Some Aspects of the Relationship between Redox Metabolism and the Structure of Calciphytes

Abstract

Calciphyte species form a systematically and structurally heterogeneous group of plants capable of tolerating highly stressful conditions. Various structural adaptations occur in calciphytes to protect them against excess light (leaf pubescence) and moisture loss (waxy coating). Their shoot structure determines the volume of primary plant production. The present work studied the relationship between the antioxidant status and structural features of some calciphyte species. Redox metabolism in plant leaves was assessed using parameters such as water content, photosynthetic pigments, soluble carbohydrates, water-soluble phenolic compounds, water-soluble and membrane-bound proteins, and lipid peroxidation (LPO) level. The data obtained showed that the contents of the components regulating redox metabolism correlate both with each other and with the structural parameters of plants. In particular, the content of photosynthetic pigments in multi-species communities is lower in taller plants than in low-growing ones. The content of phenolic compounds and the level of LPO in calciphyte leaves are associated with the level of development of wax covering. The plants forming clumps and vigorous shoots exhibit increased LPO activity

Full text

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Journal of Siberian Federal University. Biology 2021 14(3): 370–380
~ ~ ~
DOI 10.17516/1997-1389-0356
УДК 574/577+57.017.3
Some Aspects of the Relationship
between Redox Metabolism
and the Structure of Calciphytes
Elena S. Bogdanovaa*,
Lyudmila M. Kavelenovab, Viktor N. Nesterova,
Oksana A. Kuzovenkob, Resida R. Sarvarovab,
Galina N. Tabalenkovac and Olga A. Rozentsveta
aSamara Federal Research Scientic Center RAS
Institute of Ecology of Volga River Basin RAS
Togliatti, Russian Federation
bSamara National Research University
Samara, Russian Federation
cInstitute of Biology of Komi Scientic Centre
of the Ural Branch of the RAS
Syktyvkar, Russian Federation
Received 14.04.2021, received in revised form 24.08.2021, accepted 02.09.2021
Abstract. Calciphyte species form a systematically and structurally heterogeneous group of plants
capable of tolerating highly stressful conditions. Various structural adaptations occur in calciphytes
to protect them against excess light (leaf pubescence) and moisture loss (waxy coating). Their shoot
structure determines the volume of primary plant production. The present work studied the relationship
between the antioxidant status and structural features of some calciphyte species. Redox metabolism
in plant leaves was assessed using parameters such as water content, photosynthetic pigments, soluble
carbohydrates, water- soluble phenolic compounds, water- soluble and membrane- bound proteins, and lipid
peroxidation (LPO) level. The data obtained showed that the contents of the components regulating redox
metabolism correlate both with each other and with the structural parameters of plants. In particular,
the content of photosynthetic pigments in multi- species communities is lower in taller plants than in
low- growing ones. The content of phenolic compounds and the level of LPO in calciphyte leaves are
associated with the level of development of wax covering. The plants forming clumps and vigorous
shoots exhibit increased LPO activity.
© Siberian Federal University. All rights reserved
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 Internat ional License (CC BY-NC 4.0).
* Corresponding author E-mail address: cornales@mail.ru
ORCID: 0000-0002-2445-1952 (Bogdanova E.S.); 0000-0002-3679-1276 (Kavelenova L.M.); 0000-0002-3590-7097
(Nesterov V.N.); 0000-0003-3177-9590 (Kuzovenko O.A.); 0000-0002-9627-7092 (Sarvarova R.R.); 0000-0001-6312-
3620 (Rozentsvet O.A.)

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Elena S. Bogdanova, Lyudm ila M. Kavelenova… Some Aspect s of the Relationship between Redox Metabolism…
Keywords: calciphytes, redox metabolism, pigments, phenolic compounds, carbohydrates.
Citation: Bogd anova E. S., Kavelenova L. M., Nester ov V. N., Kuzovenko O. A., Sar varova R. R., Tabalenkova G. N.,
Rozentsvet O. A. Some aspects of the relationship between redox metabolism and the structure of calciphytes. J. Sib. Fed.
Univ. Biol., 2021, 14(3), 370–380. DOI: 10.17516/1997-1389-0356
Особенности взаимосвязи редокс- метаболизма
и структуры растений кальцефитов
Е. С. Богдановаа, Л. М. Кавеленоваб,
В. Н. Нестерова, О. А. Кузовенкоб,
Р. Р. Сарвароваб, Г. Н. Табаленковав, О. А. Розенцвета
аСамарский федеральный исследовательский центр РАН,
Институт экологии Волжского бассейна РАН
Российская Федерация, Тольятти
бСамарский национальный исследовательский университет
им. академика С. П. Королева
Российская Федерация, Самара
вИнститут биологии Коми научного центра
Уральского отделения РАН
Российская Федерация, Сыктывкар
Аннотация. Растения кальцефитных флор образуют систематически и структурно неоднородную
группу растений, способных переносить высокострессовые условия. Кальцефиты реализуют
различные структурные адаптации, противодействуя избытку света (опушение), снижая потери
влаги (восковой налет). Структура их побегов определяет объем первичной продукции растений.
Цель настоящей работы – изучить взаимосвязи антиоксидантного статуса со структурными
особенностями некоторых представителей кальцефитной флоры. Редокс- метаболизм оценивали
по оводненности листьев, содержанию фотосинтетических пигментов, углеводов, фенольных
соединений, водорастворимых и мембранно- связанных белков, интенсивности накопления
продуктов перекисного окисления липидов (ПОЛ). Полученные данные показали, что
количественное содержание компонентов, регулирующих редокс-метаболизм, демонстрирует
наличие корреляционных связей как между отдельными группами этих веществ, так
и со структурными показателями растений. В частности, в многовидовых сообществах у более
высоких растений содержание фотосинтетических пигментов ниже, чем у низкорослых.
Содержание фенольных соединений и уровень ПОЛ в листьях кальцефитов связаны с уровнем
развития воскового налета. Растения, формирующие куртины и мощные побеги, характеризуются
повышенной активностью ПОЛ.
Ключевые слова: кальцефиты, редокс- метаболизм, пигменты, фенольные соединения,
углеводы.

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Elena S. Bogdanova, Lyudm ila M. Kavelenova… Some Aspect s of the Relationship between Redox Metabolism…
Цитирование: Богданова, Е. С. Особенности взаимосвязи редокс- метаболизма и структуры растений кальцефитов /
Е. С. Богданова, Л. М. Кавеленова, В. Н. Нестеров, О. А. Кузовенко, Р. Р. Сарварова, Г. Н. Табаленкова, О. А. Розенцвет
// Журн. Сиб. федер. ун- та. Биология, 2021. 14(3). С. 370–380. DOI: 10.17516/1997-1389-0356
Introduction
Calciphyte species form a systematically and
structurally heterogeneous group of plants capable
of tolerating highly stressful conditions (Tyler,
2003; Malysheva, Malakhovsky, 2011). Calciphytes
grow in specic habitats: soils exhibit a high initial
pH value, rockiness, and a special moisture regime
(Escudero et al., 2015). In addition to specic soil
conditions, the plants are constantly exposed
to winds, high air temperatures, and excessive
insolation. Plants of chalk slopes and carbonate
outcrops, as a rule, have a xeromorphic structure
with their characteristic external features such
as pubescence and smaller leaves, which often
develop a silvery sheen (Kurovsky, 2009). They
are represented by different life- forms: dwarf
shrubs, semi- shrubs, root and rhizome perennials,
etc. Low- growing, creeping plants predominate
among calciphytes. The main part of photosynthetic
apparatus can be represented by many small stem-
covering leaves or well- developed root leaf rosettes,
or openwork leaf rosettes (Lambers, Oliveira, 2019).
Thus, the conditions for the growth of
calciphytes are highly stressful, and, therefore,
different structural adaptations occur in the plants.
The physiological adaptations of plants
are based on alterations in cellular processes
resulting in changes of quantitative and qualitative
composition of compounds closely related to
the main metabolic pathways including redox
metabolism. At the same time, redox regulation
of cellular processes is considered as one of
the fundamental mechanisms regulating cell
functional activity (Martinovich, Cherenkevich,
2008). Under adverse environmental conditions,
plants experience oxidative stress due to the
formation of an increased amount of highly reactive
oxygen species (ROS) (Gupta et al., 2018). Lipid
peroxidation (LPO) is one of the redox regulation
factors of enzymatic systems (Hasanuzzaman et
al., 2020).
Under abiotic stresses such as drought,
salinity, heavy metals, waterlogging, extreme
temperatures, oxygen deprivation, etc., the activity
of free- radical processes is also regulated by
non- enzymatic antioxidants. The low molecular
weight organic antioxidants (such as ascorbate,
glutathione, carotenoids, tocopherols, avonoids,
betaines, etc.) sometimes can be more effective
as metabolism protectors from ROS than enzyme
systems. Phenolic compounds are the most common
among them (Hasanuzzaman et al., 2020). They
are broad- range mediators of biotic relationships,
plant metabolism regulators, and participants in
responses to abiotic stresses (D'Amelia et al., 2018).
Recently, sugars have been considered as direct
antioxidants (Bolouri- Moghaddam et al., 2010).
The amount, chemical structure, and mechanism of
action of antioxidants can vary signicantly across
plant species, such as calciphytes (Hasanuzzaman
et al., 2020).
The aim of this work was to study the
relationship between the elements of antioxidant
system and the structural features of some
calciphile plant species.
Materials and methods
Plant material
The study was conducted on 13 species
from 9 families: Artemisia salsoloides Willd,
Anthemis trotzkiana Claus (Asteraceae); Pimpinella
titanophila Woronow, Bupleurum falcatum L.
(Apiaceae); Krascheninnikovia ceratoides (L.)
Gueldenst. (Chenopodiaceae); Onosma volgensis
Dobrocz (Boraginaceae); Gypsophila volgensis
Krasnova (Caryophyllaceae); Astragalus zingeri

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Elena S. Bogdanova, Lyudm ila M. Kavelenova… Some Aspect s of the Relationship between Redox Metabolism…
Korsh., Hedysarum grandiorum Pall. (Fabaceae);
Linum avum L., L. uralense Juz. (Linaceae);
Polygala sibirica L. (Polygalaceae); Reseda lutea
L. (Resedaceae). The plants were growing in the
Shigonsky District of the Samara Region in two
ecotopes: Ecotope 1–53°29′ N, 49°00′ E, and
Ecotope 2–53°35′ N, 48°51′ E.
We took into account such structural
parameters of the species as the height of plants
(average values in cm), the vigor and the position
of their shoots, the presence/absence of clumps
and rosettes, and the comparative levels of
leaf pubescence and wax coating (Ryabinina,
Knyazev, 2009; Maevsky, 2014).
For biochemical analyzes, we used freshly
cut leaves collected from 12–15 plants. Three
independent biological samples, 0.2–2.0 g of wet
weight, were prepared from the total mass and
stored in liquid nitrogen until laboratory studies.
The water content of the tissues was
calculated after determining the wet and air- dry
weight and expressed as %.
Biochemical analyses
The lipid peroxidation rate in leaves of plants
was determined by measuring the accumulation
of malonyldialdehyde (MDA), determined using
the color reaction with thiobarbituric acid at λ =
532 nm (Lukatkin, Golovanova, 1988).
The content of photosynthetic pigments
was determined spectrophotometrically in an
acetone extract (90 %) at λ = 662, 645, and 470
nm. The concentration of chlorophylls a, b and
carotenoids was calculated using the method of
H. K. Lichtenthaler (1987).
The water- soluble phenolic substances
were extracted from air- dry plant material, their
content was determined in aqueous extracts
using the Folin- Chocalteu reagent according
to the method (Swain, Hillis, 1959) in the drop
modication proposed by the manufacturer
of the Pancreac Quimica reagent, Spain. The
absorbance of the solutions was determined on a
photocolorimeter («KFK-2», Russia) using a red
light lter at λ = 725–730 nm. Gallic acid was
used to make a calibration graph.
The amounts of water- soluble proteins and
membrane- bound proteins were determined by
the O. N. Lowry method (Lowry et al., 1951) on
a spectrophotometer (PromEcoLab PE-3000,
Russia) at λ = 750 nm, using calibration curves
with a standard solution of bovine serum albumin
(Calbiochem, Germany) in distilled water and in
a 0.05 % Triton solution X-100, respectively.
The content of soluble carbohydrates was
determined in freeze- dried material. The weighed
portion (0.3 g) was extracted by 70 % ethanol;
the evaporated hydroalcoholic extract of the plant
sample was dissolved in water and subjected to
purication by solid- phase extraction method
in cartridges with sorbents Disorb-60-S16T
and Diasorb-60-Amine. After the purication,
the solution was analyzed under the following
conditions: column Kromasil 4.6 х 250 mm
100–5NH2 was used, the rate of eluent ow was
0.94 mL min –1, and a refractometer served as a
detector. The retention time of control substances
served as the criterion of peak identication.
Quantitative analysis was performed by absolute
calibration method using peak areas as a
reference.
Statistical analysis
The results of biochemical analyzes were
presented as the average of three biological and
three analytical replicates. The data obtained
were presented in the form of arithmetic means
(M), and the scattering of values was presented
as standard errors (± SE). Comparison of
quantitative data was carried out using one- way
analysis of variance (One- way ANOVA) (p <
0.05) followed by the Tukey's test to compare the
means. Calculations were performed using the
Statistica 6.0 for Windows and Past 3 software.

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Elena S. Bogdanova, Lyudm ila M. Kavelenova… Some Aspect s of the Relationship between Redox Metabolism…
For an expert assessment, the species were
assigned conditional scoring characteristics,
which were entered into the data matrix and,
together with biochemical indicators, were used
to calculate the pair correlation coefcients in the
Microsoft Excel (Zaitsev, 1984).
Results and discussion
The typical structural and morphological
traits of the aboveground organs of the species
studied in this work are presented in Table 1.
According to the literature data, plants differ
in both habit and characteristics of leaves. Low
(20–40 cm) and medium- sized (50–60 cm) plants
predominate among the species studied here, but
one species, the subshrub K. ceratoides, forms
vigorous leafy shoots up to 1 m in height and
more. Most of the plants have shoots rising above
the surface of the soil substrate. In four species,
the main apparatus of photosynthesis is well-
developed near- root leaf rosettes, and two species
have openwork leaf rosettes. The other species are
characterized by a relatively weak development
of the leaf surface; they form thin branched
shoots. The species also differ signicantly in the
pubescence of leaves and stems and the thickness
of the wax coating.
Redox metabolism in plant leaves was
assessed using parameters such as water content,
photosynthetic pigments, soluble carbohydrates,
water- soluble phenolic compounds, water- soluble
and membrane- bound proteins, and MDA level
(Table 2). The content of MDA, one of the nal
products of lipid oxidation, varied within wide
limits depending on the plant species (0.1–1.7
mmol g-1 dry weight). Calciphytes grow in
water- limited soil conditions, and, therefore, it is
import ant for them to maintai n water homeostasis.
Our results showed that the water content of the
leaves was 51.1–78.4 % of dry weight, which
corresponds to the values of xerophytic plants
(Table 2). The largest water decit was found in
O. volgensis, K. ceratoides and A. zingeri plants.
The water content in their leaves was 1.2 times
lower than in most of the species studied.
The content of photosynthetic pigments
in leaves is considered as an indicator of the
physiological state of plants, which characterizes
the efciency of the photosynthetic apparatus.
The concentration of chlorophylls varied from
2.4 to 6.3 mg g-1 and carotenoids from 0.4 to
1.2 mg g-1 of dry weight. Plants L. avum, P.
sibirica, and R. lutea had high pigment contents.
The calciphytes studied in the present work were
heliophytes. They exhibited a high chlorophylls
a/b ratio. This parameter varied in the range of
2.4– 4.1.
The carbohydrates synthesized by plants in
the photosynthesis process are the initial material
for plastic and energy metabolism. In addition,
they are known to have antioxidant properties
and the ability to maintain the water balance of
cells (Zakhozhiy et al., 2019). The total content
of soluble carbohydrates in the dry mass of
leaves varied from 14.9 to 78.0 mg g-1 (Table 2).
Most of the calciphyte species demonstrated the
predominance of disaccharides. The lowest
concentration of sugars was found in the leaves
of H. grandiorum, which was mainly due to the
low content of disaccharides. These plant species
are able to slow down or speed up metabolic
processes depending on external conditions
(Ilyina, 2019). One can assume that the low
sugar content compared to other species is a
consequence of these processes.
The evaluation of protein components
showed that the amount of membrane- bound
proteins ranged from 6.8 to 81.0 mg g-1 and
water- soluble ones – from 12.9 to 267.6 mg g-1
dry weight. Moreover, the content of water-
soluble proteins may be 1.2–8.0 times greater
than the content of the membrane- bound
ones. The largest amount of membrane- bound
proteins was found in the leaves of B. falcatum,

Table1. Life- forms and morphometric parameters of calciphytes
Species Life- form Shoot height, cm Vigor of shoots
Position of
shoots relative to
the surface of the
substrate
Formation of
dense aerial
shoots*
The presence of a
root leaf outlet*
The degree
of leaf
pubescence**
The degree of the
waxy coating of
leaves**
A. trotzk iana SS Up to 25 cm Medium CP ++(openwork) ++ -
A. salsoloides SS Up to 50 cm High RP +- - ++
A. zingeri SS Up to 50cm Medium CP + + +++ -
B. falcatum PP Up to 60 cm Low RP -+(openwork) -+
G. volgensis PP Up to 90 cm Low RP - - - +
H. grandiorum PP Up to 50 cm Medium RP + + ++ -
K. ceratoides SS 1 m and more High RP +-++ -
L. avum PP Up to 40 cm Medium RP +- - +
L. uralense PP Up to 20 cm Low RP + + -+
O. volgensis PP Up to 50 cm High CP +-+++ -
P. titanophila SS Up to 40 cm Low RP -+++ -
P. sibirica PP Up to 20 cm Low RP +-+-
R. lutea PP Up to 60 cm High RP - - - +
Note: SS – semi- shrubs; PP – perennial plants; CP – creeping plants; RP – raised plants. Expert characteristics criteria for some morphological features of plants: *absence (–) or presence (+);
**absence (–); minimal (+), medium (++), maximal (+++) levels.

Table 2. Physiological and biochemical parameters of calciphyte leaves
Species
MDA ,
mmol g-1 dry
weigh
Water
content, %
Total
chlorophylls Carotenoids Chlorophyll
а/bMonosaccharides Disaccharides Water- soluble
proteins
Membrane-
bound
proteins
Phenolic
compound
mg g-1 dry weight
Ecotope 1
A. salsoloides 1.7± 0. 5a 64.8±1.4bc 2.8±0.2d 0.6±0.1c 2.5 40.4±2.1a 19.3± 0. 5c 26 7.6±11. 3a 37.5±3.4c 132.5 ±7.0 a
A. trotzk iana 0.2±0.1b 70.1±2 .3b 2.4± 0.3d 0.4±0.0d 2.4 32.5±2.6b 40.2±2.5a 84.9±4.5e 14.7±2. 0e 25.9±2.3e
P. titanophila 0.4±0.1b 64.8±2.0b 3.5±0.4c 0.7±0.0c 2.9 2 9.7±1. 3b 23.1±2.0b 144 .6±12.5c 22 .7±1.9d 60.0±3.0b
K. ceratoides 0.2 ±0.1b 57.7±1.0d 3.8 ± 0.1c 0.7±0.0c 3.8 7.6 ±1.7d 11.6 ±1.5e 153.7±12 .4c 42.1±1.4 c 48.4±2 .1c
O. volgensis 0.3±0.1b 51.1±1.1e 3.8±0.2c 0.6±0.1c 2.8 14.0±1.3 c 24.6±1.3b 69.5±1.9f 10.2 ±2.0f 37.3± 3.0d
G. volgensis 0.1±0.0c 67.5±2.7b 2.7± 0.1d 0.5±0.1cd 3.2 1.2±0.1f 25.0 ±1.4b 80.3 ±1.8e 15.1±1. 0e 26.4 ±1.0e
L. uralense 0.3±0.1b 66 .0 ±1. 6b 3.5± 0.3c 0.6±0.1c 2.9 – – 12.9 ±1.2h 6 .8±1.0g –
Ecotope 2
A. zingeri 0.4±0.1b 57.6 ± 2 .0d 4.4±0.3b 0.9±0.1b 3.0 4.8±0.3d 15.6 ±1.0d 122.9±12.0d 17.7 ±1.1e 47. 6 ±2.2 c
B. falcatum 0.4±0.1b 62.6±3.0bc 4.6±0.3b 0.9±0.1b 4.1 – – 184.0±15.6b 81.0±3.0a 51.9±2.5c
H. grandiorum 0.5±0.2b 62.0±2.1c 4.9±0.3b 0.9±0.1b 3.1 5.0±1.0d 9.9±0.9e 120.0±11.0d 15.0±1.5e 26.5±2.5e
G. volgensis 0.1±0.0c 67.5±3.5b 2.7±0 .2d 0.6±0.1c 2.9 3.4±0.3e 21.7±1.6b 11 2.3± 9.0 d 24.3±2.0d 57.0±3.6b
L. avum 0.4±0.1b 78.2±4.0a 6.3±0.4a 0.9±0.2ab 2.9 32.1±2.0b 45.9±3.0a 81.2±2.5e 57.8±3.0b 27.5±2.1e
K. ceratoides 0.5±0.2b 53.1± 2. 0e 2.6±0.3d 0.6±0.1c 3.3 – – 136.9 ±13.8c d 56.9±3.6b 17.5±2.0f
P. sibirica 0.1±0.0c 62.4±2.4c 5.4±0.5b 1.2±0.1a 2.9 – – 44.1±1.2g 34.3±6.0c 27.4 ± 2 .6e
R. lutea 0.4±0.2b 78.4± 3.0a 5.1±0 .3b 0.8±0.1bc 2.9 38.5±2.1a 26.6±2.3b 115.7 ±10 .4d 17.6 ± 2 . 3e 54.9±2.4b
Note: data are mean ± SE (n = 9). Different letters indicate signicant differences at the level of p < 0.05.

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Elena S. Bogdanova, Lyudm ila M. Kavelenova… Some Aspect s of the Relationship between Redox Metabolism…
and water- soluble proteins were the highest in
A. salsoloides. It is well- known that individual
components of water- soluble proteins are
responsible for protection against oxidative
stress (Orlova et al., 2007).
Plant polyphenols have pronounced
antioxidant and antiradical properties. Due to
the antioxidant effect, phenolic compounds with
the combined action of the antioxidant system
are able to «quench» free radicals, stabilize and
protect cell membranes from damage, prevent
the autolysis of lysosomes, mitochondria, etc.
(Martinovich, Cherenkevich, 2008; Gupta et al.,
2018; Zagoskina, Nazarenko, 2016). The content
of phenolic compounds, as well as proteins and
carbohydrates, which are also involved in the
redox metabolism, varied widely across the plant
species (17.5–132.5 mg g-1 dry weight). In two
species used as an example – K. ceratoides and
G. volgensis – the content of phenolic compounds
depends not only on the species traits but also on
the growing conditions. Thus, in the leaves of
both species, sampled in different ecotopes, the
content of phenolic compounds differed by more
than a factor of two.
The content analysis of primary and
secondary metabolism components, including
those involved in the regulation of redox
metabolism, shows that their amounts vary
signicantly in different calciphyte species.
We used the correlation analysis method to
identify the possible relationship between some
str uctural tr aits and physiological and biochemical
parameters. To this purpose, the primary expert
assessment of structural features was fullled.
The plants were assigned quantitative estimates:
heights (average values in cm), the relative
degree of development of aerial shoots (from 1
to 10 points), the presence or absence of clumps
(0–1 points), the presence of outlets (absence –
openwork rosettes – well- developed rosettes,
from 1 to 3 points), the presence and degree of
development of pubescence (from 0 to 3 points),
the presence and degree of development of wax
coating (from 0 to 2 points), the position of the
shoots (creeping over the substrate or rising
above it (1 and 2 points). Table 3 presents the
results of the analysis of relationships between
the metabolic parameters and structural traits
of the calciphytes studied. Both positive and
negative correlations were found.
A high positive pair correlation was found
between photosynthetic pigment contents –
chlorophyll a/chlorophyll b, chlorophyll a/
carotenoids, chlorophyll b/carotenoids (r =
0.91; 0.86; 0.78, respectively). Similarly, a high
positive correlation was found between the MDA
level/the content of water- soluble proteins, the
MDA level/the content of phenolic compounds
(r = 0.77 and 0.79, respectively). That means
that under stressful conditions, all antioxidant
components are activated, contributing to
the development of adaptive plant responses.
The accumulation of water- soluble phenolic
compounds in leaves of calciphytes correlated
with the level of development of wax coating on
the vegetative parts of the shoots (r = 0.67), and
an average positive level of correlation between
the development of wax coating and MDA level
(r = 0.52) was also revealed.
It is well- known that under water decient
conditions, wax coating on the surface of plant
leaves not only contributes to the regulation of
the water balance, but also, unlike pubescence,
better reects sunlight, thereby protecting the
assimilation organs of plants from ultraviolet
radiation and burns (Lambers, Oliveira, 2019).
The plant height expressed in conditional
points negatively correlated with the content of
photosynthetic pigments (r values from –0.36
to –0.59), which is quite consistent with the
level of light exposure of plants with different
shoot heights in multispecies communities – the
maximal for the highest and more limited for the

Table 3. Paired correlation coefcients of biochemical and structural parameters of calciphytes
Parameters Dry mass Monosac-
charides
Disac-
charides
Phenolic
compounds
Chlorophyll
а
Chlorophyll
bCarotenoids
Water-
soluble
proteins
Membrane-
bound
proteins
MDA
Dry mass 1.00
Monosaccharides -0.55* 1.00
Disaccharides -0.64** 0.54* 1.0 0
Phenolic compounds -0.08 0.44 -0.28 1.0 0
Chlorophyll а-0.25 0.14 0.11 -0.20 1.00
Chlorophyll b -0.36 0.37 0.25 -0.07 0.91*** 1.00
Carotenoids -0.03 -0.06 -0.23 -0.13 0.86*** 0.78*** 1.00
Water- soluble proteins 0.12 0.35 -0.44 0.82*** -0.15 -0.20 -0.07 1.0 0
Membrane- bound proteins 0.03 0. 31 0.28 0.05 0.33 0.09 0.33 0.46 1.00
MDA 0.01 0.53* 0 .15 0.79*** - 0.11 0.05 -0.09 0.77*** 0.23 1.0 0
Plant height 0.14 - 0. 54* - 0.32 -0 .12 -0.40 -0.59* -0.36 0.34 0.31 - 0 .11
Vigor of shoots 0.32 0.26 -0.23 0 .19 -0.24 -0.13 - 0.35 0 .12 -0.25 0.40
Clumps 0. 32 0.12 -0.36 0.13 - 0.18 -0.09 -0.30 0 .11 - 0.36 0. 36
Rosettes -0.09 -0.45 - 0 .11 - 0.22 0.14 0.08 0.16 0.03 -0.10 - 0.15
Leaf pubescence 0. 57* -0.25 -0.24 -0.27 - 0.01 0.04 0.03 - 0.12 -0.39 - 0.15
Waxy coating of leaves -0.38 0.26 0.09 0.67** -0.08 - 0.03 -0.07 0.36 0.28 0.52*
Shoot position -0.52* 0 .31 0.17 0.05 -0.06 -0.11 -0.05 0.13 0. 31 0.07
Note: The average level of correlation (│0.3 < r < 0.6│) is indicated by bold font and light gray color; high (│r > 0.6│) – by bold font and dark gray; *The reliability of the correlation coefcient at a
condence level of 0.95 for a sample size of 15 pairs of values (species) corresponds to the values of the correlation coefcient of 0.51 and higher; **At a condence level of 0.99 – the correlation
coefcient is 0.63 and higher; ***At a condence level of 0.999 – the correlation coefcient of 0.75 and higher.

– 379 –
Elena S. Bogdanova, Lyudm ila M. Kavelenova… Some Aspect s of the Relationship between Redox Metabolism…
undersized. At the level of an average positive
relationship, an increase in lipid peroxidation
was observed in plants that had more vigorous
shoots and formed clumps of shoots (r = 0.40 and
0.36, respectively), which is logically associated
with the successful development of species
that form a signicant amount of phytomass
of densely leaved shoots in ecologically harsh
habitats.
Multiple connections of medium strength,
both positive and negative, were found for a
number of monosacchar ides as a group of primary
metabolites. The level of their accumulation was
associated wit h the activity of metabolic processe s
(water soluble proteins) and tissue antioxidant
status (MDA). There was a tendency towards a
decrease in the number of monosaccharides in
plants with an increase in their height (r = –0.54)
or the formation of basal rosettes (r = –0.45).
Conclusion
The data obtained showed that the
quantitative level of the elements of the redox
system correlates both with each other and with
the structural parameters of calciphytes. In
particular, the content of photosynthetic pigments
in multi- species communities in taller plants is
lower than in low- growing ones. The content of
phenolic compounds and the level of MDA in
calciphyte leaves is associated with the level of
development of wax covering. In ecologically
harsh habitats, plants forming clumps and
vigorous shoots are characterized by increased
LP O a ctivit y.
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