Tree Physiology 25, 1085 –1090
© 2005 Heron Publishing—Victoria, Canada
Low temperature during winter elicits differential responses among
populations of the Mediterranean evergreen cork oak (Quercus suber)
I. ARANDA,1,2 L. CASTRO,3 R. ALÍA,1 J. A. PARDOS3 and L. GIL3
1
Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Carretera de la Coruña Km., 7.5, 28040 Madrid, Spain
2
Corresponding author ([email protected])
3
Unidad de Anatomía, Fisiología y Genética Forestal, Escuela Técnica Superior de Ingenieros de Montes, Universidad Politécnica de Madrid,
Ciudad Universitaria s/n, 28040 Madrid, Spain
Received June 15, 2004; accepted January 15, 2005; published online June 1, 2005
Summary Populations of cork oak (Quercus suber L.) were
assessed for seasonal and inter-population variability in, and
temperature responses of, the ratio between light-induced
variable and maximum fluorescence of chlorophyll, Fv /Fm,
considered a surrogate for the maximum photochemical efficiency of photosystem II (PSII). Seedlings from 10 populations throughout the distribution range of Q. suber in the
Mediterranean basin were grown in a common garden in central Spain. The Fv /Fm ratio of dark-adapted leaves was measured at dawn every month for 2 years. Air temperature was
recorded at a nearby climatic station.
During the summer, when maximum air temperatures
reached 40 °C, there were no significant differences in Fv /Fm
among populations, but significant differences were seen during the winter. In colder months, Fv /Fm ranged in all populations between 0.5–0.6 and 0.2–0.3 in 2001 and 2002, respectively. The variance explained by the population effect was
greatest during winter months, especially in 2002, reaching a
peak value of 10% when minimum air temperature was below
–10 °C. Populations originating from warmer sites showed the
largest decline in Fv /Fm between the end of 2001 and the beginning of 2002. Thus, a negative linear relationship was established between mean annual temperature at the population
source and population mean Fv /Fm recorded in the coldest
month in 2002 and normalized by the Fv /Fm spring measurement.
Keywords: chlorophyll fluorescence, cold, Mediterranean evergreen oak, photoinhibition.
Introduction
Summer drought has often been identified as the main environmental stress to which forest vegetation is exposed in Mediterranean ecosystems (Aussenac and Vallet 1982, Tenhunen
et al. 1987, Oliveira et al. 1992, Sala and Tenhunen 1994,
1996). Low rainfall and a high vapor pressure deficit and temperature constrain seedling photosynthetic activity and growth.
However, low winter temperatures may also impose a significant stress on seedlings in continental areas of the Mediterranean region (Tenhunen et al. 1987, Terradas and Savé 1992,
Tretiach et al. 1997, Boorse et al. 1998, García-Plazaola et al.
1999a, 1999b, Larcher 2000, Nardini et al. 2000, Oliveira and
Peñuelas 2001).
Light-energy harvesting is impaired by low temperatures as
a consequence of reduced photochemical efficiency of PSII
(Ball et al. 1991, Adams and Demmig-Adams 1995). There is
some evidence that this phenomenon, which occurs frequently
in species at high latitudes (Ottander and Öquist 1991, Vogg et
al. 1998), also occurs in forest vegetation in continental areas
of the Mediterranean area during winter months (Méthy and
Trabaud 1990, Oliveira and Peñuelas 2000, 2001). The reduction in photochemical efficiency of PSII may be greater when
overnight frosts are followed by sunny days (Greer 1990,
Egerton et al. 2000), as frequently occurs during Mediterranean winters. Under such conditions, loss of photochemical
efficiency may be exacerbated by sudden exposure to high
light in the absence of mechanisms to dissipate excess light energy (Sonoike 1998).
Cork oak (Quercus suber L.) is a widely distributed forest
tree species in the Mediterranean basin. It is present in areas
with a mean annual rainfall of 400 –1500 mm and a mean annual temperature of 13 –20 °C (Díaz-Fernández et al. 1995,
Montero and Cañellas 1999). The species is not well adapted
to low temperatures but is able to maintain photochemical efficiency during periods of drought (Faria et al. 1996, GarcíaPlazaola et al. 1997). It is also tolerant to high temperatures
(Ghouil et al. 2003).
Thermal stress is frequently assessed in vivo by chlorophyll
fluorescence measurements (Strand and Öquist 1988, Ball et
al. 1994, Williams et al. 2003). In this study, we used chlorophyll fluorescence to assess the integrity of maximum photochemical efficiency of photosystem II (PSII) in populations of
cork oak grown in a common garden for two years. Specifically, we examined if: (1) maximum photochemical efficiency
of PSII in leaves of cork oak varies seasonally; (2) low temperatures during winter stress have a more negative impact on
1086
ARANDA, CASTRO ALÍA, PARDOS AND GIL
photochemistry of cork oak leaves than low water availability
and high temperatures in summer; and (3) there are inter-population differences in the photochemical response of cork oak
to environmental stress. Increased understanding of these
three topics will contribute to better management and conservation of genetic resources and allow better selection of provenances for afforestation.
Materials and methods
Open-pollinated seeds from 10 populations, covering the geographic and climatic range of cork oak, were collected in the
autumn of 1996 (Table 1). Plants were cultivated in a nursery
under standard conditions after seeding in the spring of 1997.
Seedlings were well watered every two days.
A common garden field trial with 15 one-year-old seedlings
per population was established in Madrid (40°25′ N, 3°44′ W)
at the beginning of 1998. During the following 2 years (1999–
2000), plants were well watered each week during the first
growing season. After the establishment period, irrigation was
terminated and seedlings endured summer drought in each of
the following years.
For 2 years after establishment of the field trial (November
2000–November 2002), chlorophyll fluorescence was recorded
monthly in 10–12 seedlings per population. Precipitation was
scarce from June to September in both years. Minimum predawn water potential evaluated in five of the populations
reached –2.1 and –1.4 MPa at the end of the summer in 2001
and 2002, respectively (data not shown).
The ratio between light-induced variable fluorescence and
maximum fluorescence, Fv /Fm, was measured as a surrogate
for maximum quantum efficiency of PSII (Kitajima and Butler
1975, Demmig-Adams et al. 1989). Maximum fluorescence
(Fm ) and ground fluorescence (Fo ) were measured in one
dark-adapted leaf per seedling from south-oriented shoots in
the uppermost canopy (PSM Chlorophyll Fluorimeter, Biomonitor S.C.I. AB, Umeå, Sweden). Leaves were included in a
leaf-clip that allowed dark acclimation of the leaves and the
maintenance of the same distance between the tip of the fiber-
optic and the sample in all measurements, thereby minimizing
the error associated with the sensitivity of Fo and Fm to the distance between the point of light pulse emission and the leaf
sample. Variable fluorescence was calculated as Fv = Fm – Fo.
The degree of maximum photoinhibition during winter months
was estimated by standardization of the winter value of Fv /Fm
for each plant by its spring value, which was assumed to approximate the optimum value of about 0.8.
Chlorophyll fluorescence was recorded at dawn after 30 min
of dark acclimation on cloudless days. Whenever possible,
measurements were repeated on the same leaves throughout
the study. Occasionally, a leaf was replaced by another one
from the same shoot. Bud burst took place at the end of May
and unfolding of new leaves was completed by mid-June. Following bud burst, measurements were made on the newly expanded leaves as well as on leaves from the previous growing
season. Afterward, measurements were made on leaves of the
current season only because the old leaves dropped at the end
of June. Only a few seedlings supported both types of leaves
until mid-July.
Statistical analysis
Chlorophyll fluorescence variables were analyzed mainly by
non-parametric statistics. The requirements for a normal distribution and homoscedasticity of variances were not met by
the parameters related to chlorophyll fluorescence (Lazár and
Nauš 1998). Therefore, the influence of population source on
fluorescence variables was evaluated by analysis of molecular
variance (AMOVA; Excoffier et al. 1992, Schneider et al.
2000). A hierarchical analysis of variance was applied to partition the total variance into covariance components due to
inter-population differences and those due to intra-population
differences. The significance of the components was tested using a non-parametric permutation approach (Excoffier et al.
1992). Under this procedure, neither the normality assumption
nor the equality of variance among populations is necessary.
Statistical analyses were performed using Arlequin (Schneider et al. 2000).
Table 1. Locations and climatic characteristics of the source locations of the cork oak populations studied. Minimum and maximum mean temperatures are referred to as the mean of the lowest and highest annual temperatures. Abbreviations: precip. = precipitation; T = temperature; min. =
minimum; and max. = maximum.
Population
Code
Country
Latitude and
longitude
Altitude
range (m)
Alburquerque
La Almoraima
Santa Coloma
de Farnés
Potes
El Pardo
Haza de Lino
San Brás de Alportel
Sicilia
Oulmés
Aïn Rami
Alb
Alm
Col
Spain
Spain
Spain
39° N 7° W
36° N 5° W
41° N 2° E
450 –500
50 –60
200 –500
Pot
Par
Haz
Alp
Sic
Oul
Ain
Spain
Spain
Spain
Portugal
Italy
Morocco
Morocco
43° N 4° E
40° N 3° W
36° N 3° W
37° N 7° W
37° N 14° W
33° N 4° W
35° N 5° W
200 –500
700
1300
440 – 485
170
1100
300
Mean annual
precip. (mm)
Min. mean
T (°C)
Max. mean
T (°C)
Mean
Tannual (°C)
642
993
802
7.0
11.4
7.5
25.7
23.3
23.6
15.5
16.6
15
1265
455
742
874
448
673
1482
7.6
5.4
6.3
10
11.1
10
–
18.8
24.0
21.9
23.2
26.2
20.8
–
12.9
13.9
13
15.9
17.7
15.4
19.0
TREE PHYSIOLOGY VOLUME 25, 2005
PHOTOINHIBITION IN CORK OAK PROVENANCES
Linear regression analysis was performed to test the relationship between photoinhibition and mean annual temperature of populations. The Pearson coefficient of determination
was used to establish the strength of the relationship (Statgraphics 5.1, Statistical Graphics).
Results
Microclimatic conditions
Over the 2-year study, the annual course of temperature was
typical of continental areas in the Mediterranean basin (Figure 1a). The lowest daily mean temperature in the winter
months was usually above 0 °C; however, there was an exceptionally cold period from November 2001 to January 2002,
with an absolute minimum temperature around –12 °C, and
for 15 days temperatures remained at or below –5 °C.
Throughout this period, the mean daily temperature was below
0 °C and cold nights were followed by sunny days. Maximum
temperatures and minimum rainfall (data not shown) were recorded in the summer months.
Maximum quantum efficiency of PSII at dawn
Just after leaf unfolding in June, Fv /Fm values peaked at
slightly above 0.8 in both years. Thereafter, the Fv /Fm ratio
progressively decreased until the end of the growing season in
both years (Figure 1b). Minimum summer values between
0.65 and 0.7 were reached in September of each year. The first
exposure to subfreezing temperatures in autumn caused an
acute depression in Fv /Fm, which declined again as a conse-
1087
quence of new frost events, reaching minimal values close to
0.55 in the winter months of 2001, and 0.2–0.3 in winter 2002.
During the summer months, differences in Fv /Fm among
populations were nonsignificant (P > 0.05). However, these
differences became statistically significant during the winter
of 2000 –2001, and highly significant in the winter of 2001–
2002. During the winter, the percent of variance attributable to
population was highest, reaching a value of 10%, and the total
variance was also at a maximum (Figure 2).
A positive relationship was found between the mean photoinhibition assessed in the coldest period and the mean annual
temperature at the place of origin of the populations (Figure 3). The warmer the population source, the greater the winter drop in Fv /Fm and the greater the sensitivity to cold stress as
measured by maximum photoinhibition. Populations from
northern Spain (Potes) or from continental areas (El Pardo)
showed the smallest winter decline in Fv /Fm , whereas the population from southern Italy (Sicilia) showed the largest.
Discussion
Seasonal influence on maximum quantum yield of PSII
Photoinhibition caused by low winter temperatures is one of
the main factors limiting survival of evergreen species at high
latitudes or altitudes (Adams et al. 2002, Williams et al. 2003).
The effect of low temperatures on vegetation from low latitudes or Mediterranean areas has received little attention because summer drought is considered to be the major environmental constraint (Werner et al. 2002, but see Larcher 2000).
Figure 1. (a) Seasonal variations in maximum, minimum
and mean daily temperature at
the experimental plot (Madrid,
Spain) during the 2-year study
period. (b) Seasonal changes
in mean maximum photochemical efficiency of
photosystem II in dark-adapted
leaves for 10 populations of
cork oak (n = 12). Data were
taken at dawn, just before sunrise. Abbreviations: Fv /Fm =
the ratio between light-induced
variable fluorescence and maximum fluorescence; T a mean =
mean annual temperature; T a
min. = minimum annual temperature; T a max. = maximum
annual temperature. Site abbreviations are as in Table 1.
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1088
ARANDA, CASTRO ALÍA, PARDOS AND GIL
Figure 2. Total variance and
variance explained by population. Numbers above the
bars indicate the probability
that the effect of population
was significant (P < 0.1;
AMOVA).
In the present study, we observed seasonal variation in
Fv /Fm in cork oak seedlings, with low winter temperatures
having a greater impact than high temperatures and drought
during the summer. In all populations, Fv /Fm decreased in
summer and winter months. However, the depression in maximum photochemical efficiency of PSII was more noticeable in
response to the first autumn frosts and a cumulative effect of
cycles with low temperature (below 0 °C) followed by cloudless days (e.g., the 2001–2002 winter). Permanent depression
of photochemistry was indicated by the lack of nocturnal recovery of Fv /Fm measured at dawn. Thus, the extremely suppressed predawn values of Fv /Fm during the winter months imply permanent photoinhibition; recovery to values close to optimum occurred only after temperatures rose during spring.
Photodamage in leaves has previously been interpreted to reflect the result of the combined effects of low temperatures and
excess light (Greer 1990). However, high stability of PSII to
dehydration and high temperature in oaks has been reported
(Faria et al. 1996, Ghouil et al. 2003). This pattern has also
been described in other evergreen sclerophyllous species
(García-Plazaola et al. 1997, Karavatas and Manetas 1999,
Oliveira and Peñuelas 2000, Ogaya and Peñuelas 2003), confirming the hypothesis that Mediterranean species are particularly sensitive to moderately low temperatures (cf. Kyparissis
et al. 2000). Although cork oak shows high susceptibility to
both cold and water stress—both disturbances impair photochemistry of leaves (García-Plazaola et al. 1997, 1999a)—in
the present study, all populations showed a greater sensitivity
to low temperatures than to summer drought.
Differences in cold tolerance among populations of cork oak
The drop in maximum efficiency of photosynthetic energy
conversion of PSII in response to winter cold has been described for many species (Boorse et al. 1998, Verhoeven et al.
1999). However, inter-population differences in the photochemical response to low temperatures and summer drought
have been analyzed less frequently. Differences among cork
oak populations in the photochemical efficiency of PSII were
significant during periods of unusually low temperatures that
occurred during the winter of 2001–2002 (see Figure 1). Dates
when total and population variances were highest corresponded
with dates on which frost caused the greatest reduction in
Fv /Fm. Populations native to cold sites were less sensitive to
cold stress than populations native to warm sites, reinforcing
the roles of extreme events as selective factors (Gurvich et al.
2002, Gutschick and BassiriRad 2003), which in cork oak
populations are related to a high sensitivity of PSII to cold
temperatures.
In summary, cork oak showed high variability in the seasonal pattern of maximum photochemical efficiency of PSII at
Figure 3. Relationship between
maximum photoinhibition (Phot)
and mean annual temperature
(T a; °C) at the population source.
Photoinhibition was the maximum decrease in the ratio between light-induced variable and
maximum fluorescence of chlorophyll (Fv /Fm ) during the winter of 2001–2002 relative to the
maximum spring values of
Fv /Fm in 2001. Values represent
the mean of the population analyzed (12 seedlings ± SE). Table
1 provides a more detailed description of each population.
TREE PHYSIOLOGY VOLUME 25, 2005
PHOTOINHIBITION IN CORK OAK PROVENANCES
dawn. The high sensitivity of cork oak to low temperatures
may explain its well-known displacement in continental areas
by deciduous trees or other, more cold-tolerant evergreens
such as Quercus ilex L. This would represent an important
constraint for the species if a shift in the frequency or timing of
extreme frost events occurred in the Mediterranean zone as
consequence of climatic change. The problem may be more
acute in continental areas or at high altitudes. Intraspecific differences in cold tolerance at the population level were observed, with populations from regions with lower temperatures sustaining a less pronounced decrease in the maximum
photochemical efficiency of PSII in response to low temperatures.
Acknowledgments
Research was supported by the Dirección General para la Biodiversidad (Convenio MMA-UPM P96 0720319). The authors thank
S. Iglesias and all the staff at the Puerta de Hierro nursery. We also
thank Dr. P. Smouse for his comments on the statistical analyses.
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