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CIVIL AND ENVIRONMENTAL ENGINEERING REPORTS
E
-ISSN
2450-8594
CEER 2018; 28 (1): 130-145
DOI: 10.2478/ceer-2018-0011
Original Research Article
PHOTOSYNTHETIC APPARATUS EFFICIENCY OF SIDA
HERMAPHRODITA CULTIVATED ON HEAVY METALS
CONTAMINATED ARABLE LAND UNDER VARIOUS
FERTILIZATION REGIMES
Szymon RUSINOWSKI1, Jacek KRZYŻAK, Marta POGRZEBA
Institute for Ecology of Industrial Areas, Katowice, Poland
A b s t r a c t
Contaminated and marginal lands are favourable place for biomass feedstock
establishment, especially due to European Union directive 2009/28/EC. This strategy not
only cover local demand for energy and heat but also can be valuable in those land
phytomanagment. The second-generation perennial energy crop species are the most
feasible for such purpose. We studied the impact of two different fertilizer treatments on
plant physiological parameters associated with photosynthesis, heavy metals (HMs) and
primary macronutrients accumulation in Sida hermaphrodita cultivated on HMs
contaminated soil under field conditions. NPK fertilized plants showed the highest values
of photosynthetic parameters at the beginning of growing season when compared to
control and microbial inoculated plants. However, at the end of the growing season
inoculated and control plants showed better photosynthetic performance than NPK
treated. NPK fertilizer caused higher Cd and Zn shoot concentrations while microbial
inoculation caused higher K and the lowest N and P concentrations in shoot. Due to Cd,
Pb and Zn concentrations in plants which should not result in alleviation of photosynthetic
apparatus efficiency and biomass production it could be summarize that Sida
hermaphrodita is a suitable plant for cultivation on land contaminated with HMs under
different fertilization regimes.
Keywords: photosynthesis rate, chlorophyll fluorescence, Cd, Pb, Zn, senescence
1 Corresponding author: Institute for Ecology of Industrial Areas, Kossutha st 6,
40-844 Katowice, Poland, e-mail: s.rusinowski@ietu.pl, tel. +48322546031 ext. 231
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PHOTOSYNTHETIC APPARATUS EFFICIENCY OF
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CULTIVATED ON HEAVY METALS CONTAMINATED ARABLE LAND UNDER
VARIOUS FERTILIZATION REGIMES
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1. INTRODUCTION
Biomass is an organic material which derived from plants (including algae, trees
and crops), strictly from conversion CO2, water, mineral nutrients and the sunlight
in to carbohydrates, which are plant structure building matter, and oxygen via
photosynthesis [1]. The process and strength of photosynthesis directly affect the
yield and quality of plants [2]. Besides the classic measurements of
photosynthesis activity of plants by gas-exchange analysis, chlorophyll
fluorescence allow evaluating photosynthesis apparatus status of plants based on
detection changes in some photosystem II (PSII) components, electron transport
chain components, and light dependent photochemical reactions [3,4].
Additionally, chlorophyll content has great importance in estimation
photosynthetic apparatus efficiency and general plant health [5].
Due to conventional energy sources decrement any environmental-saving
technology, especially in industry, are desirable. Limitation of conventional heat
production technology, based mainly on fossil fuels for increase usage of bio-
based energy sources, especially biomass is the first step to improve environment
condition.
Renewable energy directive (RED) 2009/28/EC [6] promote usage of renewable
energy sources in the members of European Union. These countries have to
increase the share of renewable energy of gross final energy consumption to 20
% in 2020. That directive also excludes several land categories from biomass
production, especially lands with high biodiversity value and high carbon stock,
what made marginal and degraded lands a favourable place to energy crops
cultivation [7].
Marginal lands could be contaminated by many different compounds or/and
harmful elements, which have got anthropogenic or environmental origin. That
contamination can significantly affect the quality of agricultural products [8].
Heavy metals could alter the photosynthetic activity indirectly, decreasing the
content of photosynthetic pigments or damaging the photosynthetic apparatus on
every level of its organization [9]. For this reason, analysis of energy crops
photosynthetic apparatus efficiency, while growing on contaminated soil is very
important.
Cultivation of energy crops on such contaminated soil especially on heavy metal
contaminated (HMC) soil can be profitable not only in biomass production but
also in phytoremediation [10].
Nowadays biomass production is focused on second generation bioenergy crops.
Such plants have got less inputs requirement, produce more energy and reduce
greenhouse gases emission more than annual crop species belonging to first
generation [11]. Sida hermaphrodita as a C3 photosynthesis perennial plant
species was already cultivated for energy purposes [12,13].
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The aim of the study was to assess influence of two different fertiliser treatments
on plant physiological parameters associated with photosynthesis, heavy metals
(HMs) and primary macronutrients accumulation in S. hermaphrodita cultivated
on HMs contaminated soil under field conditions.
2. MATERIALS AND METHODS
2.1. Site description
The experimental plots were established on contaminated arable land in Bytom
(Upper Silesia), Poland (50°20'43.1"N 18°57'17.9"E) at the beginning of the 2014
growing season, on the area lease by the Institute for Ecology of Industrial Areas.
Soil contamination with zinc, cadmium and lead on described area resulted from
Pb/Zn smelting activity over the last century. Total soil heavy metals (HMs)
concentration exceed the threshold values proscribed by Polish government
regulation [14], excluding this area from food production. Yearly average values
of temperature and sum of precipitation measured during the third growing season
(May 2016 – September 2016) were 17.5°C and 450 mm respectively (Institute
of Meteorology and Water Management, Poland).
2.2. Experiment design
Roots seedlings of Sida hermaphrodita were planted at 10 cm depths from direct
root cuttings which were originated from an uncontaminated site and pre-
cultivated in controlled conditions. In the middle of the May 2014 on each from
three plots 49 plants were planted over an area of 16m2 (3 plants per 1m2) with a
buffer zone of 4m between each plot which protected plants against uncontrolled
fertilisation. Single plot trials with pseudo-replication were performed due to high
soil homogeneity on the field before experiment establishment. During plantation
establishment, each plot was treated in different way:
SH I – control, untreated plot
SH II – plot treated with standard NPK chemical fertilizers (ammonium
sulphate and Polifoska - 4% N, 22% P2O5, 32% K2O) once before planting.
Dose was adjusted according to El Bassam [15] and amounts of applied
macronutrients were as follow: nitrogen 100 kg ha-1, phosphorus 80 kg ha-1 as
P2O5 and potassium 120 kg ha-1 as K2O.
SH III – plot treated with microbial inoculum (Emfarma Plus® ProBiotics,
Poland) which consist of Lactic Acid Bacteria > 3.0 × 105 CFU ml-1, Yeast <
1.0 × 106 CFU ml-1 and Purple Non-Sulfur Bacteria > 1.0 × 104 CFU ml-1 in
molasses suspension. Inoculum (10% water solution) was applied on roots
and on soil surface (8l per plot) before planting. In addition, plant leaves were
treated monthly during the growing season by aerosol treatment (8l per plot).
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2.3. Soil physico-chemical parameters
Results from initial soil physico-chemical analyses including: pH, EC, organic
matter content (OM), concentration of elements N, P, K, Mg, Ca, Fe, Pb, Cd, Zn
as well as bioavailable forms of analysed heavy metals (Pb, Cd, Zn) were
previously reported for investigated plots by Pogrzeba et al. [12] (Table 1).
Table 1. Soil physico-chemical characteristic according to Pogrzeba et al. [12]
Experimental variants
Soil parameters SH I SH II SH III
pH 6.50 ± 0.04a
6.48 ± 0.06a
6.58 ± 0.09a
EC (µS cm-3) 87.57 ± 3.25a
87.72 ± 1.67a
89.44 ± 2.29a
OM (%) 6.20 ± 0.16a
6.22 ± 0.23a
6.52 ± 0.27a
N (%) 0.18 ± 0.01a
0.17 ± 0.01a
0.18 ± 0.01a
P (g kg-1) 1.02 ± 0.01a
0.99 ± 0.00a
0.99 ± 0.00a
K (g kg-1) 0.98 ± 0.00a
0.97 ± 0.00a
1.02 ± 0.01a
Mg (g kg-1) 2.22 ± 0.01b
2.33 ± 0.01b
2.94 ± 0.01a
Ca (g kg-1) 4.50 ± 0.02b
4.83 ± 0.01b
5.60 ± 0.03a
Fe (g kg-1) 11.85 ± 0.01a
11.96± 0.02a
12.10 ± 0.04a
Pb (mg kg-1) 635.6 ± 3.7a
637.7 ± 5.4a
639.1 ± 8.1a
Cd (mg kg-1) 25.70 ± 0.48a
26.01 ± 0.28a
26.04 ± 0.38a
Zn (g kg-1) 2.36 ± 0.01a
2.42 ± 0.01a
2.46 ± 0.01a
Pbbio (mg kg-1) LOQ
LOQ
LOQ
Cdbio (mg kg-1) 1.87 ± 0.1a
1.85 ± 0.07a
1.71 ± 0.18a
Znbio (mg kg-1) 110.10 ± 6.67a
107.42 ± 4.11a
95.66 ± 13.19a
SH I – control plots, SH II – NPK fertilized plots, SH III – microbial inoculated plots,
EC – electrical conductivity, OM – organic matter,
bio – bioavailable fraction of heavy metals, LOQ – limit of quantification.
A lower-case letters (a, b) denotes significant differences among soils samples taken
from different plots at P ≤ 0.05 according to Fisher LSD test.
Values are means ± SE (n = 3)
2.4. Gas exchange, plant pigment content and chlorophyll a fluorescence
measurements
Gas exchange measurements were performed monthly (June – August) on each
plot using Infra-Red Gas Analyser (Lc ProSD, ADC Bioscientific, UK) with
measuring chamber set on climate condition (21°C, 1500 PAR, CO2 ambient) For
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measurements from each plot 3 plant were selected and on each plant
measurements were performed on two young fully developed leaves.
Plant pigment content measurements were performed monthly (June – August)
on each plot using plant pigment content meter (Dualex Scientific+, FORCE-A,
France). Measurements were performed on the same plants where gas exchange
measurements were performed.
Chlorophyll a fluorescence measurements were performed monthly (June –
August) on each plot using fluorimeter (Handy Plant Efficiency Analyzer,
Hansatech Instruments Ltd, UK). Measurements were performed at night when
samples were adapted to darkness, on the same plants where gas exchange and
plant pigment content measurements were performed.
2.5. Concentration of heavy metals and primary mineral macronutrients
in plants
Three plant shoots from each of investigated plants were collected at the end of
third growing season (October 2016) on each plot. Concentration of metals in the
plant shoots was determined by hot plate digestion and flame atomic absorption
spectrometry (SpektrAA 300, Varian INC., USA). Plant samples were digested in
nitric and perchloric acid (4:1 v/v) [16]. Total nitrogen concentration (N) in plant
shoots was assessed using the method described by Bremner [17], whereas total
phosphorus (P) and potassium (K) concentration in plant shoots were assessed
using ICP (Liberty 220, Varian, USA) in previously digested samples.
2.6. Statistical analysis
One-way ANOVA followed by post-hoc LSD test at P ≤ 0.05 were used to
distinguish differences between experimental variants during each month as well
as to distinguish differences between values obtained during June, July and
August measurements separately for each experimental variant.
3. RESULTS AND DISSCUSSION
3.1. Soil characteristics
Physical and chemical soil parameters are presented in Tab. 1 according to
Pogrzeba et al. [12]. Heavy metal concentrations in the soil exceeded Polish limits
for food crop production [18]. The pH was almost neutral, followed by high
content of organic matter (OM) and low electrical conductivity (EC). Despite low
Pb bioavailability, presented results indicate high concentration of Cd and Zn
bioavailable forms. There is almost no differences between plots in initial soil
characteristic what indicate that soil is highly homogenous.
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3.2. Gas exchange parameters
Gas exchange parameters are presented in Fig. 1. Photosynthesis rate (Fig. 1a)
showed no differences between experimental variants within each month, while
considering differences between month, it was found that photosynthesis rate
decrease consequently from June to August. Despite the fact that there were no
differences between experimental variants, there is tendency suggesting that NPK
treated plants showed the best photosynthesis rate in the June while the worst in
the August.
The highest transpiration rate (Fig. 1b) were found in June for plant treated with
chemical fertilizer, lower for inoculum treated plants and the lowest for control.
It was found that there were no differences between experimental variants in
August, however obtained values were about 43% lower when compare to June
measurements. Values obtained during August measurements indicate the same
tendency between experimental variants as found in photosynthesis rate.
Transpiration rate measured in June was the highest among all experimental
variants. Values obtained in August were about 30% higher when compare to
those obtained in July.
There is dearth of papers considering direct measurement of photosynthesis using
IRGA on Sida hermaphrodita. Kocoń and Jurga [13] performed this type of
measurements on S. hermaphrodita, however those were performed once a year,
in spring, on young plants, with use of different chamber set up than used in the
present study. Rosenthal et al. [19] performed continuous measurements of
photosynthesis on Glycine max during two growing seasons (from June –
September). They reported start of photosynthesis rate parameter decrease at the
turn of August and September. Constant decrease of photosynthesis rate during
growing season in present report could be associated with presence of HMs in soil
and induced senescence by reactive oxygen species (ROS) [20], this fact could be
additionally supported by month by month decreasing tendency visible for values
obtained for chlorophyll content and chlorophyll fluorescence vitality index
(Fv/Fm).
3.3. Plant pigment content
Chlorophyll content measured in June showed the highest value for plants treated
with chemical fertilizer and untreated, significantly lower values were found for
inoculated plants. In July, it was found increasing tendency of chlorophyll content
for control and inoculum treated plants while decrease was reported for NPK
treated. The chlorophyll content in July was higher by about 3 relative units (r.u.)
in control and inoculum treated plants when compare to NPK fertilized. In August
decrease of chlorophyll content in all experimental variants was found. There
were no statistically significant differences between experimental variants,
however tendency with the lowest value for NPK treated plants still occur in
August.
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Fig. 1. Influence of NPK fertilization (SH II) and microbial inoculation (SH III) on (a)
photosynthesis rate and (b) transpiration rate of Sida hermaphrodita in June,
uly and August 2016 growing season. Values are means ± SE (n = 18). Capital letters
(A, B, C) denote significant differences among parameters in plants on different plots
within one month, while lower case letters (a, b, c) denote significant differences among
parameters between months within one experimental variant at P ≤ 0.05 according to
Fisher LSD test.
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Anthocyanins content was on the same level in each experimental variant on June
and July. High decrease of anthocyanins was found in August for each
experimental variant when compare to June and July. Although, there were no
statistically significant differences between experimental variants the highest
anthocyanins content was found for plant treated with NPK fertilizer while the
lowest for plants treated with microbial inoculum.
The progression of leaf senescence is most commonly monitored as chlorophyll
degradation [21, 22]. Anthocyanin accumulation begins shortly after the onset of
chlorophyll decline, typically before any visible change in leaf color appear. This
could demonstrate a direct association between anthocyanin production and the
period of increased vulnerability to photoinhibition during senescence, and
suggest that anthocyanins may perform a photoprotective role in autumnal
foliage. In addition, under stressful conditions, even moderate irradiances can
induce photoinhibitory damage to plants [23]. This statement could additionally
be supported by the fact that there were significant negative Pearson’s correlations
between anthocyanins and chlorophyll (r = -0.621, p=0.000), photosynthesis rate
(r = -0.399, p = 0.000) and Fv/Fm (r = -0.435, p = 0.000)
3.4. Chlorophyll a fluorescence parameters
The most common parameters obtained from chlorophyll a fluorescence
measurements are Fv/Fm (Maximum quantum yield of primary photochemical
reactions) that indicates the probability of trapping the energy of absorbed
photons by PSII reaction centres and PIABS (Performance index) an indicator of
PSII functional activity normalized to the absorbed energy [24,25].
Those parameters are usually described as vitality indices [25]. The Fv/Fm
parameter was the highest for fertilized plants while the lowest for control plants
in June. There were no differences between experimental variants in July,
however in August NPK fertilized plants showed the lowest Fv/Fm values when
compare to the other experimental variants. General tendency indicate that Fv/Fm
parameter consequently decrease from June to August. Performance index
showed slightly different behavior when compare to Fv/Fm. The PIABS in June was
23% lower in control plants and those treated with microbial inoculum when
compare to NPK fertilized plants. There were no differences between
experimental variants in July while considering PIABS parameter. The control
plants showed significantly lower values of PIABS when compare to inoculum
treated plant in August. There were no differences between NPK treated plants
and other experimental variants. Control plants did not differ significantly
between months. Inoculum treated plants had the same value of PIABS in June and
July while decrease of this parameter was reported in August. The PIABS measured
for NPK treated plants decreased in July when compare to June, however it
increased in August when compare to July to value similar to this obtained in
June.
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Fig. 2. Influence of NPK fertilization (SH II) and microbial inoculation (SH III) on (a)
chlorophyll content and (b) anthocyanins content of Sida hermaphrodita in June,
July and August 2016 growing season. Values are means ± SE (n = 12). Capital letters
(A, B, C) denote significant differences among parameters in plants on different plots
within one month, while lower case letters (a, b, c) denote significant differences among
parameters between months within one experimental variant at P ≤ 0.05 according to
Fisher LSD test.
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CULTIVATED ON HEAVY METALS CONTAMINATED ARABLE LAND UNDER
VARIOUS FERTILIZATION REGIMES
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Fig. 3. Influence of NPK fertilization (SH II) and microbial inoculation (SH III) on (a)
Fv/Fm and (b) PIABS of Sida hermaphrodita in June, July and August 2016 growing
season. Values are means ± SE (n = 12). Capital letters (A, B, C) denote significant
differences among parameters in plants on different plots within one month, while lower
case letters (a, b, c) denote significant differences among parameters between months
within one experimental variant at P ≤ 0.05 according to Fisher LSD test.
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3.5. Heavy metals and mineral macronutrients concentration in plant
shoots
Heavy metals and mineral macronutrients concentration in plants shoots was
presented on Table 2. It was found that on each plot Pb concentration was below
detection limit, this phenomenon could be associated with low bioavailability of
this element in the soil [26]. Cadmium concentration in shoots was the highest in
NPK fertilized plants, while it was about 24% lower in control and inoculum
treated plants. Similar tendency was found for Zn shoot concentration, however
control and NPK fertilized plants showed significantly higher values by about
30% and 41%, respectively when compare to inoculum treated plants. Control
plants showed the highest shoot N concentration among experimental variants. It
was 0.23% and 0.30 % higher when compare to NPK and inoculum treated plants
respectively. Similar tendency was observed for shoot P concentration. The
highest shoot K concentration was found simultaneously for NPK and inoculum
treated plants and it was nearly 20% higher when compare to control plants.
The highest heavy metals concentration in NPK treated plant shoots (particularly
Cd and Zn) could be associated with application of chemical fertilizer which could
increase the mobility of heavy metals by reducing pH value. This phenomenon
occurs due to the presence of NH4+ in chemical fertilizers as the N-source, which
results in H+ extrusion by the roots and acidification of the soil [27]. Similar
phenomenon was observed for Miscanthus x giganteus on the same field [28].
Although, concentration of Cd and Zn in plants shoots did not exceed toxic
concentration describe by Kabata-Pedias [29] it could slightly affect
photosynthetic apparatus efficiency, especially in senescent plants due to its
higher sensitivity to stress factors. This could explain results obtained for NPK
fertilized plants comparing to other treatments. The highest value of chlorophyll
content, Fv/Fm, photosynthesis rate and transpiration rate in June for NPK
fertilized plants could be associated with better supplementation, however the
lowest value of those parameters for the same plants in August could be associated
with combined effect of senescence and the highest HM concentration in NPK
fertilized plants shoots. The lowest concentration of N and P in inoculated plant
shoots could be associated with competition between plant roots and applied
monthly microorganisms as well as indigenous rhizosphere microorganisms. This
phenomenon could be associated with molasses included in inoculum formula,
which derived easily decomposable C and prime microorganisms (microbial
activation) for achieving additional N from soil organic matter decomposition
[30].
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CULTIVATED ON HEAVY METALS CONTAMINATED ARABLE LAND UNDER
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Table 2. Heavy metals and primary macronutrients concentration in plant shoots
SH I SH II SH III
Pb (mg kg-1)
LOQ
LOQ
LOQ
Cd (mg kg-1)
2.46 ± 0.47b
3.06 ± 0.10a
2.23 ± 0.39b
Zn (mg kg-1)
163.3 ± 8.6b
195.7 ± 12.8a
117.2 ± 10.1c
N (%)
0.74 ± 0.03a
0.51 ± 0.03b
0.44 ± 0.03c
P (mg kg-1)
866.2 ± 66.9a
659.6 ± 72.6b
511.2 ± 42.6c
K (g kg-1)
9.28 ± 0.87b
11.11 ± 0.56a
11.66 ± 1.11a
SH I – control plots, SH II – NPK fertilized plots, SH III – microbial inoculated
plots, LOQ – limit of quantification. A lower-case letters (a, b, c) denotes
significant differences among elements concentration in plant shoots taken from
different plots at P ≤ 0.05 according to Fisher LSD test.
Values are means ± SE (n = 9)
4. CONCLUSIONS
In conclusion, application of different fertilizers did not affect photosynthesis
apparatus efficiency when compared to control. Heavy metals concentration in
shoots did not exceed toxic concentration thresholds for higher plants. Based on
chlorophyll and anthocyanins content it could be assumed that plant senescence
begins at turn of July and August. Senescence could increase vulnerability of
photosynthetic apparatus to heavy metal toxicity. It could be summarized that
Sida hermaphrodita is plant suitable for cultivation on land contaminated with
HMs under different fertilization regimes.
5. ADDITIONAL INFORMATION
The project is implemented under Maria Curie Skłodowska Actions of the 7
Framework Programme of the EU (Grant agreement No. 610797). Research
received additionally financial support from Institute for Ecology of Industrial
Area statutory founds.
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WYDAJNOŚC APARATU FOTOSYNTETYCZNEGO SIDA HERMAPHRODITA
UPRAWIANEGO NA GLEBIE ZANIECZYSZCZONEJ METALAMI CIĘŻKIMI
W WARUNKACH ZRÓŻNICOWANEGO NAWOŻENIA
S t r e s zc z e n ie
Tereny zanieczyszczone i odłogowane stanowią opcję dla uprawy roślin na cele
energetyczne, szczególnie jeśli weźmie się pod uwagę rozporządzenia dyrektywy Unii
Europejskiej w sprawie promowania stosowania energii ze źródeł odnawialnych
(2009/28/EC). Spełnienie jej wymogów może być po części zrealizowane poprzez uprawę
roślin energetycznych drugiej generacji. Zastosowanie takiego podejścia pozwoli nie
tylko pokryć lokalne zapotrzebowanie na odnawialne źródła energii, ale także wspomóc
zarządzanie terenami nieprzydatnymi w produkcji roślin na cele żywnościowe oraz
paszowe. W przedstawionej pracy badano wpływ zastosowania zróżnicowanego
nawożenia na parametry fizjologiczne ślazowca pensylwańskiego uprawianego na glebie
zanieczyszczonej metalami ciężkimi. Rośliny nawożone standardowymi nawozami
mineralnymi charakteryzowały się wyższymi wartościami parametrów fizjologicznych na
początku sezonu wegetacyjnego, podczas gdy na końcu sezonu wegetacyjnego wyższe
wartości stwierdzono dla roślin w wariancie kontrolnym i szczepionką mikrobiologiczną.
Nawożenie mineralne spowodowało wyższe zawartości Cd i Zn w roślinach, podczas gdy
rośliny traktowane szczepionką mikrobiologiczną miały wyższe zawartości K oraz
najniższe zawartości N i P w częściach nadziemnych. Stwierdzone zawartości Pb, Cd I Zn
w częściach nadziemnych ślazowca pensylwańskiego nie powinny mieć negatywnego
wpływu na stan aparatu fotosyntetycznego i wydajność produkcji biomasy. W związku
Unauthentifiziert | Heruntergeladen 30.09.19 12:23 UTC
PHOTOSYNTHETIC APPARATUS EFFICIENCY OF
SIDA HERMAPHRODITA
CULTIVATED ON HEAVY METALS CONTAMINATED ARABLE LAND UNDER
VARIOUS FERTILIZATION REGIMES
145
z tym roślina ta może być przydatna w produkcji biomasy na cele energetyczne na ternach
zanieczyszczonych.
Słowa kluczowe: Natężenie fotosyntezy, fluorescencja chlorofilu, Cd, Pb, Zn,
starzenie
Editor received the manuscript: 31.08.2017
Unauthentifiziert | Heruntergeladen 30.09.19 12:23 UTC
