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Microelement composition of soil and vegetation in a forest-steppe reserve in technogenesis conditions.


Interaction of plants with soil, especially the microelement metabolism has a twofold character. On the one hand, plants regulate the absorption and accumulation of metals, maintaining the genotypically specified "microelement homeostasis"; on the other hand, they cannot completely neutralize a "geochemical pressure" of the environment with an increase in concentrations of elements in soils above the optimum. Ilyin (1991) defines these factors as genotypic and environmental.

With the development of the heat power, metal, mining, and chemical industries the pollution of soils by the artificially produced substances happens everywhere. Plants are able to grow on soils contaminated with a large number of various microelements. Metal tolerance develops rather quickly and has a genetic basis. Evolutionary changes caused by heavy metals have been found in a large number of species growing on soils enriched with metals. These changes distinguish the plants from populations of the same species growing on normal soils [1-4]. Implementation of genetic possibilities of the higher plants during adaptation to pollutants is of particular importance for the conservation of biodiversity in reserve areas located in technologically loaded regions.

The Troitsky forest-steppe reserve occupies an area of approximately 1,200 hectares and is a reserved piece of black soil and meadow steppes surrounded by technologically loaded territories of Transurals. Studies were conducted on the black soil and meadow-solonetz observation stations of the reserve. Stipa zalesskii and Stipa pennata are the edificators of the vegetation cover on the ordinary, medium, medium-humic, heavy loamy black soil; they make up 30-45% of the cover. Medium-natric, medium columnar meadow solonetzes, and high columnar, clay solonetzes are solonchak-like and characterized by the medium salinity, mixed chemistry of salinization with the participation of soda. Vegetation cover of the meadow solonetz is formed by various factors of grass-fescue steppes, the edificator is Festuca sulcata (Hack.) Nym., also there grow species typical of saline soils (Artemisia nitrophilous, Plantago cornuti, Silaum silaus).

The purpose of this work is to assess the level of accumulation of some microelements in soils and plants of this protected area.

Materials and Methods

Samples of the humus horizon of black soil and solonetz were taken from the depth of 0-10 cm in ten locations to determine the content of microelements. Plant material was collected in five locations for each test species. The following species were used to study the chemical composition on the black soil: Stipa pennata L., Inula hirta L., Galium ruthenicum Willd., Fragaria viridis (Duch.) Weston, Genista tinctoria (L.) Maxim., on the meadow solonetz--Filipendula ulmaria Juss, Artemisia pontica L., Festuca sulcata (Hack.) Nym., Artemisia nitrosa Web., Plantago cornuti Gouan, Galatella biflora (L.) Nees. Heavy metal content was determined with a spectrograph DFS-1 by an atomic absorption method with the vaporization of the carbon electrode sample and the control of measuring accuracy on standard samples.

To study the distribution of lead and nickel in plants, a histochemical method was used [5], based on the coloration of slices of the living root and stem with dithizone and dimethylglyoxime. Selected plants of Filipendula ulmaria Juss, Galatella biflora (L.) Nees, Artemisia pontica L. were transplanted into containers with Pb[(N[O.sub.3]).sub.2] and Ni[Cl.sub.2] solutions in concentration [10.sup.-4] and [10.sup.-3] M and incubated on the solutions. Localization of lead and nickel in the tissues of roots and stems was measured after 1, 24, 48, 72, and 120 h of incubation.

Significance of differences in the microelement composition of the soil samples and above and below ground parts of plants was evaluated statistically and by analysis of variance.

Results and Discussion

The Chelyabinsk region is located on the territory of ancient and badly damaged Ural Mountains. Previously hidden in the depth, rocks are exposed and, under the influence of external factors, metals are released and migrated. Here, large deposits of minerals are developed--titanomagnetite, chromite, copper, nickel, which can serve as a source of spread of metals in the surrounding areas. The main parent rock material in the reserve is a yellow-brown loam characterized by a high content of Ni, Ti, Cu, Mn compared with the percentage abundance in lithosphere, the amount of chromium in them is 5.5 times higher (Table 1).

Air pollutants in the region are the enterprises of fuel energy, coke, and electrode; among the most hazardous pollutants there are lead, hexavalent chromium, and manganese. According to studies, humus horizons of black soil and solonetzes are enriched in microelements relative to the parent rock material (Table 1). In black soil, they are characterized by significant accumulation of Co, V, Ti, Pb, and Zn, and in meadow solonetz, Mn is accumulated in addition to these elements; the quantity of V in soils is 2 times higher, Pb and Zn--4 times higher than in parent rock material. Apparently, the modern microelement composition of soils in the reserve is formed by both natural (geochemical) and technogenic factors; pollutants including those related to the work of Troitsk GRES are deposited in the surface layers of soil. Technogenic elements are redistributed in the soil cover, as solonetzes lower plains contain significantly more Co, Mn, Cu, Pb compared with the black soil of low ridges.

Comparison with the world percentage abundance in soils (according to Vinogradov) has shown that the concentration of Zn, Pb, Cu is 4-5 times exceeded and the concentration of Co, V, Ni, Mn, Cr, Ti is 1.5-2.5 times exceeded (Table 1). The average content of heavy metals in soils of the south of Western Siberia [6] is 5 times exceeded for Cr, and 2-3 times for other heavy metals (except Mo). According to Ilyin (1995), the level of accumulation of Ni, Co, Mn, V, Cu can be estimated as medium (tolerant) and the concentration of Cr, Zn, Pb is approaching to high (dangerous). Thus, the soil cover of the forest-steppe reserve suffers from the technogenic pollution apparently connected to the aerial transfer of pollutants. Due to the natural and technogenic environment, it is noted an elevated level of accumulation of the studied microelements except Mo in humus horizons of the soil. Content of microelements in the aerial parts of plants growing in the same soil was several times different (Table 2). Apparently, the plants maintain a genotypically predetermined "microelement homeostasis", which can be particularly ensured by the barrier function of the root system. Metals are bound by the cell walls and it is assumed that a change of carbohydrate composition of the cell walls has a particular importance in this [1,7-12].

Plants growing on black soils and solonetzes of the forest-steppe reserve are rich in chromium, but poor in zinc compared to the world percentage abundance (according to Dobrovolsky) and to the regional values in the south of Western Siberia [1] and in Transurals near Orenburg [13]. Plants may be slightly different by the content of other microelements upward or downward relative to the percentage abundance. Consequently, plants of the reserve growing in high soil geochemical background conditions accumulate some trace elements only insignificantly, showing at the same time the species-specific features. Among the plants being studied stands out the meadowsweet (Filipendula ulmaria Juss) in connection with a high content of most microelements. Cereals showed low content of Mn.

Importance of the barrier function of the root system of plants growing in high soil geochemical background conditions of Transurals was found when comparing the content of microelements in the aboveground and underground parts of plants; an increased number of them in the roots was noted in more than 80% of cases. Vazhenin (1984) proposed to use the accumulation factor--ratio between the content of elements in the underground and aboveground organs--as a bioindicator of the early phase of soil pollution [14]. Accumulation factor reflects the adaptive capacity of plants and is determined by properties of the soil and plants.

According to the accumulation factor in the roots of the plants of the reserve the amount of Co, Cr, Mn, V, Ti, Cu, Zn, Pb, Mo is 2-16 times higher than in aboveground organs (Table 3). The barrier function of the root system regarding to nickel is poorly expressed, the accumulation factor of six plants is 1, 4-1,8; three species did not show the nickel accumulation in the roots.

Meadowsweet (Filipendula ulmaria) tends to have decreased accumulation factors of microelements in the underground parts of the plant; as indicated above, the absence of the barrier defense mechanisms led to the increased content of microelements in the aboveground parts of the plant. Experimental data on the incubation of plants in salt solutions has shown the importance of physiological barriers to the admission of microelements, the difference in microelement's behavior, and the species-specific features of the regulation of microelement "homeostasis". Results on the localization of Pb in the tissues of the roots of the Fragaria viridis, Filipendula ulmaria, and Artemisia pontica are shown in Table 4.

After the first hour of incubation, Pb was found in the cell walls of periderm of the rhizomes of all the plants, wherein a small amount of the metal was also found in the outer layers of the cortex of the Filipendula ulmaria.

After 24 h of incubation, cell walls of the periderm showed weak coloring. The coloring of the outer bark of Fragaria viridis and Filipendula ulmaria was very weak. The localization of Pb in the bark cells of the Artemisia pontica was not found. Over time (48-120 h), the coloring of the periderm slightly increased, which testifies the increase of the concentration of the metal, while the coloring of the outer bark remained weak or very weak. After 48 h of incubation, there were observed weakening of turgor of cells and emergence of brown spots on the leaves. By the end of the experiment, a significant mucilaginization and destruction of periderm and bark cells were observed.

Distribution of Ni in the root tissues was markedly different from the localization of Pb (Table 5).

Within 24 h, Ni was detected in all tissues of the root--from the periderm to the vascular bundles. The strongest coloring and, thus, the highest metal content were noted in the periderm and bark. Over time, the concentration of Ni in the conductive tissues increased, after 120 h a very strong staining was observed. It was detected a slight concentration of Ni in the conducting tissues of aboveground organs, although the coloring in aboveground organs was weaker than in underground.

As described previously, the studied species show a differential accumulation of metals; barrier absorption of Pb by the rhizome tissues causes its comparatively low accumulation in aboveground organs, and a weak manifestation of the rhizome barrier mechanisms with respect to Ni determines its increased accumulation in aboveground parts.


1. Soils of the forest-steppe reserve in Transurals suffer from the technogenic pollution apparently connected to the aerial transfer of pollutants, due to the natural and technogenic environment in humus horizons of the soil it is noted an elevated level of Zn, Pb, Cu, Co, V, Ni, Mn, Cr, Ti.

2. Plants of the reserve under the conditions of high content of heavy metals in soils slightly accumulate some microelements showing the species-specific features at the same time.

3. As a rule, the amount of the heavy metals in the rhizome of plants is few times higher than in the aboveground organs; it is marked their localization in the periderm and bark cell walls.


[1.] Ilyin VB (1991) Heavy Metals in Soil-Plant System. Novosibirsk: Nauka, p. 284.

[2.] Alekseeva-Popova NV, Igoshina TI, Kositsyn AV, Ilyinskaya ML (1983) Heavy metal (Pb, Zn, Cu) tolerance of the separate species and populations of natural plant associations of copper-sulphide areas. In Plants in the Extreme Conditions of Mineral Nutrition. Leningrad: Nauka, pp. 22-24.

[3.] Andras P, Lichy A, Ruskova J, Matuskova L (2010) Heavy metal contamination of the landscape at the L'ubietova deposit (Slovakia). International Journal of Civil and Environmental Engineering 2: 67-70.

[4.] Jena VK, Gupta S, Patel KS, Patel SC (2013) Evaluating heavy metals contents in medicinal plant Mentha longifolia. Journal of Materials and Environmental Science 4(3): 384-389.

[5.] Seregin IV, Ivanov VB (1997) Histochemical methods for studying the distribution of cadmium and lead in plants. Plant Physiology 44(6): 915-921.

[6.] Ilyin VB, Syso AI, Baidina NL (2003) Background levels of heavy metals in the soils of the south of Western Siberia. Soil Science 5: 550-556.

[7.] Ilyin VB (1995) The system of indicators for the assessment of soil contamination by heavy metals. Journal of Agrochemicals 1: 94-99.

[8.] Kovalevsky AL (1991) Biogeochemistry of Plants. Novosibirsk: Nauka, pp. 18-48.

[9.] Nesterova AN (1989) The effect of heavy metals on the roots of plants, delivery, localization and mechanisms of plant resistance. Biological Sciences 9: 72-86.

[10.] Prasad MN (2003) Practical use of plants to restore the ecosystems contaminated by metals. Plant Physiology 5(50): 764-780.

[11.] Krzestowska M (2011) The cell wall in plant cell response to trace metals: Polysaccharide remodeling and its role in defense strategy. Acta Physiologiae Plantarum 1(33): 35-51.

[12.] Manara A (2012) Plant responses to heavy metal toxicity. In Plants and Heavy Metals, Springer Briefs in Biometals. Furini A (Ed.). DOI: 10.1007/978-94-007-4441-7_2.

[13.] Groshev IV, Grigoryeva OV (2006) The ecological role of heavy metals in the formation of biological resources of the steppe. In Biodiversity and Bioresources of the Urals and Adjacent Territories: Materials of the Third International Scientific Conference. Orenburg: IPK Gazprompechat, pp. 88-90.

[14.] Vazhenin IG (1984) Plant roots as a bioindicator of soil pollution by toxic elements. Journal of Agrochemicals 2: 73-77.

Published: 19th Dec 2014

Olga Zinovyevna Eremchenko, Natalia Viktorovna Moskvina *, Igor Evgenyevich Shestakov Perm State University, Bukireva Street, 15, 614990, Perm, Russia.

* Corresponding author
Table 1: Content of microelements in soils (layer 0-10 cm) and in
the parent rock, mg/kg of the burnt soil.

Element   Content in   Content in    Content in
          the parent   the black    the solonetz
             rock         soil

Ni            84           83          90
Co            16           20          25# *
Cr           460          344          320#
Mn          1,140        1,278       1,660# *
V            108         213#         236#
Ti          5,200       6,111#       7,000#
Cu            86           89          95 *
Zn            54         220#         253#
Pb            10          42#          54# *
Mo            3            2            2

Element    Percentage      Percentage
          abundance in      abundance
           lithosphere       in soil
          (according to   (according to
           Vinogradov)     Vinogradov)

Ni             58              40
Co             18               8
Cr             83              200
Mn            1,000            850
V              100             100
Ti            4,500           4,600
Cu             47              20
Zn             85              50
Pb             10              10
Mo              2               2

Note: Bold text denotes significantly different data on the
content of microelements in the soil relative to parent rock.

* Significant increase in the content of microelements in
solonetz compared with black soil.

Note: Significant different data on the content of microelements
in the soil relative ti parent rock are indicated with #.

Table 2: Average content of microelements in the aboveground parts
of plants, mg/kg of dry weight.

Species                  Ni        Co        Cr         Mn        V

Stipa pennata L.         4.8       0.4       5.1       34.5      2.3

Inula hirta L.           8.8       1.5       4.0       388.6     2.4

Galium ruthenicum        3.4       0.5       3.3       99.7      1.6

Fragaria viridis         9.2       1.2       6.3       221.0     2.1
(Duch.) Weston

Genista tinctoria        4.9       0.6       2.4       118.0     0.8
(L.) Maxim.

Filipendula ulmaria      9.8       1.1       9.4        420      4.6

Artemisia pontica L.     5.4       0.5       6.2        124      5.4

Festuca sulcata          7.6       0.5      12.6        32       2.1
(Hack.) Nym.

Percentage abundance     2.0       0.5       1.8        202      --
according to

Content according to     8.1       0.3       1.3        105      --
Ilyin (1991)

Content according to   0.5-2.1   0.1-0.2   0.1-0.6   27.5-75.0   --
Groshev and
Grigoryeva (2006)

Species                 Ti       Cu         Zn         Pb      Mo

Stipa pennata L.       87.0     5.9         5.3        1.8     0.1

Inula hirta L.         29.1     10.6       12.1        1.2     0.3

Galium ruthenicum      21.3     4.6         9.2        1.1     0.2

Fragaria viridis       34.0     13.8       11.9        5.1     0.3
(Duch.) Weston

Genista tinctoria      9.5      10.9        4.8        0.8     0.6
(L.) Maxim.

Filipendula ulmaria    108      11.0       23.0        2.4     0.9

Artemisia pontica L.    49      9.7         5.5        0.8     0.2

Festuca sulcata         19      6.4        13.9        2.0     0.2
(Hack.) Nym.

Percentage abundance    --      8.0        30.0        --      0.5
according to

Content according to    --      10.0       53.3        4.0     0.9
Ilyin (1991)

Content according to    --    3.0-14.3   10.2-35.8   0.1-1.3   --
Groshev and
Grigoryeva (2006)

Table 3: Microelements accumulation factor in underground parts
of the plants as compared with the aboveground parts (data on the
content in ash).

Species            Ni    Co    Cr    Mn     V

Genista            0.9   1.6   4.4   0.8   6.0
  (L.) Maxim.
Inula hirta L.     0.8   1.0   6.0   0.6   4.4
Fragaria           1.6   2.2   5.4   1.3   8.1
  (Duch.) Weston
Galium             1.7   2.0   8.4   1.1   2.6
Filipendula        0.8   1.3   1.3   0.4   1.8
  ulmaria Juss
Galatella          1.4   1.9   2.3   1.2   1.7
  (L.) Nees.
Plantago           1.8   1.4   2.6   2.7   7.5
  cornuti Gouan
Artemisia          1.4   1.6   1.0   1.7   4.1
  pontica L.
Artemisia          1.7   2.2   2.6   2.2   4.1
  nitrosa Web.

Species             Ti    Cu    ZnS    Pb    Mo

Genista            14.5   1.5   2.3   5.1    0.8
  (L.) Maxim.
Inula hirta L.     10.0   1.4   1.7   3.2    4.9
Fragaria           15.7   2.1   3.3   1.2    3.3
  (Duch.) Weston
Galium             9.6    1.6   2.2   1.4    2.7
Filipendula        2.1    1.2   1.1   1.0    0.7
  ulmaria Juss
Galatella          13.7   1.9   3.7   8.6    2.2
  (L.) Nees.
Plantago           10.6   4.1   4.1   13.6   1.0
  cornuti Gouan
Artemisia          1.6    1.0   1.3   1.3    1.5
  pontica L.
Artemisia          3.6    2.1   4.4   3.7    0.6
  nitrosa Web.

Table 4: Distribution of Pb in the tissues of rhizome of the plants.

Species            Time   Periderm   Outer   Inner
                   (h)               bark    bark

Fragaria viridis    1        +         -       -
(Duch.) Weston      24       ++        +       -
                    48       ++        +       -
                    72       ++        +       -
                   120      +++       ++       -
Filipendula         1        ++        +       -
ulmaria Juss        24       ++        +       -
                    48      +++        +       -
                    72      +++       ++       +
                   120      +++       ++       +
Artemisia           1        +         -       -
pontica             24       +         -       -
                    48       ++       ++       -
                    72       ++       ++       -
                   120       +         +       -

Species            Time   Endoderm   Pericycle   Vascular
                   (h)                           bundles

Fragaria viridis    1        -           -          -
(Duch.) Weston      24       -           -          -
                    48       -           -          -
                    72       -           -          -
                   120       -           -          -
Filipendula         1        -           -          -
ulmaria Juss        24       -           -          -
                    48       -           -          -
                    72       -           -          -
                   120       -           -          -
Artemisia           1        -           -          -
pontica             24       -           -          -
                    48       -           -          -
                    72       -           -          -
                   120       -           -          -

Note:--no coloring, + very weak, ++ weak, + + + strong, + + + +
very strong coloring.

Table 5: Distribution of Ni in the rhizome tissues of the plants.

Species        Time   Periderm   Outer   Inner
               (h)               bark    bark

Fragaria        1       +++       ++       -
viridis         24      +++       ++      ++
(Duch.)         48      ++++      +++     +++
Weston          72      ++++     ++++    ++++
               120      ++++      +++     +++
Filipendula     1        ++        +       -
ulmaria Juss    24      +++       +++     ++
                48      +++       +++     +++
                72      ++++     ++++    ++++
               120      ++++      +++     +++
Artemisia       1        ++        +       -
pontica         24      ++++      +++     +++
                48      ++++     ++++     +++
                72      ++++      +++     +++
               120      ++++      +++     +++

Species        Time   Endoderm   Pericycle   Vascular
               (h)                           bundles

Fragaria        1        -           -          -
viridis         24       ++         ++          ++
(Duch.)         48      +++         +++        +++
Weston          72      +++         +++        +++
               120      +++        ++++        ++++
Filipendula     1        -           -          -
ulmaria Juss    24       ++          +          +
                48       ++         ++          ++
                72       ++         ++         +++
               120      +++         +++        ++++
Artemisia       1        -           -          -
pontica         24       ++         ++          ++
                48      +++         +++        +++
                72      ++++       ++++        ++++
               120      ++++       ++++        ++++

Note: - no coloring, + very weak, ++ weak, + + + strong, + + + +
very strong coloring.
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Title Annotation:Research Article
Author:Eremchenko, Olga Zinovyevna; Moskvina, Natalia Viktorovna; Shestakov, Igor Evgenyevich
Publication:Biology and Medicine
Article Type:Report
Geographic Code:4EXRU
Date:Jul 1, 2014
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