Journal of Photochemistry and Photobiology B: Biology xxx (2014) xxx–xxx

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Journal of Photochemistry and Photobiology B: Biology

journal homepage: www.elsevier.com/locate/jphotobiol

Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs)

on photosynthetic performance are not related to their aromaticity
Anjana Jajoo a,⇑, Nageswara Rao Mekala b, Rupal Singh Tomar a, Michele Grieco b, Mikko Tikkanen b,
Eva-Mari Aro b
a
School of Life Sciences, Devi Ahilya University, Indore, MP, India
b
Department of Biochemistry, Molecular Plant Biology, University of Turku, FI-20014 Turku, Finland

a r t i c l e i n f o a b s t r a c t

Article history: Polycyclic aromatic hydrocarbons (PAHs) are very toxic and highly persistent environmental pollutants
Received 14 November 2013 which accumulate in soil and affect growth of the plants adversely. This study aims to investigate inhib-
Received in revised form 15 March 2014 itory effects of 3 major PAH particularly on photosynthetic processes in Arabidopsis thaliana grown in soil
Accepted 17 March 2014
treated with PAH. The 3 PAH chosen differ from each other in aromaticity (number of rings) comprising
Available online xxxx
their structure (2 rings: naphthalene, 3 rings: anthracene and 4 rings: pyrene). Several growth parame-
ters and Chlorophyll a fluorescence was monitored in PAH treated plants. BN-PAGe analysis was done in
Keywords:
order to get information about change in the protein conformation. PAH treatment led to increased value
Photosynthesis
Polycyclic aromatic hydrocarbons (PAHs)
of Fo which collaborated with increase in the amount of free LHC as seen through BN-Page analysis. Thus
Photosystem II PAH were found to inhibit PS II photochemistry and caused distinct change in pigment composition.
Chlorophyll fluorescence However the results led us to infer that 3-ring anthracence is more inhibitory as compared to 2-ring
naphthalene and 4-ring pyrene. This indicates that aromaticity of PAH is unrelated to their response
on photosynthetic processes.
Ó 2014 Elsevier B.V. All rights reserved.

1. Introduction
Several industrial activities carried out by human beings,
involving combustion of fossil fuels, oil spills and so on, has during
the last few decades released various harmful chemical substances
to the environment. Of the numerous environmental pollutants,
polycyclic aromatic hydrocarbons (PAHs) are among the most toxic
and highly persistent [1]. PAHs can disturb several physiological
processes in plant and thus reduce crop yields [2]. This problem
is of great significance since PAHs are commonly present in water,
air, soil, food and living organisms. As much as 90% of PAHs accu-
mulates in the soil due to their hydrophobic character, which in
turn favours their rapid association with soil solid particles and
their permeation to bottom sediments [3].
Polycyclic aromatic hydrocarbons are Persistent, Bio-accumula-
tive and Toxic (PBT) compounds. PAHs are relatively inert com-
pounds, resistant to various degradation processes and therefore
it is generally supposed that PAHs are persistent in the environ-
ment [4]. However the reactivity of PAHs is influenced by several
factors like temperature, light, oxygen (O2), ozone (O3) and other
⇑ Corresponding author. Tel.: +91 731 2477166; fax: +91 731 4263453.
E-mail address: anjanajajoo@hotmail.com (A. Jajoo).
chemical reagents [5]. Plants are capable of taking up PAHs from
the environment. Investigation of the influence of selected PAHs
on higher plants is very important due to the fact that plants are
dominant components of terrestrial ecosystems with ability of
their uptake from the environment. For these reasons, plants are
used as early indicators of environment pollution [6]. The evalua-
tion of biological parameters is likely to allow faster and econom-
ical preferable pollution information than complex chemical
analyses. Therefore, some plant species may be used for detoxifica-
tion of the environment. PAHs commonly found in the environ-
ment include anthracene, benz(a)anthracene, benz(a) pyrene,
fluorene, fluoranthene, naphthalene and phenanthrene.
PAH-induced responses in plants involve interference with
membrane-mediated physiological and biochemical processes like
membrane permeability, enzymatic dysfunction, and photosynthe-
sis [7]. Because PAHs partition primarily into thylakoids, it is con-
ceivable that they have an influence on the ordered arrangement of
chloroplasts and interfere with electron transport and photosyn-
thesis [8]. It is also known that PAHs affect both the primary and
secondary processes of photosynthesis. The multifaceted action
of PAHs observed in treated plants has provided evidence that
hydrophobic PAHs accumulate in thylakoid membranes [7] and
may induce conformational changes in their structures, thus

http://dx.doi.org/10.1016/j.jphotobiol.2014.03.011
1011-1344/Ó 2014 Elsevier B.V. All rights reserved.

Please cite this article in press as: A. Jajoo et al., Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs) on photosynthetic performance are not
related to their aromaticity, J. Photochem. Photobiol. B: Biol. (2014), http://dx.doi.org/10.1016/j.jphotobiol.2014.03.011
2 A. Jajoo et al. / Journal of Photochemistry and Photobiology B: Biology xxx (2014) xxx–xxx

causing disturbance of electron transport at both the donor and
acceptor side of PSII [9,10]. Some PAH like anthracence inhibit pho-
tosynthetic activities of green alga due to lowering of quantum
efficiency of electron trapping and transport and impairment of
PSII and PSI. Lower activity of the oxygen evolving complex
(OEC) is observed in anthracene treated algal cells [9]. It is also
reported that anthracene inhibits carbon fixation, thus lowering
net photosynthesis [11]. Other PAHs like phenanthrene and pyrene
also decrease net photosynthesis. In higher plants, phenanthrene
and pyrene exposure caused a decrease in growth, photosynthetic
pigment contents, stomatal conductance, maximal quantum yield,
effective quantum yield of PSII and photochemical quenching coef-
ficient [12]. Cyanobacteria were found to be more tolerant to pyr-
ene stress when compared with eukaryotic algae [13].
Separation of thylakoid membrane protein complexes by large
pore Blue-Native (lpBN)-PAGE was carried out following the
method as explained in Jarvi et al. [15].
3. Results and discussion
To investigate the contribution of aromaticity (number of rings)
of PAH in causing inhibitory effects on plant growth, three PAH,
naphthalene (NAP), anthracene (ANT) and pyrene (PYR) were used
in this study. Plants grown without PAH and with PAH showed
very distinct morphological differences. As shown in Fig. 1 control
and PAH-treated plants showed distinct difference in growth and
the phenotype of plants. The rosettes of control plants showed
good growth and green leaves. However, there was a decline in leaf

This study was focused to assess whether the damage caused by size in PAH-treated plants, being more prominent in plants grown
PAH in plants is influenced by the number of rings comprising the in the presence of PYR and least prominent in the presence of
structure of the PAH. To test this, several photosynthetic parame- naphthalene. ANT and PYR treated plants exhibited small leaves,
ters were estimated in the plants treated with PAH having 2 rings decoloration of leaves and stunted growth. Table 1 shows the
(Naphthalene), 3 rings (Anthracene) and 4 rings (Pyrene). actual changes in the leaf size, fresh weight in control and PAH-
treated plants.
The pigment content of control and PAH-treated plants was
2. Materials and methods
estimated by using HPLC. As shown in Fig. 2 there is a difference
in the amounts of chlorophyll and carotenoid pigments in the con-
Wild-type Arabidopsis thaliana (ecotype Columbia) and PAH
trol and PAH-treated plants. The content of Chl a and Chl b
treated plants were grown for 6 weeks in phytotron in a mixture
decreased in PAH-treated plants while almost the same amount
of soil and vermiculite (1:1) under constant moderate light
of carotenoids was found in all plants. Nevertheless, the pigment
(150 lmol photons m 2 s 1), 8 h photoperiod and relative humid-
content was found to be lower in ANT treated plants as compared
ity of 60%. Light was provided by OSRAM Power Star HQIT 400/D
to NAP and PYR treated plants.
Metal Halide Lamps. Plants were replenished every day with nutri-
Photosynthetic parameters were next estimated by measuring
ent solution without PAH (control) and with PAH. PAH (Sigma–
Chl a fluorescence using the intact leaves from control and PAH-
Aldrich, USA) were dissolved in acetone for stock of 5 mM. This
treated plants. As the first approach to investigate photosynthesis
PAH stock solution was delivered to water to final PAH concentra-
tions of 25 lM. It was found that the concentration of dissolvent
did not affect seed germination and growth of seedlings and other
physiological parameters [14]. After 5 weeks of treatment, signifi-
cant changes in the plants were observed. The leaves were used
for the measurements of pigment analysis and chlorophyll (Chl)
a fluorescence while from some leaves, thylakoids were isolated
in order to carry out protein profiling. Pigment analysis was carried
out using high performance liquid chromatography (HPLC).
Flash fluorescence induction measurements were carried out at
room temperature by using the FL3500 dual-modulation fluorom-
eter (Photon System Instruments, Czech Republic). The samples
were excited with blue light (480 nm Corion narrow-band filter)
obtained by filtering the light from a slide projector. Light intensity
reaching the leaf was 3000 lmol m 2 s 1, sufficient to generate
maximal fluorescence (Fm) for all the treatments. The plant leaf
was dark-adapted for 15 min using leaf clip before fluorescence
measurement. The measurements were performed 1 cm away
from the tip and the bases i.e. in the middle portion on the ventral
(abaxial) surface of the leaves. Fluorescence measurements were
made on 5 plants of each treatment and around 5 recording on dif-
ferent leaves were done on each plant. Thus overall 25 measure-
ments were done on each treated plant. The results presented
show the averaged spectra of around 20–25 readings. The whole
set of experiments was carried out thrice. Details of measurement Fig. 1. Phenotype of Arabidopsis thaliana in control and PAH treated plants (25 lM
of Photosystem II heterogeneity can be seen in [14]. of NAP, ANT and PYR) after 6 weeks.

Please cite this article in press as: A. Jajoo et al., Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs) on photosynthetic performance are not
related to their aromaticity, J. Photochem. Photobiol. B: Biol. (2014), http://dx.doi.org/10.1016/j.jphotobiol.2014.03.011
 A. Jajoo et al. / Journal of Photochemistry and Photobiology B: Biology xxx (2014) xxx–xxx
Table 1
2 1
Morphological characteristics of Arabidopsis plants grown at 150 lmol photons m
Parameter studied Control
Max. length of leaf (cm) 3.6 ± 0.3
Min. length of leaf (cm) 2.2 ± 0.1
Max. width of leaf (cm) 1.6 ± 0.1
Min. width of leaf (cm) 1.0 ± 0.1
Fresh weight (1 rosette) (g) 2.54 ± 0.2
as a potential site of action for PAH, Chl a fluorescence induction
was measured in control and PAHs treated plant leaves (Fig. 3).
Measurement of Chl a fluorescence allows to evaluate primary
photochemical reactions of photosynthesis, efficiency of Photosys-
tem II (PSII) and the electron transport chain [16]. From the Chl
fluorescence induction curves, several parameters which describe
photochemical events taking place particularly at PS II were
derived. Remarkable changes in most of the parameters of Chl a
fluorescence were observed at 25 lM PAH. In PAH-treated plants,
a significant decrease in Fv/Fm and an increase in initial fluores-
cence (Fo) values were observed (Table 2), where Fv is the variable
fluorescence (Fm–Fo), and Fm is the maximal fluorescence. Altera-
tions in these parameters represent damage to the PSII reaction
centers, reduced photosynthetic capacity and photochemical effi-
ciency [17], concomitant damage or impairment of the leaf photo-
synthetic system as well as reduced photosynthetic CO2 fixation
[18]. Elevated Fo recorded in PAH-treated plants may be because
of dissociation of the antennae complexes in PSII which was later
tested by analyzing BN-PAGE data. Increased Fo can be also caused
by enhanced reduction of PQ-pool by NDH-complex or by the dam-
age of Photosystem I (PSI) (limitation at PSI). The efficiency of the
water-splitting complex on the donor side of PSII can be under-
stood by measurement of Fv/Fo ratio [19]. The value of Fv/Fo
decreased by more than 50% at 25 lM PAH concentration in all
PAHs. Fraction of active oxygen evolving complexes was calculated
and a significant decrease (50%) in the number of oxygen evolving
complexes in PAH exposed plants was observed.
To localize the effects of PAH on the acceptor side of PS II, the
values of relative variable fluorescence (Vj), which is equivalent
to (Fj–Fo/Fm–Fo) was calculated. The efficiency by which a trapped
electron can move further ahead of QA is equal to (1 Vj) or wo. In
the present study, no change was observed in the value of 1 Vj in
PAH-treated plant suggesting that re-oxidation capacity of QA and
Fig. 2. HPLC Analysis of pigment content of control and PAH-treated Arabidopsis
thaliana plants grown for 6 weeks. Leaf discs were taken from the plants and
extracted with methanol.
Please cite this article in press as: A. Jajoo et al., Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs) on photosynthetic performance are not
related to their aromaticity, J. Photochem. Photobiol. B: Biol. (2014), http://dx.doi.org/10.1016/j.jphotobiol.2014.03.011
3
s for 5 weeks. Leaf size was measured from six plants of each treatment (n = 6 ± SE).
Naphthalene Anthracene Pyrene
2.8 ± 0.2 2.1 ± 0.2 2.0 ± 0.2
1.8 ± 0.2 1.4 ± 0.2 1.3 ± 0.1
1.2 ± 0.2 1.0 ± 0.1 1.0 ± 0.1
0.8 ± 0.1 0.6 ± 0.1 0.5 ± 0.1
1.44 ± 0.1 0.83 ± 0.1 0.78 ± 0.11
Fig. 3. Chl a fluorescence induction curves measured in control and PAH treated
plants. Experimental details are provided in Section 2.
electron transport at the acceptor side of PSII remain unaffected by
PAH treatment. It is noticeable that the changes in Chl fluorescence
parameters were most prominent in ANT treated plants as com-
pared to NAP and PYR treated plants.
A number of papers have reported negative effects of PAH on
PSII, however, none of them has addressed whether the effect of
PAH is dependent on PSII heterogeneity. Different from other
pigment protein complexes participating in photosynthetic light
reaction, PSII shows diverse nature in structural and functional
aspects and this is termed as PSII heterogeneity. The most intrigu-
ing observation is that the extent and nature of PSII heterogeneity
is dependent on environmental conditions i.e. salinity, osmotic,
temperature and pH stress [20–22]. Two major types of PSII heter-
ogeneity have been identified: reducing side heterogeneity and
antenna heterogeneity. Reducing side heterogeneity of PSII is
based on the electron transport properties at the reducing side of
the reaction center. There centers with efficient electron transport
from QA to QB are known as QB reducing type PSII centers, while
centers that are photochemically competent but unable to transfer
electron from QA to QB are known as QB non-reducing type PSII
centers [20]. QB reducing centers are so called ‘active centers’ while
QB non-reducing centers are termed as ‘inactive centers’. Antenna
heterogeneity of PSII is related to heterogeneity in the antenna size
as well as their energetic connectivity between PSIIs. Three distinct
populations of PSII centers in chloroplasts are termed as PS IIa, PS
IIb and PS IIc [24]. PSII a, b and c are distinguished on the basis of
difference in the rate of closure of reaction centres (RC) [25] where
a shows shorter life time exhibiting fastest rates of electron trans-
fer through them, and PS IIc have maximum life time. However in
our samples, no PS IIc centres were observed.
PSII heterogeneity in early stages of growth is emerging as an
important parameter to assess plant stress tolerance. Recent works
on abiotic stresses have supported this contention. Moreover, PSII
was found to undergo changes in its structural and functional
4 A. Jajoo et al. / Journal of Photochemistry and Photobiology B: Biology xxx (2014) xxx–xxx

Table 2
Chl a fluorescence parameters measured in intact leaves of control and PAH-treated plants (n = 6 ± SE).

Fv/Fm Fv/Fo 1 Vj % of active OEC Fo

Control 0.82 ± 0.01 4.82 ± 0.17 0.53 ± 0.02 100 201 ± 2
Naphthalene 0.72 ± 0.01 2.72 ± 0.13 0.45 ± 0.01 53 267 ± 3
Anthracene 0.65 ± 0.01 2.45 ± 0.11 0.40 ± 0.01 50 289 ± 2
Pyrene 0.69 ± 0.01 2.55 ± 0.17 0.42 ± 0.01 50 250 ± 2

Table 3
Changes in heterogeneity of Photosystem II in control and PAH-treated plants. (n = 6 ± SE).

% of QB non-reducing centers % of QB reducing centers a centers b centers

Control 21 ± 1 79 ± 1 74 ± 1 26 ± 1
Naphthalene 27 ± 1 73 ± 1 65 ± 1 25 ± 1
Anthracene 28 ± 1 72 ± 1 62 ± 1 32 ± 1
Pyrene 29 ± 2 71 ± 1 62 ± 1 32 ± 1

of the plant. There is a loss in pigment concentration as well as

change in protein composition and photosynthetic performance,
all these processes being inhibited by all PAH species. However,
3-ring anthracene was found to be more deleterious as compared
to 2-ring naphthalene and 4-ring pyrene. This led us to conclude
that the inhibitory effects of PAH are not directly proportional to
their aromaticity.

4. Abbreviations

ANT anthracence
Fm, Fo, Fv maximal, minimal and variable fluorescence
LHC light harvesting complex
OEC oxygen evolving complex
NAP napthalene
PAH polycyclic aromatic hydrocarbon
Fig. 4. Changes in thylakoid membrane protein composition in control and PAH PSII Photosystem II
treated plants of Arabidopsis thaliana. The thylakoids were isolated for 6 week old PYR pyrene
plants. Lane are marked as A (ANT treated), N (NAP treated) and P (PYR treated). QA primary plastoquinone
QB secondary plastoquinone
heterogeneity differently in response to PAHs toxicity [13] When RC reaction center
PSII heterogeneity was calculated in control and PAH-treated
plants, it appeared that PAH-treated plants had a higher number
of QB non-reducing centres as compared to control (Table 3). At Acknowledgments
the same time, number of inactive b centres increased at the
expense of active a centres. Increased number of inactive centres AJ thanks Department of Biotechnology (DBT) India for
also explains the reason for increased Fo. However, the change in DBT-CREST Award (BT/IN/BDT-CREST Awards/31/AJ/2011-12).
PSII heterogeneity was more or less similar in NAP, ANT and PYR EMA acknowledges the Academy of Finland Grant No: 118637.
treated plants and aromaticity of PAH did not seem to have signif-
icant effects in causing the changes in PSII heterogeneity. References
From BN-PAGE analysis, it is evident that all PAH- treated plants
have less PSII-LHCII supercomplexes, less LHCII trimer and pre- [1] D.J. Burritt, The polycyclic aromatic hydrocarbon phenanthrene causes
oxidative stress and alters polyamine metabolism in the aquatic liverwort
sumably also less PSII dimers in the it thylakoid membranes in Riccia fluitans L, Plant Cell Environ. 31 (2008) 1416–1431.
chloroplasts as compared to control plants (Fig. 4). Nonetheless, [2] M. Kummerová, L. Váňová, Chlorophyll fluorescence as an indicator of
distinctly the PSII-LHCII sc, LHC trimers and LHC monomer were fluoranthene phototoxicity, Plant Soil Environ. 53 (2007) 430–436.
[3] B. Bałdyga, J. Wieczorek, S. Smoczyński, Z. Wieczorek, K. Smoczyńska, Pea plant
affected most significantly in ANT treated sample as compared to response to anthracene present in soil, Pollut. J. Environ. Stud. 14 (2005) 397–
those treated with NAP and PYR. As explained earlier, an increase 401.
in Fo in PAH-treated plants may be because of dissociation of the [4] X. Liu, G. Zhang, K.C. Jones, X. Li, X. Peng, S. Qi, Compositional fractionation of
polycyclic aromatic hydrocarbons (PAHs) in mosses (Hypnum plumaeformae
antennae complexes in PSII. This is evident from an increase in WILS.) from the northern slope of Nanling Mountains, South China, Atmos.
amount of free LHCII complexes in which do not transfer excitation Environ. 39 (2005) 5490–5499.
energy to PS II RC. It is probable that a structure–function relation- [5] R.M. Kamens, Z.H. Fan, Y.L. Yao, D.H. Chen, S.F. Chen, M. Vartiainen, A
methodology for modeling the formation and decay of nitro-PAH in the
ship is exhibited by PAH-treated plants as evident from change in
atmosphere, Chemosphere 28 (1994) 1623–1632.
fluorescence parameters as well as change in protein profile. It [6] M. Guidotti, D. Stella, M. Owczarek, A. De Marco, C. De Simone, Lichens as
would be interesting to explore it more in future studies as it polycyclic aromatic hydrocarbon bioaccumulators used in atmospheric
may prove to be beneficial in many stress-related research studies. pollution studies, J. Chromatogr., A 985 (2003) 185–190.
[7] C.L. Duxbury, D.G. Dixon, B.M. Greenberg, Effects of simulated solar radiation
Our results provide evidence that the number of rings in a PAH on the bioaccumulation of polycyclic aromatic hydrocarbons by the duckweed
molecule does have a specific impact on growth and development Lemna gibba, Environ. Toxicol. Chem. 16 (1997) 1739–1748.

Please cite this article in press as: A. Jajoo et al., Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs) on photosynthetic performance are not
related to their aromaticity, J. Photochem. Photobiol. B: Biol. (2014), http://dx.doi.org/10.1016/j.jphotobiol.2014.03.011
 A. Jajoo et al. / Journal of Photochemistry and Photobiology B: Biology xxx (2014) xxx–xxx
[8] H. Saxe, Physiological and biochemical tools in diagnosis of forest decline
and air pollution injury to plants, in: M. Yunus, M. Iqbal (Eds.), Plant
Response to Air Pollution, John Wiley & Sons, New York, 1996, pp. 449–
487.
[9] A. Aksmann, Z. Tukaj, Intact anthracene inhibits photosynthesis in algal cells: a
fluorescence induction study on Chlamydomonas reinhardtii cw92 strain,
Chemosphere 74 (2008) 26–32.
[10] M. Kummerová, L. Vanová, J. Krulová, S. Zezulká, The use of physiological
characteristics for comparison of organic compounds phytotoxicity,
Chemosphere 71 (2008) 2050–2059.
[11] X.D. Huang, B.J. McConkey, T.S. Babu, B.M. Greenberg, Mechanisms of
photoinduced toxicity of photomodified anthracene to plants: inhibition of
photosynthesis in the aquatic higher plant Lemna gibba (duckweed), Environ.
Toxicol. Chem. 16 (1997) 1707–1715.
[12] G.J. Ahammed, H.L. Yuan, J.O. Ogweno, Y.H. Zhou, X.J. Xia, W.H. Mao, K. Shi, J.Q.
Yu, Brassinosteroid alleviates phenanthrene and pyrene phytotoxicity by
increasing detoxification activity and photosynthesis in tomato, Chemosphere
86 (2012) 546–555.
[13] J. Shao, G. Yu, Z. Wu, X. Peng, R. Li, Response of Synechocystis sp. PCC 6803
(cyanobacteria) photosystem II to pyrene stress, J. Environ. Sci. 22 (7) (2010)
1091–1095.
[14] R.S. Tomar, A. Jajoo, Alteration in PSII heterogeneity under the influence of
polycyclic aromatic hydrocarbon (fluoranthene) in wheat leaves (Triticum
aestivum), Plant Sci. 209 (2013) 58–63.
[15] S. Järvi, M. Suorsa, V. Paakkarinen, E.M. Aro, Optimized native gel systems for
separation of thylakoid protein complexes: novel super- and mega-complexes,
Biochem. J. 439 (2011) 207–214.
[16] R.J. Strasser, M.M. Tsimilli, A. Srivastava, Analysis of chlorophyll a fluorescence
transient, in: G.C. Papageorgiou, Govindjee (Eds.), Advances in Photosynthesis
and Respiration. Chlorophyll a Fluorescence: A Signature of Photosynthesis,
Springer, Dordrecht, 2004.
Please cite this article in press as: A. Jajoo et al., Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs) on photosynthetic performance are not
related to their aromaticity, J. Photochem. Photobiol. B: Biol. (2014), http://dx.doi.org/10.1016/j.jphotobiol.2014.03.011
View publication stats
5
[17] D.H. Willits, M.M. Peet, Using chlorophyll fluorescence to model leaf
photosynthesis in green house pepper and tomato, Acta Hortic. 507 (2003)
311–315.
[18] G.C. Percival, A. Hendersons, An assessment of the freezing tolerance of urban
trees using chlorophyll fluorescence, J. Hortic. Sci. Biotechnol. 78 (2003) 254–
260.
[19] H.M. Kalaji, Govindjee, K. Bosa, J. KosÍcielniak, K.Z. Goiaszewska, Effects of salt
stress on photosystem II efficiency and CO2 assimilation of two Syrian barley
landraces, Environ. Exp. Bot. 73 (2011) 64–72.
[20] P. Mehta, S.I. Allakhverdiev, A. Jajoo, Characterization of photosystem II
heterogeneity in response to high salt stress in wheat leaves (Triticum
aestivum), Photosynth. Res. 105 (2010) 249–255.
[21] S. Mathur, S.I. Allakhverdiev, A. Jajoo, Analysis of the temperature stress on the
dynamic of antenna size and reducing side heterogeneity of photosystem II in
wheat leaves (Triticum aestivum), Biochim. Biophys. Acta 2011 (1807) 22–29.
[22] R.S. Tomar, S. Mathur, S.I. Allakhverdiev, A. Jajoo, Changes in PS II
heterogeneity in response to osmotic and ionic stress in wheat leaves
(Triticum aestivum), J. Bioenergy Biomembr. 44 (2012) 411–419.
[24] A. Melis, P.H. Homann, Heterogeneity of the photochemical centers in
photosystem II of chloroplasts, Photochem. Photobiol. 23 (1976) 343–350.
[25] S.Z. Toth, R.J. Strasser, The specific rate of QA reduction and photosystem II
antenna heterogeneity, in: Proceedings of the 13th International Congress on
Photosynthesis. Montreal, Canada, 2005, pp. 198–200.
Further reading
[23] T. Graan, D.R. Ort, Detection of oxygen-evolving photosystem II centers
inactive in plastoquinone reduction, Biochim. Biophys. Acta 852 (1986) 320–
330.