trichomes occurs
during the secondary thickening of the leaf
epidermal walls. Phenolic substances are
transferred to the cell walls of trichomes,
where they are diffusely deposited, providing
protection against UV-B radiation and acting
as optical filters, screening out wavelengths
that can damage sensitive tissues. Protection
from strong irradiation is also provided by
the increased light reflectance of the surface
(LoPresti, 2015; Karabourniotis et al., 2020).
Considering the above literature data on the
functional importance of trichomes in tree
leaves, including oaks, and our data, we can
assume that the trichomes of the oak samples
we studied can also accumulate or synthesize
flavonoids. This question remains open and
requires further cytochemical investigation.
Regarding the changes in the density of
trichomes in the leaves of the oaks we studied,
we conclude that the trichome density is
a typical sign of the structural plasticity of
leaves, which changes to optimize the water
balance of the plant and the species’ resistance
to environmental changes (light intensity and/
or changes in soil moisture).
Ultrastructural analysis of the epidermis of
oak leaves growing in the Kyiv area showed
that the abaxial epidermis is characterized by
a large number of waxy inclusions that cover
both the guard cells of stomata and the walls of
regular epidermal cells in a continuous layer.
It is known that wax, formed in the periclinal
walls of the epidermis, inhibits transpiration
and reflects ultraviolet radiation (Kerstiens,
1996). The presence of wax in the epidermal
cells of leaves is inherent in many plants,
including tree leaves, which are exposed to
unfavorable environmental conditions (Leon
& Bukovac, 1978; Liakoura et al., 1999; Chaves
et al., 2002; Richardson & Berlyn, 2002; Nevo
et al., 2013). The wax on the cuticle surface
plays an important role in structuring the
surface at the subcellular level, as it can form
crystals that function as the main transport
barrier for water and small water molecules
from the cells, including ions, as well as
reduce the absorption of liquids and various
molecules from the outside (Barlott et al., 2017).
Considering the mentioned literature data and
the results of our studies, we can assume that
wax inclusions on the abaxial surface of four
tested oak specimens are an adaptive feature
protecting against UV irradiation and playing
a positive role in maintaining the optimal
temperature and water balance.
The role of silicon inclusions
Laser confocal microscopy revealed the
presence of silicon inclusions in the cell walls
of the adaxial and abaxial surfaces of the
leaves of four oaks growing on the outskirts
of Kyiv, regardless of their place of growth
and light intensity. Using the Pascal program,
we found an increase in the intensity of the
silicon fluorescence profile in the anticlinal
and periclinal walls of the abaxial surface, as
well as in the trichomes and guard cells of this
surface in oaks (Nrs 3 and 4) that grew under
high sunlight intensity compared to the same
structures of leaves of shaded oaks (trees Nrs 1
and 2).
Silicon inclusions are a natural
form of silicon ions in connection with
polysaccharides, proteins, or lipids (Müller &
Grachev, 2009). In cell walls, silicon is usually
bound to polysaccharides and forms siliceous
inclusions (Lins et al., 2002; Guerriero et al.,
2016; Grašič et al., 2020).
It is known that silicon can improve the
light flux characteristics of both expanded and
contracted leaves. This chemical element also
reduces the heat load due to silica’s effective
far-infrared heat transfer, which provides
a passive mechanism for cooling the leaves
during intense insolation (Wang et al., 2005; Ma
et al., 2011). Silicon can absorb light in a wide
specter (from infrared to ultraviolet), ca. 1017
photons per cm2 per second (Mirshafieyan
& Guo, 2014; Yahaya et al., 2013). It has been
estimated that the ideal absorption and
reflection of light by silicon occurs when the
thickness of silicon inclusions (or structures)
varies from 110 to 140 nm (Hofmeister et al.,
2009).
We observed the increase in fluorescence
of amorphous silicon inclusions up to 150 nm
Plant Introduction • 97/98 29
Phenotypic variability of epidermis and silicon inclusions in the leaves of Quercus robur
in the cell walls of the adaxial epidermis, and
trichomes and closing cells of stomata of the
abaxial epidermis of oak leaves growing in
direct sunlight. It has been established that
such silicon structures in the amorphous state
(not in the crystalline one) absorb light best
(Hofmeister et al., 2009). We hypothesize that
the increase in silicon inclusions fluorescence
in trichomes and stomatal cells of oaks
growing in direct sunlight increases both
the absorption and reflection of sunlight by
epidermal cells to optimize the functioning of
photosynthesis.
Investigations of silicon inclusions are
essential for fundamental and applied
botany, including plant-related medicine
and pharmacology. It is well known that
silicophilous plants containing a high silicon
concentration are used in medicine and
pharmacology. Adding plant silicon to the
human diet promotes calcification and the
repair of damaged bone tissue, while inorganic
silicates do not show such an effect. Among
such silicophilous dietary plants are Inula
helenium L., Crocus sativus L., Gentiana
decumbens L., and Bidens tripartita L. (Aseeva
et al., 1985). Many medicinal plants (i.e., Sedum
hybridum L. and Rhodiola linearifolia Boriss.)
also contain a lot of silicon (Kolesnikov & Gins,
2001). Hence, the use of oak leaves containing
phenolic substances and polyphenol-bounded
silicon is perspective.
Conclusions
It was found that the growth of common oak
(Quercus robur) trees under direct sunlight
(without shading) leads to the appearance of
xeromorphic features: a decrease in the size
of leaf blades, an increase in the density of
trichomes, stomata, and waxy inclusions, as
well as the formation of thickened periclinal
walls of epidermal cells on the adaxial surface
of the leaves. We consider these features to be
signs of phenotypic plasticity in plants, which
are adaptive markers of the effects of sunlight.
The laser confocal microscopy showed that
direct sunlight (without shading) increased the
silicon content in trichomes and guard cells of
stomata. We found that the anticlinal walls of
the adaxial epidermis, trichomes, and stomata
of the abaxial epidermis of leaves are the main
silicon accumulators. We assume that the high
silicon content in oak leaves growing in direct
sunlight (without shading) causes a decrease
in cuticular and stomatal transpiration.
Acknowledgements
The authors are grateful to Dr. O. Polischuk for
help gathering plant samples.
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32 Plant Introduction • 97/98
Nedukha et al.
Фенотипічна мінливість структури епідермісу та кремнієві включення у листках
Quercus robur у парку “Феофанія”
Олена Недуха 1, *, Олена Золотарева 2, Максим Нецветов 3
1 Відділ клітинної біології та анатомії, Інститут ботаніки ім. М.Г. Холодного НАН України,
вул. Терещенківська, 2, Київ, 01004, Україна, * o.nedukha@hotmail.com
2 Відділ мембранології та фітохімії, Інститут ботаніки ім. М.Г. Холодного НАН України,
вул. Терещенківська, 2, Київ, 01004, Україна
3 Відділ фітоекології, Інститут еволюційної екології НАН України, вул. Академіка Лєбєдєва, 37, Київ,
03143, Україна
За допомогою скануючої електронної мікроскопії та лазерної конфокальної мікроскопії досліджено
мікроморфологію листкового епідермісу, а також локалізацію та вміст кремнію в епідермальних
клітинах листків дерев Quercus robur, що зростали у затінку та під прямим сонячним світлом у
парку “Феофанія” (Київ, Україна). В антиклінальних і периклінальних стінках клітин адаксіального
епідермісу, у трихомах, замикаючих клітинах продихів і стінках звичайних клітин епідермісу
абаксіальної поверхні виявлено кремнієві включення, кількість яких варіювала залежно від умов
зростання. Виявлено, що природне затінення та інтенсивність сонячного опромінення впливають
на розмір листкових пластинок, ультраструктуру епідермісу листків та вміст кремнію в листках
дубу. Дослідження показали, що антиклінальні стінки адаксіального епідермісу, а також трихоми
і продихи абаксіального епідермісу листків є основними накопичувачами кремнію. Отримані дані
дозволяють припустити, що зміни мікроструктури листків та вмісту кремнію сприяють підтримці
оптимального водного балансу рослин і можуть розглядатися як ознаки фенотипової пластичності,
а також як адаптивний маркер залежно від умов сонячного освітлення дуба звичайного.
Ключові слова: Quercus robur, мікроморфологія листка, кремній, лазерна конфокальна мікроскопія, скануюча електронна
мікроскопія, вплив затінення
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https://doi.org/10.2525/ecb.52.203
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| id | oai:ojs2.plantintroduction.org:article-1623 |
| institution | Plant Introduction |
| keywords_txt_mv | keywords |
| language | English |
| last_indexed | 2025-07-17T12:54:12Z |
| publishDate | 2023 |
| publisher | M.M. Gryshko National Botanical Garden of the NAS of Ukraine |
| record_format | ojs |
| resource_txt_mv | wwwplantintroductionorg/2f/432a1f24faa8f6ff7db49571fa652e2f.pdf |
| spelling | oai:ojs2.plantintroduction.org:article-16232023-08-26T20:36:09Z Phenotypic variability of epidermis structure and silicon inclusions in the leaves of Quercus robur in the Feofaniya Park Фенотипічна мінливість структури епідермісу та кремнієві включення у листках Quercus robur у парку “Феофанія” Nedukha, Olena Zolotareva, Olena Netsvetov, Maksym The micromorphology of the leaf epidermis, localization, and silicon content in the epidermal cells of Quercus robur leaves growing in the shade and under direct sunlight in the Feofaniya Park (Kyiv, Ukraine) were studied using scanning electron microscopy and laser confocal microscopy. Silicon inclusions were found in the anticlinal and periclinal walls of adaxial epidermal cells, trichomes, guard cells of stomata, and walls of regular epidermal cells on the abaxial leaf surface, the amount of which varied according to the conditions of growth. Natural shading and the intensity of solar irradiation were found affecting the size of leaf blades, the ultrastructure of the leaf epidermis, and changes in the silicon content of oak leaves. Studies have shown that the anticlinal walls of the adaxial epidermis and the trichomes and stomata of the abaxial epidermis of leaves are the main silicon accumulators. The findings suggest that changes in leaf microstructure and silicon content contribute to maintaining optimal water balance in plants and can be regarded as signs of phenotypic plasticity in plants and an adaptive marker depending on the sunlight conditions of oak growth. За допомогою скануючої електронної мікроскопії та лазерної конфокальної мікроскопії досліджено мікроморфологію листкового епідермісу, а також локалізацію та вміст кремнію в епідермальних клітинах листків дерев Quercus robur, що зростали у затінку та під прямим сонячним світлом у парку “Феофанія” (Київ, Україна). В антиклінальних і периклінальних стінках клітин адаксіального епідермісу, у трихомах, замикаючих клітинах продихів і стінках звичайних клітин епідермісу абаксіальної поверхні виявлено кремнієві включення, кількість яких варіювала залежно від умов зростання. Виявлено, що природне затінення та інтенсивність сонячного опромінення впливають на розмір листкових пластинок, ультраструктуру епідермісу листків та вміст кремнію в листках дубу. Дослідження показали, що антиклінальні стінки адаксіального епідермісу, а також трихоми і продихи абаксіального епідермісу листків є основними накопичувачами кремнію. Отримані дані дозволяють припустити, що зміни мікроструктури листків та вмісту кремнію сприяють підтримці оптимального водного балансу рослин і можуть розглядатися як ознаки фенотипової пластичності, а також як адаптивний маркер залежно від умов сонячного освітлення дуба звичайного. M.M. Gryshko National Botanical Garden of the NAS of Ukraine 2023-04-30 Article Article application/pdf https://www.plantintroduction.org/index.php/pi/article/view/1623 10.46341/PI2023001 Plant Introduction; No 97/98 (2023); 18-32 Інтродукція Рослин; № 97/98 (2023); 18-32 2663-290X 1605-6574 en https://www.plantintroduction.org/index.php/pi/article/view/1623/1539 Copyright (c) 2023 Olena Nedukha, Olena Zolotareva, Maksym Netsvetov http://creativecommons.org/licenses/by/4.0 |
| spellingShingle | Nedukha, Olena Zolotareva, Olena Netsvetov, Maksym Фенотипічна мінливість структури епідермісу та кремнієві включення у листках Quercus robur у парку “Феофанія” |
| title | Фенотипічна мінливість структури епідермісу та кремнієві включення у листках Quercus robur у парку “Феофанія” |
| title_alt | Phenotypic variability of epidermis structure and silicon inclusions in the leaves of Quercus robur in the Feofaniya Park |
| title_full | Фенотипічна мінливість структури епідермісу та кремнієві включення у листках Quercus robur у парку “Феофанія” |
| title_fullStr | Фенотипічна мінливість структури епідермісу та кремнієві включення у листках Quercus robur у парку “Феофанія” |
| title_full_unstemmed | Фенотипічна мінливість структури епідермісу та кремнієві включення у листках Quercus robur у парку “Феофанія” |
| title_short | Фенотипічна мінливість структури епідермісу та кремнієві включення у листках Quercus robur у парку “Феофанія” |
| title_sort | фенотипічна мінливість структури епідермісу та кремнієві включення у листках quercus robur у парку “феофанія” |
| url | https://www.plantintroduction.org/index.php/pi/article/view/1623 |
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