Біохімічні та алелопатичні особливості Adonis vernalis, Allium ursinum та Leucojum vernum у Національному ботанічному саду імені М.М. Гришка НАН України
The article presents the results of a study on the content and dynamics of the accumulation of biogenic elements and brassinolides in plants of Adonis vernalis, Allium ursinum, and Leucojum vernum in Kyiv, Ukraine. Data is provided on allelopathic activity, content of macro- and microelements, pheno...
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M.M. Gryshko National Botanical Garden of the NAS of Ukraine
2024
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| author | Zaіmenko, Natalia Gnatiuk, Alla Gritsenko, Victoria Zakrasov, Oleksandr Pavliuchenko, Nataliia Kharytonova, Iryna Dziuba, Oksana Didyk, Nataliya Yunosheva, Olena Blum, Oleg Likhanov, Artur Holichenko, Nataliia |
| author_facet | Zaіmenko, Natalia Gnatiuk, Alla Gritsenko, Victoria Zakrasov, Oleksandr Pavliuchenko, Nataliia Kharytonova, Iryna Dziuba, Oksana Didyk, Nataliya Yunosheva, Olena Blum, Oleg Likhanov, Artur Holichenko, Nataliia |
| author_sort | Zaіmenko, Natalia |
| baseUrl_str | https://www.plantintroduction.org/index.php/pi/oai |
| collection | OJS |
| datestamp_date | 2026-03-05T18:42:33Z |
| description | The article presents the results of a study on the content and dynamics of the accumulation of biogenic elements and brassinolides in plants of Adonis vernalis, Allium ursinum, and Leucojum vernum in Kyiv, Ukraine. Data is provided on allelopathic activity, content of macro- and microelements, phenolic compounds, and laccase activity in plants and the rhizosphere soil under the conditions of the M.M. Gryshko National Botanical Garden of the National Academy of Sciences of Ukraine (NBG). The plants from the collection of the NBG were used as objects of study in field experiments. The content of biogenic elements in plant tissues and soil was analyzed using an inductively coupled plasma spectrometer. The allelopathic analysis of soil was conducted using a direct bioassay method with Lepidium sativum seedlings as the test object. Phenolic compounds were extracted from the soil using the ion exchange (desorption) method. The content of brassinosteroids was measured spectrophotometrically at a wavelength of 450 nm. The content of laccase was measured spectrophotometrically at a wavelength of 530 nm.The results demonstrate that model plant species employ a wide range of physiological mechanisms throughout the vegetation period to enhance their resistance to abiotic factors. These mechanisms include maintaining potassium and calcium balance and utilizing hormonal compounds. Plants have been proven to have compensatory mechanisms in response to stress factors, substituting one biochemical marker of resistance with another. Both, brassinosteroids and silicon, contribute to the adaptive capacity of organisms. |
| doi_str_mv | 10.46341/PI2023011 |
| first_indexed | 2025-07-17T12:54:17Z |
| format | Article |
| fulltext |
Plant Introduction, 101/102, 3–18 (2024)
© The Authors. This content is provided under CC BY 4.0 license.
RESEARCH ARTICLE
Biochemical and allelopathic features of Adonis vernalis, Allium ursinum,
and Leucojum vernum in the M.M. Gryshko National Botanical Garden of
the NAS of Ukraine
Natalia Zaіmenko 1, Alla Gnatiuk 1, *, Victoria Gritsenko 1, Oleksandr Zakrasov 1,
Nataliia Pavliuchenko 1, Iryna Kharytonova 1, Oksana Dziuba 1, Nataliya Didyk 1,
Olena Yunosheva 1, Oleg Blum 1, Artur Likhanov 2, Nataliia Holichenko 3
1 M.M. Gryshko National Botanical Garden, National Academy of Sciences of Ukraine, Sadovo-Botanichna str. 1, 01014 Kyiv, Ukraine;
* gnatiukalla@gmail.com
2 National University of Life and Environmental Sciences of Ukraine, Heroyiv Oborony str. 15, 03041 Kyiv, Ukraine
3 Ukrainian Institute for Plant Variety Examination, Henerala Rodymtseva str. 15, 03041 Kyiv, Ukraine
Received: 21.11.2023 | Accepted: 07.02.2024 | Published online: 17.02.2024
Abstract
The article presents the results of a study on the content and dynamics of the accumulation of biogenic
elements and brassinolides in plants of Adonis vernalis, Allium ursinum, and Leucojum vernum in Kyiv, Ukraine.
Data is provided on allelopathic activity, content of macro- and microelements, phenolic compounds, and
laccase activity in plants and the rhizosphere soil under the conditions of the M.M. Gryshko National
Botanical Garden of the National Academy of Sciences of Ukraine (NBG). The plants from the collection
of the NBG were used as objects of study in field experiments. The content of biogenic elements in
plant tissues and soil was analyzed using an inductively coupled plasma spectrometer. The allelopathic
analysis of soil was conducted using a direct bioassay method with Lepidium sativum seedlings as the test
object. Phenolic compounds were extracted from the soil using the ion exchange (desorption) method.
The content of brassinosteroids was measured spectrophotometrically at a wavelength of 450 nm. The
content of laccase was measured spectrophotometrically at a wavelength of 530 nm.
The results demonstrate that model plant species employ a wide range of physiological mechanisms
throughout the vegetation period to enhance their resistance to abiotic factors. These mechanisms include
maintaining potassium and calcium balance and utilizing hormonal compounds. Plants have been proven
to have compensatory mechanisms in response to stress factors, substituting one biochemical marker of
resistance with another. Both, brassinosteroids and silicon, contribute to the adaptive capacity of organisms.
Keywords: biogenic elements, phenolic compounds, laccase, brassinolides, plant adaptation, phytohormones
https://doi.org/10.46341/PI2023011
UDC 574.24 + 581.19 : 581.524.13 + 58.006 (477)
Authors’ contributions: Nataliia Zaimenko developed the research concept, designed the experiments, wrote, revised and proved
the manuscript, analyzed literary sources, and interpreted the experimental data results. Gnatiuk A. and Gritsenko V. grew plants
(objects of study), collected and delivered samples for experiments. Zakrasov O., Dziuba O., Pavliuchenko N., Kharytonova I.,
Didyk N., Yunosheva O., Blum O., Likhanov A., and Holichenko N. were engaged in the preparation and conduct of the analyzes,
writing methodological part of the research, interpreted the results and presented the results of experiments, created figures аnd
tables. Zakrasov O. realized statistical data processing. Blum O., Gritsenko V. revised and redacted the text. Gnatiuk A. coordinated
the writing of the manuscript, combined experimental data, and prepared the manuscript for publishing. All authors approved the
manuscript for publication.
Funding: This research was supported by the target program of scientific research “The Role of Biogenic Elements in Inducing
Brassinosteroid Synthesis for Enhancing Plant Resistance to Stress Factors” for 2021–2022.
Competing Interests: Authors declared that they have no conflict of interest.
https://creativecommons.org/licenses/by/4.0/
https://orcid.org/0000-0003-2379-1223
https://orcid.org/0000-0001-5001-971X
https://orcid.org/0000-0002-1783-6977
https://orcid.org/0009-0005-0753-5547
https://orcid.org/0000-0001-8934-7163
https://orcid.org/0000-0001-9540-5278
https://orcid.org/0000-0002-8298-9822
https://orcid.org/0000-0001-8448-7490
https://orcid.org/0000-0003-1349-7733
https://orcid.org/0000-0002-0765-9866
https://orcid.org/0000-0001-6580-7241
https://orcid.org/0000-0002-0382-318X
4 Plant Introduction • 101/102
Zaіmenko et al.
Introduction
Studying the bioecological characteristics
of rare plants has theoretical and practical
significance for better understanding the
reasons for their disappearance and creating
optimal conditions for their conservation.
Plant introduction in botanical gardens allows
for in-depth studies of biological, ecological,
and biochemical features of species with
different life forms (Zaimenko & Rakhmetov,
2022).
To overcome adverse environmental
factors, plants develop special adaptive
systems that enable them to respond
appropriately to various ecological influences
(Chung et al., 2022). Among the survival and
adaptation strategies that plants employ
during evolution and in response to changing
environmental conditions, they exhibit
morphological, physiological, biochemical
changes, and molecular reactions. These
adaptations are realized through various
pathways, including the synthesis of specific
phytohormones. Phytohormones play a crucial
role in the plant’s response to internal and
external stimuli, including stressors. In recent
decades, the term ‘stress phytohormones’ has
become established in scientific literature.
Stress phytohormones, among others,
include brassinosteroids (Kolupaev et al.,
2016; Kosakivska et al., 2019). Brassinosteroids
enhance plant resistance to environmental
stress factors, reduce the toxic effects of
heavy metals, and strengthen the antioxidant
defense system (Kosakivska et al., 2019).
Currently, brassinolide is considered the
most active representative of brassinosteroids.
Brassinolide is a plant hormone that plays a
key role in plant growth and development as
it regulates numerous physiological processes,
including proton pump activity, cell and
shoot growth, leaf architecture, biosynthesis
of ethylene and pigments, photosynthesis,
stress responses, and more (Golovatskaya
& Nikonorova, 2008; Nolan et al., 2020;
Ghassemi-Golezani et al., 2020).
Research on the ecology of nutrients has
become of enormous importance as it is
known that mineral compounds are rarely
found in different soils in optimal quantity.
At the same time, a balanced ratio is essential
for plant growth and development. Plants
always compensate for the influence of stress
factors through nutrition and subsequent
physiological adaptations to the external
environment (Zaimenko, 2008). Micro- and
macroelements are the most important
catalysts of various biochemical processes
in plant cells. They regulate photosynthetic
activity, participate in biochemical exchanges,
and play a significant role in plant resistance
to drought, frost, and diseases.
Soils vary in nutrient content, which,
in turn, influences the specific chemical
composition of plants and determines their
growing success. The potential for nutrient
uptake depends on the actual need of plants
for biogenic elements that support growth
functions. On the other hand, different
tissues accumulate only a certain amount
of nutrients. Research on the absorption of
mineral elements and their content in plants
shows that these indicators can determine
plant adaptation to stress factors (Ivanitska
& Zaimenko, 2008). For example, it has been
found that potassium deficiency leads to an
increase in root diameter, while phosphorus
deficiency increases their volume (Zaimenko
et al., 2005). Changes in soil pH towards
alkaline or acidic reactions reduce the uptake
of almost all macro- and micronutrients
by plants, except for nitrogen (Ivanitska &
Zaimenko, 2008).
Enzymes such as laccases, which can
catalyze the oxidation of a wide range of
organic and inorganic substrates, also play
a vital role in plants’ life (Baldrian, 2006).
Laccases were found in many species of plants,
fungi, and microorganisms (Thurston, 1994).
Once in the soil, laccases participate in the
transformation of organic matter entering the
soil contributing to the formation of humus
and other humus-like substances (Zavarzina et
al., 2004; Eichlerová et al., 2012).
One of the most significant problems today
is the contamination of soils with heavy metals,
which negatively affect plant morphological
structure (Zhang et al., 2011), plant growth
and development (Kosakivska et al., 2019),
photosynthesis activity (Mathur et al., 2016),
transport of organic and mineral compounds
(Zhao et al., 2012), and water exchange
(Mukhopadhyay & Mondal, 2015). In this regard,
aluminum is essential in providing plants with
biogenic elements as it forms stable soluble
complexes with natural organic acids. The
formation of humic and fulvic complexes of
Plant Introduction • 101/102 5
Biochemical and allelopathic features of Adonis vernalis, Allium ursinum, and Leucojum vernum
aluminum in the soil is determined mainly by
the distribution of natural organic substances
in the soil profile (Tyutyunnik et al., 2007).
The most phytotoxic effect of aluminum is the
inhibition of root growth. The phytotoxicity
of aluminum is enhanced in combination with
iron ions, aluminum, and manganese, as well
as in the absence of phosphorus, calcium,
magnesium, and molybdenum in the soil
(Kovalevsky, 2011).
Conversely, silicon deserves attention as
one of the most abundant chemical elements
in the Earth’s crust. It is present in clay
minerals and silicates. In the soil, silicon in its
ionic form acts as a catalyst in the conversion
processes of macro- and micronutrient
compounds, facilitating their transition
from insoluble forms to forms accessible to
plants. Under such conditions, the plant’s
consumption of necessary micronutrients
from the soil significantly increases. Silicon
plays a positive role in plant development
under normal conditions and in response to
adverse environmental factors, stimulating
mechanisms of stability and plasticity
(McGinnity, 2015; Frew et al., 2018). It has been
found that under drought and soil salinity
conditions, there is active root absorption
of silicon from the soil, leading to increased
silicon content in leaves (Nedukha, 2019).
It is worth noting that allelopathic
activity is inherent in practically all plants
and indirectly affects their biochemical
composition. Biologically active compounds
of above-ground parts (including seeds and
fruits) and root exudates determine the level
of allelopathic activity. Alkaloids, which are
crucial for the chemical defense of plants
against phytopathogenic microorganisms,
play a significant allelopathic role in root
exudates (Wink, 2008). In addition, high
content of alkaloids in seeds, fruits, bulbs,
and root residues inhibits seed germination
and plant growth and development (Rice,
1978; Grodzinsky, 1987; Levchyk et al.,
2021). Physiologically active plant exudates
influence metabolic processes, resulting in
either stimulation or inhibition of growth
processes. Among water-soluble compounds
adsorbed by the soil, phenolic acids, such as
p-coumaric, hydroxycinnamic, vanillic, ferulic,
and hydroxybenzoic acids, play a significant
role in allelopathic interactions of the plants
(Grodzinsky, 1973).
We did not find any data in the literature
regarding the content of biogenic elements
in tissues of Adonis vernalis L. and Leucojum
vernum L., in particular, with respect to the
soil. The available information on such topic
for Allium ursinum L. (Tymochko & Hrynyk,
2015) requires supplementation. There is
no information regarding the content of
brassinosteroids in A. vernalis, A. ursinum,
and L. vernum plants, and there is no data
on the enzymatic activity of the rhizospheric
soil. Information on the allelopathic activity
of these plants is fragmented (Dragoeva et al.,
2015; Kachalova & Dzyuba, 2014; Levchyk et al.,
2021).
Adonis vernalis, A. ursinum, and L. vernum
are rare species listed in the Red Book of
Ukraine (Didukh, 2009). They are decorative
spring-flowering herbaceous perennials of
different ecomorphotypes. Adonis vernalis is
a steppic species with a short rhizome. Allium
ursinum is a forest species, and L. vernum is
a forest-meadows species, both with bulbs. In
the M.M. Gryshko National Botanical Garden
of the National Academy of Sciences of Ukraine
(NBG), these three species formed stable
populations in ex situ conditions. Recently,
various botanical studies of A. vernalis
(Gritsenko, 2023) and L. vernum (Gnatiuk &
Gaponenko, 2023) were implemented, and the
study of A. ursinum is ongoing at the NBG.
Therefore, the investigation of biochemical
and allelopathic properties of these species is
prioritized.
Hence, this research aimed to investigate
the dynamics of accumulation of biogenic
elements and brassinosteroids in plants,
determine allelopathic activity, phenolic
compounds, and laccase activity in the
rhizosphere soil of A. vernalis, A. ursinum, and
L. vernum in the conditions of the NBG.
Material and methods
The plants of A. vernalis, A. ursinum, and
L. vernum from the collection of the Natural
Flora Department of the NBG (Fig. 1) were
selected for the field experiments.
Adonis vernalis (Ranunculaceae) is a Euro-
Siberian forest-steppe species. In Ukraine, it is
mainly associated with meadow steppes and is
classified as a mesoxerophyte (Didukh, 2009).
The plant is ornamental. Its parts, especially the
6 Plant Introduction • 101/102
Zaіmenko et al.
above-ground shoots, are used for medicinal
purposes (Colalto, 2020). They contain
cardiac glycosides, including adonitoxin,
cymarin, K-strophanthin-β, acetyladonitoxin,
adonitoxol, vernadigine, and others. The herb
also contains genins such as β-strophanthidin,
strophadogenin, acetyl-strophadogenin,
and flavonoids like adonivernit, vitexin,
homoadonivernit, phytosterol, adonit alcohol,
and others (Grodzinsky, 1989; Shang et al.,
2019; Sattari et al., 2020). It demonstrated
allelopathic activity (Dragoeva et al., 2015).
Allium ursinum (Alliaceae) is a Central
European forest species with a disjunct
distribution, geophyte, and mesophyte. In
Ukraine, it often acts as a dominant species
in natural populations of early spring
herbaceous cover in forests (Didukh, 2009).
The plant is used as food and applied in folk
medicine (Hanelt et al., 1992; Shirataki et al.,
2001; Schulz et al., 2003). It contains proteins,
carbohydrates, cellulose, organic acids,
carotene, vitamins (B group and C), lysozyme,
and essential oil. The strong garlic-like aroma
is due to the presence of sulfur-containing
compounds. It contains steroidal saponins,
pregnane glycoside, polysaccharides, lectins,
fatty acids, and pigments (Sobolewska et al.,
2006, 2015). It is a lectin-containing plant
with high hemolytic activity and antibacterial
and antifungal properties (Kachalova &
Dzyuba, 2014).
Leucojum vernum (Amaryllidaceae) is a
Central European species at the eastern edge
of its range, geophyte and hygromesophyte.
In Ukraine, it is most commonly found in
broad-leaved forests of the lower mountain
belt (Transcarpathia) and floodplain forests
(Ciscarpathia region and plain territories)
(Didukh, 2009). This toxic plant is ornamental
and applied in folk medicine. It contains
alkaloids N-desmethyl galantamine,
hippeastrine, 9-O-demethylhomolycorine,
5-α-hydroxyhomolycorine, 11-hydroxyvittatine,
lycorine, homolycorine, 2-O-acetyllycorine,
leucovernine, acetylleucovernine (Straley
& Utech, 2002; Forgo & Hohmann, 2005;
Birks, 2006).
The botanical garden (NBG) is located in
the Pechersk district, in South-Eastern part of
Kyiv city. The area belongs to the Right-Bank
Forest Steppe of Ukraine, a temperate climate
zone. The gray forest soils with different
textures dominate in the NBG. The artificial
populations of A. ursinum and L. vernum are
located in the collection plot “Rare species of
Ukrainian flora”, having loamy-sandy soil with
pH 6.0–6.5. At the same time, the population
of A. vernalis is located in the botаniсаl-
geographical plot “Stepps of Ukraine”, having
loamy soil with pH 5.6–6.8.
Figure 1. Adonis vernalis (A), Allium ursinum (B), and
Leucojum vernum (C), in the M.M. Gryshko National
Botanical Garden (Kyiv, Ukraine). Photo credits:
A – Victoria Gritsenko; B & C – Alla Gnatiuk.
B
A
C
Plant Introduction • 101/102 7
Biochemical and allelopathic features of Adonis vernalis, Allium ursinum, and Leucojum vernum
For analysis, plant samples and
rhizosphere soil were collected using a
standardized method (Zaimenko, 2021). The
term ‘rhizosphere soil’ refers to the distal
fraction of rhizospheric area adjacent to
rhizoplan, still under roots’ influence but
without direct contact with them (Barillot
et al., 2013). Plants and their associated soil
samples were collected during the plant
growing season: in May (during plants’
flowering stage), August (for A. vernalis
plants – fruiting stage; for A. ursinum and
L. vernum plants – shoot senescence stage),
and October (for A. ursinum and L. vernum
plants – dormant stage; for A. vernalis plants
– shoot senescence stage). To avoid damage
to the population, the sampling of A. ursinum
and L. vernum was not conducted in October
when the plants reached the dormant stage.
Soil lumps (ca. 200 cm3) were collected from
the plant root zone at 15–20 cm depth. Plants
and soils were immediately transferred
in polyethylene bags to avoid excessive
desiccation during transportation and stored
at 4–6 °C.
The preparation of the soil samples for
the analysis of the biogenic elements content
was carried out according to the Rinkis &
Nolendorf (1982) method. Acid-soluble forms
of heavy metals and other chemical elements
were extracted using a 1.0 N solution of nitric
acid (HNO3). Preparation of plant samples for
analysis was carried out by wet ashing with
a solution of nitric acid of high purity using
Speedwave Xpert DAP-60X (Berghof, GmbH,
Germany), a special system of microwave
decomposition of samples. Concentrations
of chemical elements in the solution were
measured on an ICAP 6300 DUO plasma
emission spectrometer (Thermo Fisher
Scientific, USA). The content of chemical
elements was calculated on the air-dry weight
of plant samples and expressed as μg/kg.
The relative uncertainty (Ellison & Williams,
2012) ranged from 7 % to 12 % (it was different
for different chemical elements). Internal
laboratory control of the accuracy of the
measurement results was carried out using a
standard certified sample of moss M2 (Moss
Reference Material M2, Pleurozium schreberi
– The Finnish Forest Research Institute),
using the compatibility criterion.
The allelopathic analysis of soil was
conducted using a direct bioassay method
with cress seedlings (Lepidium sativum L.)
as the test object (Zaimenko, 2021). Phenolic
compounds were extracted from the soil
using the ion exchange (desorption) method,
utilizing the ion exchanger KU-2-8 (H+) as a
model of the root system with desorbing and
absorbing capacity towards mobile organic
compounds (Zaimenko, 2021).
For the analysis of endogenous
brassinosteroids, plant samples (leaves of
A. vernalis and bulbs of A. ursinum and
L. vernum) were transferred to a dark climatic
chamber at a temperature of –8 °C. The
extraction was carried out in two stages: the
first stage with ethyl acetate (three times,
5 ml each) from the aqueous tissue extract
(1 g tissue + 5 ml extraction solution). The
ethyl acetate fraction was evaporated under
vacuum, and the residue was extracted with
cyclohexane (5 ml). The second stage of
extraction was performed using a mixture
of ethanol and water (4 : 1) (three times, 5 ml
each) from the phase containing cyclohexane.
The ethanol extract was evaporated under
vacuum, and the residue was dissolved
in a small amount of ethyl acetate. The
content of brassinosteroids was measured
spectrophotometrically at a wavelength
of 450 nm (Kravets et al., 2011) using a
spectrophotometer SPECORD 200 (Analytik
Jena, Germany, 2003).
Laccase activity was determined by
measuring the rate of syringaldazine
oxidation in the soil extract. Measurements
were conducted on a spectrophotometer at a
wavelength of 530 nm (Baldrian, 2009) using
a spectrophotometer SPECORD 200 (Analytik
Jena, Germany, 2003).
The research results were analyzed
using mathematical methods of parametric
statistics at a significance level of 95 %.
The groups of values were compared
using the Mann-Whitney U-test, which is
used to evaluate differences between two
independent samples and allows detecting
differences in parameter values between
small samples for P ≤ 0.05.
The work was carried out at NBG as part
of the research project “The role of biogenic
elements in inducing brassinosteroid
synthesis for enhancing plant resistance to
stress factors”.
8 Plant Introduction • 101/102
Zaіmenko et al.
Results
The analysis of the content of chemical
elements in the soil under A. vernalis plants
(Table 1) revealed significant amounts of Al and
Fe at the beginning and end of the vegetation
period of plants. The peak values of aluminum
content were recorded in October (17070.0
mg/kg in the soil and 231.0 mg/kg in the
plant). The highest iron content was observed
in May (8635.0 mg/kg in soil) and in October
(168.4 mg/kg in plant). Adonis vernalis plants
demonstrated the highest content of Ca and K.
The calcium content in plants (32335.0 mg/ kg)
at the beginning of the vegetation period
was almost ten times higher than in the soil
(3104.0 mg/kg). The maximum concentration
of potassium in plants (27410.0 mg/kg) was
detected in August, which exceeds its content
in the soil (3783.0 mg/kg) in over seven times.
From May to October, рlants accumulated Mn
(its content increased from 22.2 mg/kg to 45.8
mg/kg) and Si (its content increased from
247.0 mg/kg to 819.0 mg/kg).
The distribution of chemical elements in the
soil under A. ursinum plants also revealed the
highest content of Al (8327.0 mg/kg) in May,
which gradually decreased by October. The
maximum iron content in the soil was observed
in May (8016.0 mg/kg). Alium ursinum plants
had the highest content of K, Ca and S. From
May to August, рlants actively accumulated Al,
К, Mn, and Zn. The plants mainly accumulated
K; its content increased from 3299.0 mg/kg in
May to 11510.0 mg/kg in August. The calcium
content in the plants did not increase so much
– from 1860.0 mg/kg in May to 2810.0 mg/kg
in August (Table 2).
The rhizosphere soil under L. vernum
plants had a high content of Ca (10510.0 mg/
kg) and Al (9975.0 mg/kg) in October. In
plants, potassium had the leading position; its
content in August was the highest and reached
8957.0 mg/kg. From May to August, рlants
accumulated Al, Сu, Fe, Mn, S, Si, and Zn. The
content of these elements had increased in
several times (Table 3).
The analysis of chemical elements content
in plant tissues (Tables 1–3) of the studied
species revealed several general trends. The
accumulation of silicon in plants showed a
similar pattern until the end of the vegetation
period. Compared to the beginning of the
vegetation period, the content of Si in plants
increased by 3.3 times in A. vernalis, by 1.1 times
in A. ursinum, and by 8.8 times in L. vernum.
Also, all studied species accumulated Mn
during the vegetation season and K from May
to August. During this period, the potassium
content in plants increased by 2.5 times in
A. vernalis, by 3.5 times in A. ursinum, and by
1.7 times in L. vernum.
Chemical
element
Soil Plant
May August October May August October
Al 11995.0 ± 1032.8 13440.0 ± 41.5 17070.0 ± 1484.9 116.0 ± 11.2 159.0 ± 13.5 231.0 ± 20.4
B 7.08 ± 0.6 7.16 ± 0.6 11.30 ± 1.1 19.33 ± 1.7 23.89 ± 2.1 28.82 ± 2.3
Ca 3104.0 ± 273.5 5771.0 ± 574.9 6254.0 ± 560.1 32335.0 ± 3115.2 27450.0 ± 2559.2 26750.0 ± 2445.2
Cu 15.8 ± 1.2 24.4 ± 2.1 21.5 ± 1.7 9.5 ± 0.8 11.4 ± 1.1 9.9 ± 0.7
Fe 8635.0 ± 397.9 7980.0 ± 1797.6 7496.0 ± 319.0 97.0 ± 4.3 79.2 ± 3.8 168.4 ± 12.7
K 2346.0 ± 159.2 3783.0 ± 451.9 3092.0 ± 197.1 11177.0 ± 1935.9 27410.0 ± 1717.3 9330.0 ± 539.8
Mg 1520.0 ± 99.6 5945.0 ± 358.7 1548.0 ± 112.9 3476.0 ± 201.5 2598.0 ± 237.4 3791.0 ± 236.7
Mn 284.8 ± 17.6 311.1 ± 0.9 336.3 ± 22.8 22.2 ± 1.9 30.1 ± 2.3 45.8 ± 2.3
P 384.0 ± 18.6 323.0 ± 20.3 433.0 ± 27.5 1608.0 ± 128.2 1695.0 ± 103.5 539.2 ± 27.3
S 345.0 ± 31.6 492.0 ± 49.1 405.0 ± 37.7 2238.0 ± 197.7 3818.0 ± 369.2 1039.0 ± 95.4
Si 1438.0 ± 98.4 1062.0 ± 92.3 837.0 ± 33.6 247.0 ± 10.6 568.0 ± 23.2 819.0 ± 49.8
Zn 47.0 ± 2.3 30.0 ± 1.9 46.0 ± 2.5 14.0 ± 0.8 25.0 ± 0.7 12.0 ± 0.6
Table 1. The content and dynamics of biogenic elements in the leaves of Adonis vernalis and the surrounding
rhizosphere soil, mg/kg ± U (k = 2, P = 0.95).
Plant Introduction • 101/102 9
Biochemical and allelopathic features of Adonis vernalis, Allium ursinum, and Leucojum vernum
Chemical
element
Soil Plant
May August October May August
Аl 8327.0 ± 403.4 8222.0 ± 452.8 6201.0 ± 301.9 94.0 ± 8.23 342.0 ± 21.3
В 5.4 ± 0.4 6.5 ± 0.5 7.9 ± 0.7 6.8 ± 0.5 9.3 ± 0.8
Са 3755.0 ± 121.5 2318.0 ± 121.7 16.2 ± 0.9 1860.0 ± 114.1 2810.0 ± 137.4
Сu 19.5 ± 1.7 22.3 ± 1.7 22.4 ± 1.9 9.5 ± 0.9 14.3 ± 1.1
Fе 8016.0 ± 1.3 6426 ± 351.6 3657.0 ± 198.4 59.1 ± 3.6 30.0 ± 7.1
К 1596.0 ± 98.0 1440.0 ± 103.7 1153.0 ± 98.7 3299.0 ± 285.9 11510.0 ± 534.7
Мg 1173.0 ± 85.3 1005.0 ± 78.7 957.0 ± 6.4 588.0 ± 41.2 1068.0 ± 71.3
Мn 246.0 ± 19.3 312.7 ± 21.0 204.5 ± 15.2 7.87 ± 0.3 17.06 ± 1.2
Р 255.0 ± 13.9 224.0 ± 12.7 263.0 ± 15.9 1250.0 ± 97.9 1999.0 ± 111.3
S 209.0 ± 12.8 335.0 ± 18.6 281.0 ± 14.3 2518.0 ± 126.4 2539.0 ± 130.3
Si 1217.0 ± 10.8 1452.0 ± 11.7 881.0 ± 14.9 696.0 ± 4.7 730.0 ± 21.4
Zn 73.0 ± 2.9 25.0 ± 1.2 20.0 ± 0.8 7.0 ± 0.3 41.0 ± 1.5
Table 2. The content and dynamics of biogenic elements in the bulbs of Allium ursinum and the surrounding
rhizosphere soil, mg/kg ± U (k = 2, P = 0.95).
Chemical
element
Soil Plant
May August October May August
А1 6379.0 ± 59.7 7032.0 ± 64.2 9975.0 ± 93.8 63.0 ± 3.2 491.0 ± 18.3
В 4.3 ± 0.1 7.7 ± 0.3 6.5 ± 0.2 6.8 ± 0.3 6.8 ± 0.2
Са 2931.0 ± 27.4 8482.0 ± 78.7 10510.0 ± 119.3 819.0 ± 24.3 1558.0 ± 63.8
Сu 27.84 ± 1.2 21.32 ± 1.1 20.08 ± 0.1 8.6 ± 0.4 19.9 ± 1.1
Fе 5475.0 ± 122.9 125.0 ± 4.5 4595.0 ± 218.3 49.0 ± 1.7 399.0 ± 12.8
К 1179.0 ± 49.6 2717.0 ± 84.4 1522.0 ± 52.8 5193.0 ± 176.2 8957.0 ± 98.2
Mg 896.0 ± 37.5 1762.0 ± 65.0 911.0 ± 44.7 618.0 ± 29.5 889.0 ± 39.1
Мn 198.7 ± 8.3 87.34 ± 4.2 238.6 ± 10.6 5.40 ± 0.3 21.03 ± 1.1
Р 267.0 ± 11.6 201.0 ± 8.9 209.0 ± 9.1 1499.0 ± 15.6 2049.0 ± 77.8
S 277.0 ± 12.6 337.0 ± 17.4 165.0 ± 7.9 802.0 ± 29.5 5305.0 ± 186.7
Si 2035.0 ± 79.3 1515.0 ± 62.6 653.0 ± 27.4 107.0 ± 5.3 943.0 ± 28.6
Zn 23.0 ± 1.1 23.0 ± 0.9 38.0 ± 1.5 15.0 ± 0.7 35.0 ± 1.4
Table 3. The content and dynamics of biogenic elements in the bulbs of Leucojum vernum and the
surrounding rhizosphere soil, mg/kg ± U (k = 2, P = 0.95).
According to Tables 1–3, for each of the
studied species, an increase in magnesium
content in plants was observed from May
until the completion of the vegetation period.
The content of Mg in plant tissues increased
by 1.1 times in A. vernalis, by 1.8 times in
A. ursinum, and by 1.4 times in L. vernum.
Similarly, the copper content in plant tissues
of all studied species increased. However,
the iron content increased only in A. vernalis
and L. vernum plants, while in A. ursinum its
content decreased almost in two times.
The obtained results of studying the
allelopathic activity of soils under the
experimental plant species are presented in
Fig. 2. The allelochemicals in the rhizosphere
10 Plant Introduction • 101/102
Zaіmenko et al.
soil of A. ursinum exhibited phytotoxic
effects at the end of the summer season
(inhibited biotest growth by 21.7 % compared
to the control), but had the most significant
impact in autumn (43.0 % inhibition). During
the summer period, the physiologically
active compounds in the soil under
A. vernalis showed a slight allelopathic effect
with 11.9 % inhibition of root growth in the
receptor plants compared to the control. In
autumn, the allelopathic activity of the soil
under A. vernalis slightly increased (19.8 %
phytotoxic effect). There was a growth-
stimulating effect (20.3 % compared to the
control) of the allelochemicals in the soil
under L. vernum in May. However, by early
autumn, their allelopathic activity shifted
towards inhibiting the growth processes
of the receptor plants, which intensified
towards the end of the vegetation period
(14.9 % and 21.1 % inhibition compared to the
control).
The dynamics of the accumulation of
phenolic compounds in the soil under
A. ursinum indicates a 1.5-fold increase in their
content from spring to the end of the growing
season (Fig. 3). Analogous results were
obtained for the concentration of phenolic
compounds in the soil under A. vernalis.
The content of phenolic compounds in the
soil under L. vernum also increased during
the growing season. At the same time, their
content in autumn was two times higher than
in spring.
The maximum soil laccase activity was in
spring, with a gradual decrease throughout
the entire vegetation season (Fig. 4). It
negatively correlated with the content of
phenolic compounds in the soil.
The evaluation of brassinosteroid
content in different plant organs of the
studied species reveals noteworthy findings
(Table 4). Certain patterns are observed in
the distribution of brassinosteroids in leaves
and bulbs. Specifically, a 2.1-fold increase
in brassinosteroid content in A. vernalis
leaves at the end of the vegetation period
corresponds to a 3.3-fold increase in silicon
concentration. In A. ursinum bulbs, a reverse
relationship is observed: a 1.2-fold decrease
in brassinosteroid concentration and a
7.6-fold increase in silicon concentration.
A similar pattern is observed for L. vernum
bulbs: a 19.0-fold reduction in brassinosteroid
content and an 8.8-fold increase in silicon
concentration.
Figure 2. Allelopathic activity of soil under Allium ursinum, Adonis vernalis, and Leucojum vernum plants
(bioassay – growth of Lepidium sativum roots). Whiskers indicate the standard deviation.
Plant Introduction • 101/102 11
Biochemical and allelopathic features of Adonis vernalis, Allium ursinum, and Leucojum vernum
Figure 3. The content of phenolic compounds in the soil under Allium ursinum, Adonis vernalis, and Leucojum
vernum plants. Whiskers indicate the standard deviation.
Figure 4. Soil laccase activity under Allium ursinum, Adonis vernalis, and Leucojum vernum plants. Whiskers
indicate the standard deviation.
12 Plant Introduction • 101/102
Zaіmenko et al.
Discussion
The studied plant species differ significantly
in their ecomorphotype. Comparative
biochemical analysis revealed differences
in the distribution of biogenic elements and
brassinosteroids in their tissues. For all plants,
there is an increase in the concentration of
Al, Fe, Si, and Mn. However, bulbs show more
pronounced fluctuations in the concentration
of these elements than leaves. Notably,
bulbs have higher contents of P, K, Ca, and
Zn, which can be attributed to assimilation
processes involved in plant preparation
for dormancy. Calcium is one of the most
important signaling molecules in plant cells
under stress conditions, controlling processes
that contribute to the homeostasis of various
macroelements such as potassium, nitrogen,
and magnesium, as well as the microelement
iron (Wang et al., 2019; Kong et al., 2020; Dong
et al., 2021; Liu et al., 2021; Ghosh et al., 2022).
The functional role of Ca2+ in stress signaling
and subsequent activation of tolerance
mechanisms has been well established (Sharma
et al., 2022). It is known that the perception of
the environment and internal signals leads to
changes in cytosolic Ca2+ signatures, which, in
turn, results in gene expression changes and
alterations in cellular functions (Wang et al.,
2021; Verma et al., 2022).
On the other hand, magnesium is
essential for a wide range of physiological
and biochemical processes in plants,
including chlorophyll synthesis, transport
and distribution of photoassimilates,
enzyme activation, and protein synthesis
(Ishfaq et al., 2022). Potassium regulates the
osmotic potential of plants and is crucial
for maintaining water balance under stress
conditions. Additionally, it plays a vital
role in various aspects of plant life, such as
photosynthesis, phloem transport, and cellular
electrochemistry (Cui & Tcherkez, 2021;
Kumari et al., 2021; Li et al., 2021; Lotfi et al.,
2022).
Silicon modulates the expression of
different genes in plants under stress,
regulates the synthesis and accumulation
of reactive forms of oxygen and nitrogen,
and reduces the negative impact on
photosynthesis. Silicon also activates the
antioxidant defense system in plants, thereby
maintaining cellular redox homeostasis
and preventing oxidative damage to cells. It
regulates H2S synthesis or acts synergistically
with NO, assuring stress tolerance in plants
(Ahire et al., 2021; Basu & Kumar, 2021; Dhiman
et al., 2021; Rastogi et al., 2021; Etesami &
Jeong, 2023). Based on the abovementioned,
the experimentally obtained relationship
indicates the high resilience of plants to
abiotic and biotic factors, particularly
dehydration. Furthermore, the increase in Zn
content in bulb tissues provides additional
cold tolerance to the plants during winter.
The concept of nutrient availability for
plants of different ecomorphotypes should
be considered from two independent
perspectives. According to the first
perspective, in natural soil ecosystems,
redistribution of mineral compounds
occurs from inaccessible pools to available
pools, which supply plants with chemical
elements and determine their levels. Habitats
significantly differ in the intensity of organic
matter decomposition or mineral weathering
processes. From the second perspective,
the productivity of plants and the entire
ecosystem is influenced by inadequate
mineral nutrition, which determines the
space where productivity decreases due
Sampling date
Brassinosteroids Silicon
Leaves Bulbs Bulbs Leaves Bulbs Bulbs
A. vernalis A. ursinum L. vernum A. vernalis A. ursinum L. vernum
May 2.5 ± 0.21 2.6 ± 0.21 11.4 ± 0.09 247 ± 20.35 9.6 ± 0.80 107.0 ± 9.50
August 4.1 ± 0.33 2.1 ± 0.17 0.6 ± 0.05 568 ± 51.67 7.3 ± 68.70 943.0 ± 89.80
October 5.3 ± 0.49 - - 819.0 ± 77.80 - -
Table 4. The content of brassinosteroids and silicon in different organs of Adonis vernalis, Allium ursinum,
and Leucojum vernum, mg/kg ± U (k = 2, P = 0.95).
Plant Introduction • 101/102 13
Biochemical and allelopathic features of Adonis vernalis, Allium ursinum, and Leucojum vernum
to insufficient doses of nutrients that have
been supplied (Zaimenko, 2008; Zaimenko
et al., 2022).
Therefore, the concentration of macro-
and micronutrients in the plant’s tissues is
the most reliable indicator of its chemical
status. Currently, most hypotheses regarding
the uptake of macro- and micronutrients
(see Zaimenko, 2008; Zaimenko et al.,
2022) are based on ion transport, including
thermodynamic forces, characteristics
of biological membrane structure and
composition, specific chemical properties of
elements considering their tendency to form
complexes with organic ligands, sensitivity to
redox processes, and pH changes.
In light of the mentioned above, research
on the allelopathic activity of the soil becomes
particularly relevant. All studied plant species
exhibit the presence of physiologically active
compounds with allelopathic properties in the
adjacent rhizosphere soil. Overall, moderate-
reductive processes prevail in the rhizosphere
soil during the summer under all plants, while
intensive-reductive processes dominate in
the autumn. This trend is likely associated
with the influx of mobile forms of organic
compounds into the rhizosphere environment.
The accumulation of phenolic compounds in
the rhizosphere soil increased throughout
the vegetation period, reaching its peak in
the autumn, presumably contributing to its
phytotoxic properties. It is known that soil
phenolic substances encompass various types
of compounds, including simple flavonoids,
phenolic acids, complex flavonoids, and
anthocyanins (Babbar et al., 2014). These
compounds are usually associated with
plant defense reactions. Polyphenols such
as resveratrol, quercetin, butein, fisetin,
piceatannol, and curcumin reduce the degree
of oxidative stress and restore redox balance
(Singh et al., 2023). However, phenolic
metabolites also play an essential role in other
processes. They serve as attractive substances
for pollination acceleration, providing
coloration for camouflage and protection
against herbivores, as well as demonstrate
antibacterial and antifungal effects (Alasalvar
et al., 2001; Acamovic & Brooker, 2005; Edreva
et al., 2008).
The laccase activity, which catalyzes the
transformation of aromatic and non-aromatic
substrates with the reduction of molecular
oxygen to water, deserves attention. Apart
from lignin degradation, differentiation, and
fruiting body formation in fungi, laccases
are involved in processes such as the
adhesion of phytopathogens to host plant
cells, organic residue humification, and
xenobiotic detoxification (Rivera-Hoyos et al.,
2013; Rangelov & Nicell, 2019; Ben Younes
et al., 2019).
Conclusions
Our research demonstrated that model
species of rare and endangered plants employ
a wide range of physiological mechanisms
throughout the vegetation period to enhance
their resistance to abiotic factors. These
mechanisms include maintaining potassium
and calcium balance and utilizing hormonal
compounds. These plants have been proven to
have compensatory mechanisms in response
to stress factors, substituting one biochemical
marker of resistance with another. Both
brassinosteroids and silicon contribute to the
adaptive capacity of organisms. Furthermore,
A. ursinum and L. vernum enter a period of
dormancy and accumulate silicon in their
bulbs during the second half of summer,
providing additional resistance to low
temperatures. Therefore, further study of the
biology and ecology of these rare plant species
in the context of conservation and enrichment
of biodiversity is promising.
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Біохімічні та алелопатичні особливості Adonis vernalis, Allium ursinum та Leucojum
vernum у Національному ботанічному саду імені М.М. Гришка НАН України
Наталія Заіменко 1, Алла Гнатюк 1, *, Вікторія Гриценко 1, Олександр Закрасов 1, Наталія Павлюченко 1,
Ірина Харитонова 1, Оксана Дзюба 1, Наталія Дідик 1, Олена Юношева 1, Олег Блюм 1, Артур Ліханов 2,
Наталія Голіченко 3
1 Національний ботанічний сад імені М.М. Гришка НАН України, вул. Садово-Ботанічна, 1, Київ,
01014, Україна; * gnatiukalla@gmail.com
2 Національний університет біоресурсів та природокористування України, вул. Героїв Оборони, 15,
Київ, 03041, Україна
3 Український інститут експертизи сортів рослин, вул. Генерала Родимцева, 15, Київ, 03041, Україна
У статті наведено результати дослідження вмісту та динаміки накопичення біогенних елементів і
брасинолідів у рослинах Adonis vernalis, Allium ursinum та Leucojum vernum у Києві, Україна. Наведено дані
https://doi.org/10.1016/j.envexpbot.2022.104935
https://doi.org/10.1016/j.envexpbot.2022.104935
https://doi.org/10.1016/j.plantsci.2019.110192
https://doi.org/10.1016/j.plantsci.2019.110192
https://doi.org/10.1016/j.chom.2021.07.003
https://doi.org/10.1002/9783527621071.ch1
https://doi.org/10.1002/9783527621071.ch1
https://doi.org/10.15421/012241
https://doi.org/10.1016/j.soilbio.2003.10.010
https://doi.org/10.1016/j.soilbio.2003.10.010
https://doi.org/10.1007/s00299-011-1056-4
https://doi.org/10.1007/s00299-011-1056-4
https://doi.org/10.1016/j.jplph.2012.04.016
https://doi.org/10.1016/j.jplph.2012.04.016
18 Plant Introduction • 101/102
Zaіmenko et al.
щодо алелопатичної активності, розподілу макро- і мікроелементів, фенольних сполук, активності
лаккази в ризосферному ґрунті в умовах Національного ботанічного саду імені М.М. Гришка НАН
України (НБС). Як об’єкти дослідження в польових дослідах використовувалися рослини з колекції
НБС. Вміст біогенних елементів у тканинах рослин і ґрунті аналізували за допомогою спектрометра
з індуктивно зв’язаною плазмою. Алелопатичний аналіз ґрунту проводили методом прямого
біотестування з використанням проростків Lepidium sativum як тест-об’єкта. Фенольні сполуки
екстрагували з ґрунту іонообмінним (десорбційним) методом. Вміст брасиностероїдів вимірювали
спектрофотометрично при довжині хвилі 450 нм. Вміст лаккази вимірювали спектрофотометрично
на довжині хвилі 530 нм.
Результати показали, що модельні види рослин використовують широкий спектр фізіологічних
механізмів протягом вегетаційного періоду для підвищення стійкості до абіотичних факторів. Ці
механізми включають підтримку балансу калію та кальцію та використання гормональних сполук.
Доведено, що рослини мають компенсаторні механізми у відповідь на стресові фактори, замінюючи
один біохімічний маркер стійкості іншим. І брасиностероїди, і кремній сприяють адаптаційній
здатності організмів.
Ключові слова: біогенні елементи, фенольні сполуки, лакказа, адаптація рослин, фітогормони
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| spelling | oai:ojs2.plantintroduction.org:article-16302026-03-05T18:42:33Z Biochemical and allelopathic features of Adonis vernalis, Allium ursinum, and Leucojum vernum in the M.M. Gryshko National Botanical Garden of the NAS of Ukraine Біохімічні та алелопатичні особливості Adonis vernalis, Allium ursinum та Leucojum vernum у Національному ботанічному саду імені М.М. Гришка НАН України Zaіmenko, Natalia Gnatiuk, Alla Gritsenko, Victoria Zakrasov, Oleksandr Pavliuchenko, Nataliia Kharytonova, Iryna Dziuba, Oksana Didyk, Nataliya Yunosheva, Olena Blum, Oleg Likhanov, Artur Holichenko, Nataliia The article presents the results of a study on the content and dynamics of the accumulation of biogenic elements and brassinolides in plants of Adonis vernalis, Allium ursinum, and Leucojum vernum in Kyiv, Ukraine. Data is provided on allelopathic activity, content of macro- and microelements, phenolic compounds, and laccase activity in plants and the rhizosphere soil under the conditions of the M.M. Gryshko National Botanical Garden of the National Academy of Sciences of Ukraine (NBG). The plants from the collection of the NBG were used as objects of study in field experiments. The content of biogenic elements in plant tissues and soil was analyzed using an inductively coupled plasma spectrometer. The allelopathic analysis of soil was conducted using a direct bioassay method with Lepidium sativum seedlings as the test object. Phenolic compounds were extracted from the soil using the ion exchange (desorption) method. The content of brassinosteroids was measured spectrophotometrically at a wavelength of 450 nm. The content of laccase was measured spectrophotometrically at a wavelength of 530 nm.The results demonstrate that model plant species employ a wide range of physiological mechanisms throughout the vegetation period to enhance their resistance to abiotic factors. These mechanisms include maintaining potassium and calcium balance and utilizing hormonal compounds. Plants have been proven to have compensatory mechanisms in response to stress factors, substituting one biochemical marker of resistance with another. Both, brassinosteroids and silicon, contribute to the adaptive capacity of organisms. У статті наведено результати дослідження вмісту та динаміки накопичення біогенних елементів і брасинолідів у рослинах Adonis vernalis, Allium ursinum та Leucojum vernum у Києві, Україна. Наведено дані щодо алелопатичної активності, розподілу макро- і мікроелементів, фенольних сполук, активності лаккази в ризосферному ґрунті в умовах Національного ботанічного саду імені М.М. Гришка НАН України (НБС). Як об’єкти дослідження в польових дослідах використовувалися рослини з колекції НБС. Вміст біогенних елементів у тканинах рослин і ґрунті аналізували за допомогою спектрометра з індуктивно зв’язаною плазмою. Алелопатичний аналіз ґрунту проводили методом прямого біотестування з використанням проростків Lepidium sativum як тест-об’єкта. Фенольні сполуки екстрагували з ґрунту іонообмінним (десорбційним) методом. Вміст брасиностероїдів вимірювали спектрофотометрично при довжині хвилі 450 нм. Вміст лаккази вимірювали спектрофотометрично на довжині хвилі 530 нм.Результати показали, що модельні види рослин використовують широкий спектр фізіологічних механізмів протягом вегетаційного періоду для підвищення стійкості до абіотичних факторів. Ці механізми включають підтримку балансу калію та кальцію та використання гормональних сполук. Доведено, що рослини мають компенсаторні механізми у відповідь на стресові фактори, замінюючи один біохімічний маркер стійкості іншим. І брасиностероїди, і кремній сприяють адаптаційній здатності організмів. M.M. Gryshko National Botanical Garden of the NAS of Ukraine 2024-02-17 Article Article application/pdf https://www.plantintroduction.org/index.php/pi/article/view/1630 10.46341/PI2023011 Plant Introduction; No 101/102 (2024); 3-18 Інтродукція Рослин; № 101/102 (2024); 3-18 2663-290X 1605-6574 10.46341/PI101-102 en https://www.plantintroduction.org/index.php/pi/article/view/1630/1549 Copyright (c) 2024 Natalia Zaіmenko, Alla Gnatiuk, Victoria Gritsenko, Oleksandr Zakrasov, Nataliia Pavliuchenko, Iryna Kharytonova, Oksana Dziuba, Nataliya Didyk, Olena Yunosheva, Oleg Blum, Artur Likhanov, Nataliia Holichenko http://creativecommons.org/licenses/by/4.0 |
| spellingShingle | Zaіmenko, Natalia Gnatiuk, Alla Gritsenko, Victoria Zakrasov, Oleksandr Pavliuchenko, Nataliia Kharytonova, Iryna Dziuba, Oksana Didyk, Nataliya Yunosheva, Olena Blum, Oleg Likhanov, Artur Holichenko, Nataliia Біохімічні та алелопатичні особливості Adonis vernalis, Allium ursinum та Leucojum vernum у Національному ботанічному саду імені М.М. Гришка НАН України |
| title | Біохімічні та алелопатичні особливості Adonis vernalis, Allium ursinum та Leucojum vernum у Національному ботанічному саду імені М.М. Гришка НАН України |
| title_alt | Biochemical and allelopathic features of Adonis vernalis, Allium ursinum, and Leucojum vernum in the M.M. Gryshko National Botanical Garden of the NAS of Ukraine |
| title_full | Біохімічні та алелопатичні особливості Adonis vernalis, Allium ursinum та Leucojum vernum у Національному ботанічному саду імені М.М. Гришка НАН України |
| title_fullStr | Біохімічні та алелопатичні особливості Adonis vernalis, Allium ursinum та Leucojum vernum у Національному ботанічному саду імені М.М. Гришка НАН України |
| title_full_unstemmed | Біохімічні та алелопатичні особливості Adonis vernalis, Allium ursinum та Leucojum vernum у Національному ботанічному саду імені М.М. Гришка НАН України |
| title_short | Біохімічні та алелопатичні особливості Adonis vernalis, Allium ursinum та Leucojum vernum у Національному ботанічному саду імені М.М. Гришка НАН України |
| title_sort | біохімічні та алелопатичні особливості adonis vernalis, allium ursinum та leucojum vernum у національному ботанічному саду імені м.м. гришка нан україни |
| url | https://www.plantintroduction.org/index.php/pi/article/view/1630 |
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