CZECH POLAR REPORTS 2 (1): 42-51, 2012
———
Received October 5, 2012, accepted October 15, 2012.
*
Corresponding author: P.Ocenasova@gmail.com
Acknowledgement: The authors acknowledge the possibility to use the infrastructure provided by
the CzechPolar project (LM 20010009) funded by the Czech Ministry of Education, Youth, and
Sports.
42
Photoinhibition of photosynthesis in Antarctic lichen Usnea
antarctica. I. Light intensity- and light duration-dependent
changes in functioning of photosystem II
Miloš Barták, Josef Hájek, Petra Očenášová*
Masaryk University, Department of Experimental Biology, Laboratory of Photosynthetic
Processes, University Campus Bohunice, Kamenice 5, 625 00 Brno, Czech Republic
Abstract
The paper deals with the differences in sensitivity of Antarctic lichen to photoinhibition.
Thalli of Usnea antarctica were collected at the James Ross Island, Antarctica
(57°52´57´´W, 63°48´02´´S) and transferred in dry state to the Czech Republic. After
rewetting in a laboratory, they were exposed to 2 high light treatments: short-term (30
min), and long-term (6 h). In short-term treatment, the sample were exposed to 1000 and
2000 µmol m-2
s-1
of photosynthetically active radiation (PAR). In long-term experiment,
PAR of 300, 600, and 1000 µmol m-2
s-1
were used. Photosynthetic efficiency of U.
antarctica thalli was monitored by chlorophyll fluorescence parameters, potential
(FV/FM) and actual (PSII) quantum yield of photochemical processes in photosystem II
in particular. In short-term treatments, the F0, FV and FM signals, as well as the values of
FV/FM, and PSII showed light-induced decrease, however substantial recovery after
consequent 30 min. in dark. Longer exposition (60 min) to high light led to more
pronounced decrease in chlorophyll fluorescence than after 30 min treatment, however
dark recovery was faster in the thalli treated before for longer time (60 min). Long-term
treatment by high light caused gradual decrease in FV/FM and PSII with the time of
exposition. The extent of the decrease was found light dose-dependent. The time course
was biphasic for FV/FM but not for PSII. The study showed that wet thalli of Usnea
antarctica had high capacity of photoprotective mechanisms to cope well either with
short- or long-term high light stress. This might be of particular importance in the field at
the James Ross Island, particularly at the begining of growing season when melting
water is available and, simultaneously, high light stress may happen on fully sunny days.
Key words: chlorophyll fluorescence, high light, potential quantum yield, effective
quantum yield
Abbreviations: ROS - reactive oxygen species, PSII - photosystem II, D1 - D1 protein,
LHCs - light harvesting complexes, F0 - basic fluorescence, FV - variable fluorescence,
FV/FM - potential photosynthetic quantum yield of photosystem II, PSII - effective
photosynthetic quantum yield of photosystem II
M. BARTÁK et al.
43
Introduction
Lichens are poikilohydric organisms
that respond to high light and consequent
increase in thallus temperature by gradual
drying and dehydration-dependent loss of
photosynthetic activity. In moist and/or
cold habitats, including polar and mountainous
ecosystems, many lichen species
are exposed to high light in fully hydrated
state. Such exposure to high light in the
hydrated state produces photoinhibition in
chlorolichens and cyanolichens The effect
is much more pronounced in cyanolichens,
which do not reverse photosynthetic
depression after a recovery period as
chlorolichens do (see e.g. Gasulla et al.
2012).
Physiological effects of high light to
photosynthetic apparatus of lichens are
similar to those of desiccation (Jensen et
Feige 1991). Both stresses lead to production
of reactive oxygen species (ROS)
in core of photosystem II (PS II) and
neighbouring pigment-protein complexes
of light harvesting complexes (LHCs).
High light-induced ROS act as strong
oxidative agens that cause negative
changes in thylakoidal photosynthetic
apparatus. Oxidation on donor side of PS
II, excessive reduction on the acceptor side
of PSII, and consequently, destruction of
D1 protein are major damages to PS II
(Anderson et Barber 1996). Therefore,
under both high light stress and
dehydration, reactive oxygen species are
considered major cause of damage in
photosynthetic organisms (DemmigAdams
et Adams III, 2000). During
photoinhibition, however, several mechanism
are activated that minimize such
damages to photosynthetic apparatus. Such
protective mechanism comprise mainly
thermal dissipation of absorbed light
energy. The mechanisms are present in
higher plants (Adams III et al. 2006) as
well as in lichens.
Both in chlorolichens and cyanolichens,
photoinhibition could be diminished by
several photoprotective mechanisms
(Demmig-Adams et al. 1990a). Among
them, formation of zeaxanthin during the
initial phases of photoinhibition is well
known (Demmig-Adams et al. (1990b) and
documented for number of chlorolichens
from polar regions, e.g. Usnea antarctica
(Barták et al. 2003), Umbilicaria antarctica
(Barták et al. 2004). This effect,
however, was not observed in cyanolichens.
Short-term changes in gluthatione
pool (Vráblíková et al. 2005), as well as its
redox state is another antioxidative
mechanism activated by high light in
chlorolichens (Štěpigová et al. 2007).
Content of carotenoids (Valladares et al.
1995) and phenolic compounds (Buffoni
Hall et al. 2002) is also reported to protect
lichens form light-induced ROS, especially
the environments rich in high UV-B.
Appart from the above-mentioned biochemical
photoprotective mechanisms
activated in the photosynthetic apparatus
of lichen photobionts, there are several
other mechanisms helping the lichens to
minimize negative effects of high light.
The mechanisms comprise dehydrationdependent
movements of thalli parts that
provides self-shading effect (Barták et al.
2006), and production of light-screening
compounds by mycobiont hyphae forming
the upper cortex (Gauslaa et Solhaug
2004). The ability of lichens to exploit
such mechanisms depends strongly on the
physical characteristics of particular
habitat, prevailing light environment in
particular (Gauslaa et Solhaug 1996,
2000).
Majority of studies of photoinhibition
in the lichens and mosses from polar
regions are made under controlled laboratory
conditions. Several field experiments,
however, have been made to study
photoinhibition in Antarctica using both
gas exchange and chlorophyll fluorescence
approach in the field (e.g. Kappen et al.
1998). Among them, the study made on
PHOTOINHIBITION IN ANTARCTIC LICHEN
44
Antarctic mosses (Lovelock et al. 1995)
pointed out reversible photoinhibition in
an Antarctic moss measured at wet state.
Field studies made on Antarctic lichens
could hardly distiguish between limitation
of photosynthetic processes related to
thallus dehydration and progressive photoinhibition
because the processes co-occur
simultaneously. That was why the photoinhibition
of Antarctic lichens is studied
under constant thallus hydration in
laboratory-based facilities. Last studies
showed large capacity of lichens to cope
with short-term high light stress. For
Usnea antarctica, Barták et al. (2003)
reported substantial decrease of chlorophyll
fluorescence parameters found
immediatelly after photoinhibitory treatment,
as well as their fast recovery. In the
study, fast phase of recovery (lasting
typically 30 min) was attributed to
structural changes in PSII and LHC and
the effects of antioxidative mechanisms.
Slow phase of recovery (lasting from tens
to hundreds of minuts) was attributed to
resynthetic processes that repair damaged
components of PSII an LHCs. Long-term
photoinhibition exploiting the exposition
of wet lichen thalli to high light for the
periods longer than 1 h, has been applied
in Central European (Barták et al. 2008)
but not Antarctic lichens. To fill the gap,
we decided to compare the negative effects
of short- and long-term exposition of
Usnea antarctica to high light using a
chlorophyll fluorescence approach. In this
paper, we bring the results of photoinhition
of PSII and analyze time- and
light dose-dependent changes of FV/FM
and PSII. Forthcoming paper (MS in
prep.) will focus activation of quenching
mechanism during short- and longh-term
photoinhibition in Usnea antarctica.
Material and Methods
Lichen collection and handling
Thalli of fruticose lichen Usnea
antarctica were collected at the James
Ross Islands, Halozetes Valley, during
summer field campains (Jan. - Feb. 2012).
They were transferred in dry state to the
laboratory in Brno, Czech Republic, where
stored in a fridge at 5°C, for three months.
For experiments, the thalli were re-wetted
48 or 72 hours before the begining of the
experiments (see below). The thalli were
placed into Petri dishes on Pehazell®
cellulose wadding and hydrated by regular
spraying with demineralized water.
Optimum hydration was checked fluorometrically.
When FV/FM reached maximum
values, the sample was considered
optimally hydrated. During hydration
period, the thalli were stored at 5°C at low
irradiance of 10 µmol m-2
s-1
or 100 µmol
m-2
s-1
of photosynthetically active radiation
(checked by a Li-1600 radiometer LiCor,
USA). The two iradiances during
hydration period were used because of two
different experimental designs. The thalli
treated by 10 µmol m-2
s-1
were used in the
experimental set-up mimicking long-term
but low-light photoinhibition. The other
pretreatment (100 µmol m-2
s-1
) was used
for the experiment mimicking short-term
photoinhibion (see High light treatments).
High light treatments
In our experiments, short-term high
light stress was achieved by the exposition
of the U. antarctica thalli to two
irradiances: 1000 and 2000 µmol m-2
s-1
,
duration of which was 30 and 60 min at
each irradiance. During the exposition, the
M. BARTÁK et al.
45
Petri dishes with thalli were kept on a
thermostated metal block (Peltier cooling
unit, Con Brio, Czech Republic) surrounded
by melting ice to reach constant
low temperature of thallus (5o
C, checked
by a infrared thermometer) througout
experiment. Light was provided by a
source consisting of several white
superbright LEDs. During the expositions,
individual U. antarctica thalli were placed
horizontally on the metal block, i.e.
contrastingly to natural arrangement in the
field, they were irradiated from side not
from top. In long-term light treatments,
thalli of U. antarctica were exposed to
light (300, 600, and 1000 µmol m-2
s-1
,
respectively) for 240 min under the same
physical conditions as described above.
Both in short-term and long-term
treatments, the extent of treatment-induced
photoinhition was evaluated as the change
in chlorophyll fluorescence parameters.
Fig. 1. Wet thalli of Usnea antarctica used for the experiments studying photoinhibition.
Chlorophyll fluorescence measurements
Light treatment-induced changes in
photosynthetic apparatus of U. antarctica
were evaluated by several chlorophyll
fluorescence parameters. In short-term
experiment, the values of chlorophyll
fluorescence parameters (i) before photoinhibitory
treatment, (ii) immediately after,
and (iii) after 60 min of dark recovery
were recorded. In long-term experiment,
the parameters were measured (i) before
light treatment, and (ii) during light
treatment (each 30 min) so that time
course of chlorophyll fluorescence change
could be determined.
For chlorophyll fluorescence measurements,
a FluorCam (HFC-010, Photon
Systems Instuments, Czech Republic –
short-term treatment) and PAM-2000
(Heinz Walz, Germany – long-term
tratment) were used. The chlorophyll
fluorescence parameters were evaluated on
dark-adapted thalli (10 min) using the
measurement of slow Kautsky kinetics
supplemented with quenching analysis.
The method consisted of determination of
basic fluorescence (F0), maximum fluorescence
(FM) in dark adapted state,
steady-state fluorescence recorded on the
PHOTOINHIBITION IN ANTARCTIC LICHEN
46
sample exposed to actinic light for 5 min
(FS), maximum fluorescence measured on
actinic light-adapted sample (FM´) and
maximum chlorophyll fluorescence (FM´´)
measured after 1 min of dark relaxation.
For each treatment, at least three replicates
were measured.
Fig. 2. Simplified scheme of exposition and measuring set up. Source of laptop clipart:
http://www.clker.com/clipart-14661.html.
Results
Short-term exposition of U. antarctica
thalli was aimed to show the changes in
the shape of kinetics of chlorophyll
fluorescence (see Fig. 3) as well as
absolute signals recorded after saturation
pulses (FM, FM´) and the parameters
(FV/FM, PSII) derived from them. From
the kinetics follows that all these
characteristics are affected by short-term
high-light treatment. In general, chlorophyll
fluorescence kinetics recorded
immediately after the short-term exposition
to high light were typical by a
decrease in basic chlorophyll fluorescence
(F0), chlorophyll fluorescence during
actinic light period (FV), as well as steadystate
chlorophyll fluorescence (FS). The
decrease in the three above-specified
parameters was more pronounced in the
thalli treated by 2000 mol m-2
s-1
than in
those treated by 1000 mol m-2
s-1
. The
expectation, that the decrease would be
more pronounced in those thalli exposed to
photoinhibitory light for 60 min
(compared to those treated for 30 min) was
not proven. The thalli showed oposite
response. With prolonged duration of
photoinhibitory treatment at particular
light intensities (1000, 2000 mol m-2
s-1
),
rather smaller extent of decrease in
particular chlorophyll fluorescence levels
(F0, FV, FS) was found immediately after
the treatment.
The shapes of chlorophyll fluorescence
kinetics were affected by high light
treatment. Compared to pre-photoinhibition
shape, the kinetics were strongly
flattened in those recorded immediately
after high-light treatment, especially in the
range delimited by peak chlorophyll
fluorescence (FP) and steady-state chlorophyll
fluorescence FS. Moreover, the
chlorophyll fluorescence (FV) values found
at the dip following FP were smaller than
M. BARTÁK et al.
47
F0 at the same curves. Such response, i.e.
the decrease of FV below F0 value is
indicative of strong quencher present
either in PS II or its closest neighbour-
hood.
Recovery from photoinhibition was
apparently high light dose- and durationdependent.
As regards the shape of the
chlorophyll fluorescence kinetics and the
values of their particular signals recorded
between the time of F0 and FS, it is clear
that they were almost fully recovered in
the 60 minutes treatments, while only
partial recovery was apparent in 30
minutes treatments. When calculated from
the kinetic presented in Fig. 3, the typical
chlorophyll fluorescence parameters (Table
1) showed different, i.e. light dose- and
light duration-dependent sensitivity to
photoinhibiton and recovery.
30 min 2000 mol m-2
s-1
Chlorophyllfluorescence(mV)
200
300
400
500
600
700
30 min 1000 mol m-2
s-1
Chlorophyllfluorescence(mV)
200
300
400
500
600
700
60 min 2000 mol m-2
s-1
Time (min.)
0 1 2 3 4 5 6 7
100
200
300
400
500
600
60 min 1000 mol m-2
s-1
Time (min.)
0 1 2 3 4 5 6 7
100
200
300
400
500
600
A
B
C
D
Fig. 3. Kinetics of chlorophyll fluorescence recorded before (green line), after (red line)
photoinhibitory treatment and after 60 min dark recovery (blue line).
Long-term exposition to high light led to
gradual photoinhibition of photosynthetic
processes in PS II indicating cummulative
stress to PS II. Decline of potential yield
of photosynthetic processes in photosystem
II (FV/FM) was fastest and most
pronounced when the highest dose of
photosynthetically active radiation, i.e.
1000 mol m-2
s-1
was used (Fig. 4). Lightinduced
decrease in FV/FM caused by 300
and 600 mol m-2
s-1
showed similar trend
but reached higher value at the end of light
exposition period (0.34 and 0.27) than
under those recorded when the highest
light dose was used. In all PAR treatments,
biphasic FV/FM decrease was apparent. The
most significant fall of about 25-40% of
maximum value was found during initial
phase of light treatment, i.e. within the
first 50 min of exposition to particular
light. Then, slow phase of FV/FM decline
was recorded between 50 and 360 min of
light exposition period. Within the slow
phase, following decrease of about similar
or smaller extent than during the first
phase was found.
PHOTOINHIBITION IN ANTARCTIC LICHEN
48
1000 mol m-2
s-1
Exposition 30 min 60 min
F0/FM FV/FM FP-F0/FP PSII F0/FM FV/FM FP-F0/FP PSII
Before HL 0.416 0.584 0.246 0.448 0.519 0.481 0.224 0.346
After HL 0.580 0.420 0.096 0.363 0.772 0.228 0.038 0.239
Recovery 0.465 0.535 0.184 0.238 0.550 0.450 0.167 0.327
2000 mol m-2
s-1
Exposition 30 min 60 min
F0/FM FV/FM FP-F0/FP PSII F0/FM FV/FM FP-F0/FP PSII
Before HL 0.423 0.577 0.272 0.392 0.491 0.509 0.218 0.370
After HL 0.689 0.322 0.063 0.295 0.819 0.180 0.034 0.151
Recovery 0.508 0.492 0,173 0.363 0.531 0.469 0.155 0.372
Table 1. Chlorophyll fluorescence parameters derived from kinetics supplemented with saturation
pulses. For particular photoinhibitory treatments, the values (means of 3 replicates) were measured
before, and after exposition to high light (HL). Consequently, the values were recorded after 60
min dark recovery.
Time (min.)
0 50 100 150 200 250 300 350 400
FV/FM
0.2
0.3
0.4
0.5
0.6
Time (min.)
0 50 100 150 200 250 300 350 400
PSII
0.2
0.3
0.4
0.5
0.6
30 min 300 µmol m-2
s-1
30 min 600 µmol m-2
s-1
30 min 1000 µmol m-2
s-1
Fig. 4. Time courses of potential (FV/FM - left) and effective (PSII - right) quantum yield of
photosystem II recorded during long-term exposition of Usnea antarctica to 300 (), 600 () and
1000 () mol m-2
s-1
of PAR.
Light-induced decrease in effective
quantum yield of PS II (PSII) showed
somewhat ambiguous trend. General trend,
i.e. decrease of PSII with time of
exposition to light was found for all PAR
treatments (Fig. 4). However, fast and
slow phase of PSII decrease could not be
distinguished. For smallest (300) and
highest (1000 mol m-2
s-1
) light doses,
more or less regular PSII fall with
duration of light was apparent. For 600
mol m-2
s-1
, irregularly fluctuating values
were recorded in between 60 and 270 min
of light duration. At the end of exposition
period, PSII declined at regular rate.
Overall decline from maximum value
(about 0.4) to the minimum found at the
end of exposition period was PARdependent.
PSII reached the minimum of
about 0.3 for 300 and 600 mol m-2
s-1
treatment. It was found lower (PSII =
0.23) when 1000 mol m-2
s-1
was used.
M. BARTÁK et al.
49
Discussion
Short-term experiment showed decrease
in FV/FM and PSII as well as fast
recovery. The results are comparable to
the earlier study made on U. antarctica
(Barták et al. 2003) in which 70 and 60%
recovery was found for FV/FM and PSII
after 240 min of dark recovery. In our
study, background chlorophyll fluorescence
F0 decreased immediately after
short-term high-light stress. Therefore, all
the chlorophyll fluorescence parameters
derived from F0 were affected (see Table
1). Some studies, however, reported an
increase in F0 caused by photoinhibitory
treatment (Manrique et al. 1993). Such
difference could be explained as a consequence
of different set up of both experiments.
In our measurements, higher light
values and much shorter exposition time
were used. Therefore, F0 decrease might
be considered as a short-term response of
lichen photosynthetic apparatus to high
light stress. When exposed for long period,
such as e.g. 3 days (Manrique et al. 1993),
photosynthetic apparatus tends to acclimate
to higher light doses that could lead
to the increase in F0. Our data presented in
Fig. 3 suggest that acclimatory changes in
structure and function of photosystem II
may happen even after 1 h of exposition to
high light. It is because the shape of
chlorophyll fluorescence kinetics gets back
to control faster in lichen thalli treated for
1 h than those treated only for 30 min.
This supports the idea that acclimatory
changes to high light in PS II may start
soon after the photoinhibitory light began.
They may comprise structural arrangement
of PSII and LHC, redox state of plastoquinone
as well as the balance between
photochemical and biochemical processes
of photosynthesis.
In long-term experiment, gradual
decrease in FV/FM was found, similarly to
the evidence from Lasallia pustulata
exposed to high light for several hours
(Barták et al. 2008). Our data could be
interpreted that wet thalli of U. antarctica
exhibited decrease in FV/FM reaching more
or less constant value after 6 h treatment
by 1000 mol m-2
s-1
. Smaller decrease in
FV/FM recorded for lower light doses
throughout the exposition period indicates
that U. antarctica may thrive well under
such light, exhibiting less damage to PSII.
The same conclusion might be made for
effective quantum yield. Photochemical
processes of U. antarctica photosynthesis
tend to decrease gradually, the extent of
their inhibition is light dose-dependent.
This again demonstrates the ability of
long-term treated U. antarctica to maintain
substantial photosynthesis at the irradiances
below 600 mol m-2
s-1
.
Lichen responses to high light and
dehydration may involve similar mechanisms,
such as light- or dehydrationdependent
xanthophyll cycle pigments
conversion, and state 1-2 transition. Both
mechanism quench excess light energy
captured by PSII and convert to thermal
dissipation of energy. Last studies (e.g.
Heber et al. 2000, 2006, 2007), however,
indicated that there is another effective
quencher in photosynthetic apparatus of
PS II of desiccating lichens. It is not
related to zeaxanthin formation and
independent on light. According to Heber
et al. (2006), it may involve conformational
changes in pigment-protein
complexes in PS II. Thus, highly-effective
dissipation centers are formed in which
excitation energy is trapped (Heber et al.
2010). In such centers, the first excited
state of chlorophyll molecule is thermally
taken back to ground state before charge
separation takes place (Heber et Lüttge
2011). In such way, overenergization of
PSII and ROS formation is avoided.
Moreover, presence of strong quencher in
core of PSII and/or PSII antennae is
reported by Veerman et al. (2007) for
Parmelia sulcata desiccating on light.
Chemical structure of the quencher, how-
PHOTOINHIBITION IN ANTARCTIC LICHEN
50
ever, is not know. Our study showed that
wet thalli of Usnea antarctica had high
capacity of photoprotective mechanisms to
cope well either with short- or long-term
high light stress. This might be of
particular importance in the field at the
begining of growing season when air and
surface temperatures are above zero.
Within this period, melting water from
snowfields and glaciers is available and
supply lichen thalli for long periods.
Under such circumstances, photoinhibition
may occur on fully sunny days, because
high quantities of light reaches wet lichen
thalli. In our experiment exploiting shortterm
high-light stress, however, fast
recovery of chlorophyll fluorescence
parameters towards prephotoinhibition
values indicated that U. antarctica has low
susceptibility to photoinhibition.
References
ADAMS III, W.W., ZARTER, C.R., MUEH, K.E., AMIARD, V. and DEMMIG-ADAMS, B. (2006): Energy
Dissipation and Photoinhibition: A Continuum of Photoprotection. In: B. Demmig-Adams,
William W. Adams III and A.K. Mattoo (eds): Photoprotection, Photoinhibition, Gene
Regulation, and Environment. Springer, The Netherlands, pp. 49-64.
ANDERSON, B., BARBER, J. (1996): Mechanism of photodamage and protein degradation during
photoinhibition of photosystem II. In: Photosynthesis and the enviroment. Baker N.R. (ed.),
Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 101-121.
BARTÁK, M., VRÁBLÍKOVÁ, H. and HÁJEK, J. (2003): Sensitivity of photosystem 2 of antarctic
lichens to high irradiance stress: Fluorometric study of fruticose (Usnea antarctica) and foliose
(Umbilicaria decussata) species. Photosynthetica, 41: 497-504.
BARTÁK, M., HÁJEK, J., VRÁBLÍKOVÁ, H. and DUBOVÁ, J. (2004): High-light stress and
photoprotection in Umbilicaria antarctica monitored by chlorophyll fluorescence imaging and
changes in zeaxanthin and glutathione. Plant Biology, 6: 333-341.
BARTÁK, M., SOLHAUG, K.A., VRÁBLÍKOVÁ, H. and GAUSLAA, Y. (2006): Curling during
desiccation protects the foliose lichen Lobaria pulmonaria against photoinhibition. Oecologia,
4: 553-560.
BARTÁK, M., VRÁBLÍKOVÁ-CEMPÍRKOVÁ, H., ŠTEPIGOVÁ, J., HÁJEK, J., VÁCZI, P. and VEČEŘOVÁ,
K. (2008): Duration of irradiation rather than quantity and frequency of high irradiance inhibits
photosynthetic processes in the lichen Lasallia pustulata. Photosynthetica, 46: 161-169.
BUFFONI HALL, R.S., BORNMAN, J.F. and BJÖRN, L.O. (2002): UV-induced changes in pigment
content and light penetration in the fruticose lichen Cladonia arbuscula sp. Mitis. Journal of
Photochemistry and Photobiology B: Biology, 66: 13-20.
DEMMIG-ADAMS, B., ADAMS III, W.W., CZYGAN, F-C., SCHREIBER, U. and LANGE, O.L. (1990a):
Differences in the capacity for radiationless energy dissipation in the photochemical apparatus
of green and blue-green algal lichens associated with differences in carotenoid composition.
Planta, 180: 582-589.
DEMMIG-ADAMS, B., MAGUAS, C., ADAMS, W.W., MEYER, A., KILIAN, E. and LANGE, O.L.
(1990b): Effect of High Light on the Efficiency of Photochemical Energy-Conversion in a
Variety of Lichen Species With Green and Blue-Green Phycobionts. Planta, 180: 400-409.
DEMMIG-ADAMS, B., ADAMS III, W.W. (2000): Harvesting sunlight safely. Nature, 403: 371-374.
GASULLA, F., HERRERO, J., ESTEBAN-CARRASCO, A., ROS-BARCELÓ, A., BARRENO, E., ZAPATA, J.M.
and GUÉRA, A. (2012): Photosynthesis in lichen: Light reactions and protective mechanisms.
Chapter 8, pp. 149-174. In: M. M. Najafpour (ed.): Advances in Photosynthesis - Fundamental
Aspects. Publisher: InTech, Published: February 15, 2012 under CC BY 3.0 license, in subject
Agricultural and Biological Sciences, DOI: 10.5772/1385, ISBN 978-953-307-928-8, p. 588.
GAUSLAA, Y., SOLHAUG, K.A. (1996): Differences in the Susceptibility to Light Stress Between
Epiphytic Lichens of Ancient and Young Boreal Forest Stands. Functional Ecology, 10: 344-
354.
M. BARTÁK et al.
51
GAUSLAA, Y., SOLHAUG, K.A. (2000): High-light-intensity damage to the foliose lichen Lobaria
pulmonaria within natural forest: The applicability of chlorophyll fluorescence methods. The
Lichenologist, 32: 271-289.
GAUSLAA, Y., SOLHAUG, K.A. (2004): Photoinhibition in lichens depends on cortical
characteristics and hydration. The Lichenologist, 36: 133-143.
HEBER, U., BILGER, W., BLIGNY, R. and LANGE, O.L. (2000): Phototolerance of lichens, mosses and
higher plants in an alpine environment: analysis of photoreactions. Planta, 211: 770-780.
HEBER, U., BILGER, W. and SHUVALOV, V.A. (2006): Thermal energy dissipation in reaction
centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against
photo-oxidation. Journal of Experimental Botany, 57: 2993-3006.
HEBER, U., AZARKOVICH, M. aanndd SHUVALOV, V.A. (2007): Activation of mechanisms of
photoprotection by desiccation and by light: poikilohydric photoautotrophs. Journal of
Experimental Botany, 58: 2745-2759.
HEBER, U., BILGER, W., TÜRK, R. and LANGE, O.L. (2010): Photoprotection of reaction centres in
photosynthetic organisms: mechanisms of thermal energy dissipation in desiccated thali of the
lichen Lobaria pulmonaria. New Phytologist, 185: 459-470.
HEBER, U., LÜTTGE, U. (2011): Lichens and Bryophytes: Light Stress and Photoinhibition in
Desiccation/Rehydration Cycles – Mechanisms of Photoprotection. In: Plant Desiccation
Tolerance. Ecological Studies, No. 215, pp. 121-137.
JENSEN, M., FEIGE, G. B. (1991): Quantum efficiency and chlorophyll fluorescence in the lichens
Hypogymnia psysodes and Parmelia sulcata. Lichen Biology, 11: 2-3.
KAPPEN, L., SCHROETER, B., GREEN, T.G.A. and SEPPELT, R. D. (1998): Chlorophyll a fluorescence
and CO2 exchange of Umbilicaria aprina under extreme light stress in the cold. Oecologia,
113: 325-331.
LOVELOCK, C.E., JACKSON, A.E., MELICK, D.R. and SEPPELT, R.D. (1995): Reversible
Photoinhibition in Antarctic Moss during Freezing and Thawing. Plant Physiology, 109: 955-
961.
MANRIQUE, E., BALAGUER, L., BARNES, J. and DAVISON, A. W. (1993): Photoinhibition studies in
lichens using chlorophyll fluorescence analysis. The Bryologist, 96: 443-449.
ŠTEPIGOVÁ, J., VRÁBLÍKOVÁ, H., LANG, J., VEČEŘOVÁ, K. and BARTÁK, M. (2007): Glutathione and
zeaxanthin formation during high light stress in foliose lichens. Plant, Soil and Environment,
53: 340-344.
VALLADARES, F., SANCHEZ-HOYOS, A. and MANRIQUE, E. (1995): Diurnal changes in
photosynthetic efficiency and carotenoid composition of the lichen Anaptychia ciliaris: effects
of hydration and light intensity. Bryologist, 98: 375-382.
VEERMAN, J., VASIL’EV, S., PATON, G.D., RAMANAUSKAS, J. and BRUCE, D. (2007):
Photoprotection in the lichen Parmelia sulcata: The origins of desiccation-induced
fluorescence quenching. Plant Physiology, 145: 997-1005.
VRÁBLÍKOVÁ, H., BARTÁK, M. and WONISCH, A. (2005): Changes in glutathione and xanthophyll
cycle pigments in high light-stressed lichens Umbilicaria antarctica and Lasallia pustulata.
Journal of Photochemistry and Photobiology B: Biology, 79: 35-41.