CZECH POLAR REPORTS 2 (1): 31-41, 2012
———
Received September 15, 2012, accepted October 15, 2012.
*
Corresponding author: mbartak@sci.muni.cz
Acknowledgement: The work reported here was supported by the project No. LM20010009
(CzechPolar) provided by the Czech Ministry of Education, Youth and Sports. The authors are
grateful for the possibility to use the infrastructure of the CzechPolar. The authors are grateful to
Dr. M. Forbelská (Masaryk University, Brno) for the help she provided during mathematical data
processing.
31
Interspecific differences in photosynthetic efficiency and
spectral reflectance in two Umbilicaria species from Svalbard
during controlled desiccation
Radek Jupa, Josef Hájek, Jana Hazdrová, Miloš Barták*
Department of Experimental Biology, Laboratory of Photosynthetic Processes, Faculty
of Science, Masaryk University, University Campus – Bohunice, Kamenice 5, 62500
Brno, Czech Republic
Abstract
This study aimed to evaluate the effective photosynthetic quantum yield (PSII) and the
Photochemical Reflectance Index (PRI) for assessment of photosynthetic performance of
two Umbilicaria lichens during gradual desiccation of their thalli. U. cylindrica and
U. decussata exhibited curvilinear relationship (S-shape curve) of decreasing PSII
values with decreasing water potential (WP) of thalli. During initial phase of desiccation
(WP from 0 to -10 MPa), no decrease of PSII was apparent, further desiccation (WP
from -10 to -20 MPa) led to fast PSII decrease from 0.6 to 0.1 indicating strong
inhibition of photosynthetic processes. Critical WP at which photosythetic processes are
fully inhibited was found bellow -25 MPa in both lichen species. Photochemical
Reflectance Index (PRI) exhibited curvilinear increase with thalli desiccation
(decreasing WP). At full thallus hydration, the PRI reached the value of -0.18 in both
species. Under strong dehydration (WP from -20 to -30 MPa), however, U. cylindrica
showed somewhat lower value (-0.04) than U.decussata (-0.02 MPa). PRI to WP
relationship is discussed and compared to existing evidence from higher plants and
poikilohydric organisms.
Key words: Quantum yield, water potential, chlorophyll fluorescence, Photochemical
Reflectance Index, lichen, water stress
Abbreviations: FV/FM - potential photosynthetic quantum yield of photosystem II, PSII effective
photosynthetic quantum yield of photosystem II, NDVI - normalized
differentiate vegetation index, NPQ - non-photochemical quenching, PPFD photosynthetic
photon flux density, PRI - Photochemical Reflectance Index, PS II photosystem
II, WP - water potential
R. JUPA et al.
32
Introduction
Lichens are poikilohydric symbiotic
organisms exhibiting maximum photosynthetic
rate at optimum hydration that is
species-specific. If hydration of lichens
decreases below such optimum due to
progressive desiccation, photosynthetic
processes are gradually inhibited. During
desiccation of lichen thallus, several biochemical
and biophysical mechanism are
activated to minimize damages to photobionts
(Kranner et al. 2008) and their
photosynthetizing pigments (Zorn at al.
2001). Initial phase of desiccation is
typical by partial water loss from a thallus
but no reduction of photosynthetic rate is
apparent. More pronounced water loss,
however, leads to fast decrease of photosynthetic
processes. At severe dehydration
of thalli, full inhibition of photosynthesis
occurs. Within last couple of years, the
dependence of photosynthesis of numerous
Arctic and Antarctic lichens on thallus
dehydration expressed as water potential
has been investigated in our laboratory
(see e.g. Barták et al. 2005). Representatives
of genus Umbilicaria typically
show substantial photosynthesis even at
strong dehydration, i.e. within water
potential (WP) range from -15 to -20 MPa.
In this study, we investigated two lichens
form Svalbard (Umbilicaria cylindrica and
Umbilicaria decussata) during gradual
desiccation using measurements of chlorophyll
fluorescence, effective quantum
yield of photosynthetic processes in photosystem
II (PSII) of symbiotic alga in
particular. The other aim of this study was
to evaluate critical water potential (WP) at
which photosynthetic processes are fully
inhibited and compare to existing data
from other lichen species.
The Photochemical Reflectance Index
(PRI) is based on a reflectance measurement
developed by Gamon (1992). The
PRI uses two wavelengths, 531 nm and
570 nm, respectively.
PRI = (R531 - R570) / (R531 + R570)
Reflectance at 531 nm is mostly
affected by the changes in carotenoid
pigments, especially xanthophyll-cycle
pigments. Therefore, numeric value of the
PRI is sensitive to zeaxanthin formation
which is activated under high light
conditions and water stress in photosynthetizing
tissue. PRI is thus used as an
effective indicator of photoinhibitory and
water stress in higher plants (e.g. Liu et al.
2012). In most studies, PRI is well related
to non-photochemical quenching of access
light energy absorbed by photosynthetic
pigments in chloroplasts. It is because of
substantial involvement of light- or
drought-induced zeaxanthin formation into
protective mechanisms of non-photochemical
nature activated during initial
and the following phases of stress in
plants. The PRI is generally used for the
assessment of changes in carotenoid
content (Sims et Gamon 2002), interconversion
of xanthophyll-cycle pigments
in particular. Some of recent studies,
however, pointed out that PRI might be
used also as an indicator of water stress in
plants (Thenot et al. 2002). For lichens, no
such study investigating PRI in relation to
the hydration status of thallus has been
performed since NDVI index is generally
used much more frequently than PRI
(Gloser et Gloser 2007). Moreover, the use
of NDVI is recently devoted to large scale
studies exploiting remote sensing approach
with the main emphasis given to the
identification of components of vegetation
cover (e.g. Rees 2012).
DESICCATION IN UMBILICARIA LICHENS
33
Recently, there is trend to use several
biophysical methods to measure photosynthesis
in plants in order to identify
limiting factors of photosynthesis of particular
species. Over last few decades, chlorophyll
fluorescence technique has been
used frequently in the assessment of the
extent of stress in photosynthetic apparatus
in plants. That was why we decided to
measure water limitation of photosynthesis
in desiccating lichens by chlorophyll fluorescence
and ongoing changes in PRI
indicating the extent of water stress. Recently,
simultaneous measurements of Chl
fluorescence data and PRI are used to
evaluate the effect of leaf development
stage (Rahimzadeh-Bajgiran et al. 2012),
radiation and temperature variation during
growing season (Weng et al. 2006), actual
leaf temperature (Inamullah et Isoda
2005), and exposure to ozone (Meroni et
al. 2008) on functioning of photosynthetic
apparatus of higher plants. In poikilohydric
plants and organisms, however,
such approach is used only to a limited
extent. In our study, we focused on
simultaneous measurements of PRI and
effective quantum yield of photosynthetic
processes in photosystem II (PSII). Close
correlation is found between PRI and PSII
(e.g. Gamon et al. 1997) in higher plants.
However, in poikilohydric autotrophic organisms,
lichens at different level of hydration
in particular, the PRI to PSII
relationship, has not yet beeen investigated.
Only scarce data are available on
PRI and potential yield of photochemical
reactions in PS II (FV/FM) in desiccating
lichens. Yamano et al. (2006) found linear
relationship between PRI and FV/FM in
lichens forming desert soil crust. We
therefore hypothesized, that reasonable
correlation should be found between PSII
and PRI when measured on gradually
desiccating lichen thalli. Combination of
the two biophysical methods is beneficial
because it brings a deeper insight into
functioning of chloroplastic photosynthetic
apparatus under stress.
Fig. 1. Map of Central Svalbard with the indication of the plots at which thalli of U. cylindrica
and U. decussata were collected during field campaign in Arctic summer 2012. Modified map
extract (source: NPI: http://toposvalbard.npolar.no/).
R. JUPA et al.
34
Fig. 2. One of collection plots with high occurence of U. cylindrica and U. decussata. The thalli of
both species were abundant mainly on rock surfaces, several centimeters above ground level where
the upper margin of snow cover occurs.
Material and Methods
Samples of lichen Umbilicaria cylindrica
were collected in the first half of
July 2012 on several field locations of
central part of Spitsbergen Island (16˚E,
78˚N; Svalbard), in the vicinity of
Petuniabukta (see Fig. 1). All samples
grew on stones and rocks near the coast in
the elevation to 100 m above sea level.
Typical thalli of Umbilicaria cylindrica
are round-shaped. It is grey or brownishgrey
and often divided into multiple lobes.
For the experiment, we selected thalli
sized at least 3 cm in diameter (see Fig. 3).
Umbilicaria decussata has more or less
round-shaped thallus, typically 1 to 5 cm
in diameter. Thallus upper surface is light
gray to dark gray or brownish gray, with
sharp ridges radiating from the central
point. Lower surface of thallus is white
(see Fig. 3). Thalli, typically attached at
central point (umbilicus), were cut of by
sharp blade from surface of stones (Fig. 2)
and hydrated for 24 hours. Fully hydrated
thalli were placed in plastic dishes and
subjected to slow desiccation at room
temperature (25°C, 40% RH). Dependence
of quantum yield of photochemical
reactions in photosystem II (ΦPSII) on
water potential (WP) of thalli was determined
using PAM-2000 modulated fluorometer
(Walz, Germany) connected to a
portable computer and a dew point water
potential meter WP4T (Decagon Devices,
USA) with programmed temperature control.
Determination of WP by the device
was based on chilled-mirror dewpoint
technique. The instrument enables the
measurement of samples up to 40 mm in
diameter and 10 mm in height with an
accuracy of 0.1 MPa.
DESICCATION IN UMBILICARIA LICHENS
35
Fig. 3. Typical thallus of U. cylindrica (upper) and U. decussata (lower). The photographs were
taken with dry thalli.
R. JUPA et al.
36
For WP determination, samples were
placed into a measuring chamber of the
device and equilibrated to constant relative
humidity. After measuring of WP, the
same sample was exposed for 5 min to
constant artificial irradiance of 40 µmol
m-2
s-1
photosynthetic photon fluence density
(PPFD) and then the PSII was
immediately measured. LED was used as
the source of PPFD and the value of PPFD
was determined using radiometer EMS-12
(Photon System Instruments, Czech Republic).
After PSII measurement, Photochemical
Reflectance Index (PRI) was
determined. For PRI measurements, a
PlantPen PRI 200 (Photon System Instruments,
Czech Republic) was used. The
whole cycle of measurements was repeated
during the desiccation period until
PSII reached zero.
Results
At full thallus hydration, suprasaturation
effect on photosynthesis was
observed in U. cylindrica but not in
U. decussata (see Fig. 4, the PSII values at
WP=0). Either no or mild decrease of ΦPSII
was observed in both species within the
WP range of 0 to -10 MPa which reflects
initial phase of thallus dehydration.
Further decrease of water potential (below
-10 MPa) led to substantial and rapid
decrease of PSII in both experimental
lichen species. Significant limitation of
photochemical processes in PS II appeared
at WP below -20 MPa. Critical WP
at which PSII was close to zero differed
between species. Full inhibition of photosynthetic
processes was reached at about
-25 MPa in U. decussata while the same
was apparent at lower values of about -30
MPa in U. cylindrica.
Relation between PRI and WP was
curvilinear and exhibited PRI increase
with WP decrease (Fig. 5). The relationship
was similar in both investigated
species. At full thallus hydration, PRI
values reached the values between -0.19
and -0.17. When very limited loss of water
from lichen thallus occured (WP decrease
from 0 to -2 MPa), PRI increased up to the
values about -0.07 (U. cylindrica) and
-0.05 (U. decussata). There were also
some minor interspecific differences found
in bending of the PRI to WP relationship
as well as the maximum PRI values found
at heavily desiccated thalli (see data points
in Fig. 4). While in U. cylindrica the PRI
maximum was about -0.04, it reached
slightly higher values in U. decussata
(-0.03 to -0.02). Slight differences, however,
were found in the PRI to PSII relation
(Fig. 6). The relation was of curvilinear
shape. Under full hydration and
initial phases of water loss, i.e. at PSII
ranging from 0.7 to 0.6, PRI values
increased rapidly, typically from -0.18 to
-0.06. This was found in U. cylindrica
while the increase was much less pronounced
in U. decussata (from -0.10 to
-0.06). Further decrease in the intrathalline
water content led to the decrease in PSII
(from 0.4 to 0.1), however, PRI values
showed only minor increase from -0.06 to
-0.04 in U. cylindrica and -0.06 to -0.02 in
U. decussata.
DESICCATION IN UMBILICARIA LICHENS
37
U. cylindrica
WP [MPa]
-35 -30 -25 -20 -15 -10 -5 0
PSII
0.0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
U. decussata
WP [MPa]
-35 -30 -25 -20 -15 -10 -5 0
PSII
0.0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
Fig. 4. Relation between the effective quantum yield of photosystem II (PSII) and water potential
(WP) recorded during desiccation of lichen thalli from wet (WP = 0 MPa) to dry (WP below -25
MPa) state. The curve is the best fit of log-logistic S-curve.
U. cylindrica
WP [MPa]
-60 -50 -40 -30 -20 -10 0
PRI
-0.18
-0.15
-0.12
-0.09
-0.06
-0.03
0.00
U. decussata
WP [MPa]
-60 -50 -40 -30 -20 -10 0
PRI
-0.18
-0.15
-0.12
-0.09
-0.06
-0.03
0.00
Fig. 5. Relation of Photochemical Reflectance Index (PRI) to water potential (WP) recorded in
U. cylindrica and U. decussata during gradual desiccation form full thalli hydration (WP=0 MPa)
to fully dehydrated thalli.
U. cylindrica
PSII
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
PRI
-0.18
-0.15
-0.12
-0.09
-0.06
-0.03
0.00
U. decussata
PSII
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
PRI
-0.18
-0.15
-0.12
-0.09
-0.06
-0.03
0.00
Fig. 6. Relation of effective quantum yield of photosynthetic processes (PSII) to Photochemical
Reflectance Index (PRI). Data points were recorded during gradual desiccation of U. cylindrica
and U. decussata thalli.
R. JUPA et al.
38
Discussion
Critical WP ranged between -25 and
-30 MPa for both investigated Umbilicaria
species. This was well comparable to the
WP values found in the earlier studies
done on Antarctic species. Critical WP
was found -25 MPa in Xanthoria elegans
(Barták et al. 2005) and -30 MPa for lichenized
Nostoc (Moudrá et Barták, 2009).
There are, however, indications that interspecific
differences exist in critical WP of
lichen species growing in polar regions.
Results obtained for lichen species collected
at Galindez Island (Antarctica) and
measured by the same method showed that
Umbilicaria antarctica had critical WP of
about -40 MPa, while much higher values
were found for Stereocaulon (-30 MPa)
– Barták et Gloser (2004).
Our data supports the evidence from
literature, that gradual loss of water from
lichen thalli leads to decrease in rate of
photochemical processes of photosynthesis,
ΦPSII in particular. Dehydrationdependent
decrease in photochemistry
leads to the decline biochemical part of
photosynthesis as proven by numerous gas
exchange studies in desiccating lichens in
a laboratory (e.g. Lange et al. 2001) or in
the field (Reiter et al. 2008). Such
dehydration-dependent decrease in photosynthesis
is accompanied by the activation
of protective mechanisms that protect
components of photosystem II from
damages. These mechanisms are similar to
those activated in lichens during photoinhibition
and include interconversion of
xantophyll cycle pigments (Calatayud et
al. 1997, Vráblíková et al. 2005). They
comprise several pathways of thermal
energy dissipation (Heber et al. 2007,
2010) that act in reaction centers of PS II
during lichen dehydration. To protect
themselves from overenergization, reaction
centers of PS II are converted from
energy absorbing centers to energy
dissipating centers at certain level of
dehydration (Heber et al. 2011). Presence
of strong quencher in core of PS II and/or
PS II antennae is reported from lichens
desiccating on light (Veerman et al. 2007),
however its chemical structure is not
known. Recent studies showed, that the
association of fungal and algal partners
plays also important role since the lichen
association showed higher resistance to
dehydration stress than isolatated photobionts
(Kosugi et al. 2006).
In higher plants, positive relation
between PRI and ΦPSII has been reported
for a variety of species and experimental
treatments. The relation, however, differs
from what we found in U. cylindrica and
U. decussata. Inamullah et Isoda (2005)
showed that different irrigation regimen of
Gossypium hirsutum and Glycine max
resulted in a decrease of ΦII with water
limitation. In these plants, PRI was possitively
correlated with ΦPSII, i.e. PRI
declined with pronounced water limitation.
Similar response was found by Stylinski et
al. (2000) who reported that an increase in
photosynthetic electron rate brought an
increase in PRI in Quercus pubescenc
leaves exposed to natural and elevated
CO2 concentrations. Positive relation between
ΦPSII and PRI was also found in
grasses (Weng et al. 2012) as well as two
srubs Baccharis halimifolia and Myrica
cerifera exposed to salt stress (Zinnert et
al. 2012).
For poikilohydric autotrophic organisms,
relation between PRI and ΦPSII
has been investigated only exceptionally.
In mosses, Van Gaalen et al. (2007)
showed decreasing values of nonphotochemical
quenching (NPQ) with increasing
PRI in desiccating Sphagnum sp.
The same authors reported linear increase
of PRI with Sphagnum dehydration
expressed as relative water content. We
may, therefore, conclude that reasonable
agreement exists between our findings of
PRI to WP relationship and available data
from poikilohydric moss, because both
DESICCATION IN UMBILICARIA LICHENS
39
they show the PRI increase with water loss
from thalli. The PRI to WP relationship
found in this study showed, however,
curvilinear shape. This might be explained
either by optical properties of desiccating
Umbilicaria sp. thalli that differ from
those of Spagnum ones. The other explanation
is that relation of WP to relative
water content is curvilinear in U. cylindrica
(our data, not shown). General
conclusion from our data is that PRI
increases with decreasing WP in both
Umbilicaria species investigated in this
study. This conclusion can be supported
also by the data presented by Gauslaa
(1984). In his paper, spectral reflectance
curves are given for several species of
Umbilicaria genus. We used the data
derived from the curves that he recorded
for wet and dry thalli. We calculated PRI
values (not shown here) for several
Umbilicaria species. In U. rigida, U. spodochlora
and U. vellea, we found an
increase of PRI values in dry thalli which
support the general trend found for U.
cylindrica and U. decussata in Fig. 5.
Conclusion
The results indicated high degree of
tolerance of genus Umbilicaria species to
water stress and their ability to photosynthesize
even under substantial water
loss from their thalli. Moreover, critical
water potential values were below -25
MPa which indicates the ability of the two
lichen species to perform photochemical
processes of photosynthesis at strongly
desiccated state of a thallus as well (Jupa
et Barták 2012). We may, therefore, conclude
that U. cylindrica and U. decussata
may thrive well in polar ecosystems with
limited water availability and short period
of thallus hydration.
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