Tree Physiology 28, 761–771
© 2008 Heron Publishing—Victoria, Canada
Leaf physiological versus morphological acclimation to high-light
exposure at different stages of foliar development in oak
J. RODRÍGUEZ-CALCERRADA,1 P. B. REICH,2 E. ROSENQVIST,3 J. A. PARDOS,1
F. J. CANO1 and I. ARANDA4,5
1
Unidad de Anatomía, Fisiología y Genética Forestal, Escuela Técnica Superior de Ingenieros de Montes, Universidad Politécnica de Madrid
(UPM), Ciudad Universitaria s/n, E-28040, Madrid, Spain
2
Department of Forest Resources, University of Minnesota, St. Paul, MN 55108, USA
3
Department of Agricultural Science, University of Copenhagen, Hojbakkegaard Allé 21, DK-2630 Taastrup, Denmark
4
Centro Nacional de Investigación Forestal (CIFOR), Instituto Nacional de Investigación Agraria y Alimentaria (INIA), Apdo. 8111, E-28080,
Madrid, Spain
5
Corresponding author ([email protected])
Received June 18, 2007; accepted September 18, 2007; published online March 3, 2008
Summary We investigated light acclimation in seedlings of
the temperate oak Quercus petraea (Matt.) Liebl. and the
co-occurring sub-Mediterranean oak Quercus pyrenaica Willd.
Seedlings were raised in a greenhouse for 1 year in either
70 (HL) or 5.3% (LL) of ambient irradiance of full sunlight,
and, in the following year, subsets of the LL-grown seedlings
were transferred to HL either before leaf flushing (LL-HLBF
plants) or after full leaf expansion (LL-HLAF plants). Gas exchange, chlorophyll a fluorescence, nitrogen fractions in photosynthetic components and leaf anatomy were examined in
leaves of all seedlings 5 months after plants were moved from
LL to HL. Differences between species in the acclimation of
LL-grown plants to HL were minor. For LL-grown plants in
HL, area-based photosynthetic capacity, maximum rate of
carboxylation, maximum rate of electron transport and the effective photochemical quantum yield of photosystem II were
comparable to those for plants grown solely in HL. A rapid
change in nitrogen distribution among photosynthetic components was observed in LL-HLAF plants, which had the highest
photosynthetic nitrogen-use efficiency. Increases in mesophyll
thickness and dry mass per unit area governed leaf acclimation
in LL-HLBF plants, which tended to have less nitrogen in
photosynthetic components and a lower assimilation potential
per unit of leaf mass or nitrogen than LL-HLAF plants. The
data indicate that the phenological state of seedlings modified
the acclimatory response of leaf attributes to increased irradiance. Morphological adaptation of leaves of LL-HLBF plants
enhanced photosynthetic capacity per unit leaf area, but not per
unit leaf dry mass, whereas substantial redistribution of nitrogen among photosynthetic components in leaves of LL-HLAF
plants enhanced both mass- and area-based photosynthetic capacity.
Keywords: competitive ability, nitrogen partitioning, photosynthetic acclimation, Quercus petraea, Quercus pyrenaica.
Introduction
Plants regulate photosynthetic processes in response to
changes in irradiance that occur on various time scales (Külheim et al. 2002, Schurr et al. 2006). For example, the onset of
mechanisms of thermal dissipation in the light-harvesting complexes, as well as the engagement of alternative non-photosynthetic electron pathways, can protect the photosynthetic
apparatus from oxidative damage after shaded plants are exposed to a sudden increase in irradiance (Ort 2001). However,
the ability of preexistent foliage to acclimate to changes in
light environment requires a transition from high light-use efficiency under low irradiances to high photosynthetic capacity
under high irradiances (Hikosaka and Terashima 1995). Such
a transformation enhances total carbon assimilation and reduces susceptibility to photoinhibition (Baker and Oxborough
2004).
Nitrogen availability, allocation and remobilization (e.g.,
increasing uptake by roots, or translocation among plant organs or photosynthetic components) play a role in acclimation
to a changed light environment (Naidu and DeLucia 1997a,
Ramalho et al. 2000, Frak et al. 2001, Walters 2005). The ratio
of leaf chlorophyll to nitrogen (e.g., Ellsworth and Reich
1992), Rubisco, cytochrome f or the electron transport rate decrease with an increase in irradiance (Yin and Johnson 2000,
Walters 2005), suggesting a reallocation of nitrogen from
light-harvesting to energy-transformation processses and the
balancing of antenna size relative to photosystem content.
Studies of leaf nitrogen fractionation (i.e., among light-harvesting pigments, electron transport chain proteins, carbon
fixation enzymes and non-photosynthetic components) show
rapid modulation following a change in light environment
(Frak et al. 2001). In contrast, anatomical features of shadedeveloped leaves do not change as readily (Eschrich et al.
1989, Sims and Pearcy 1992), limiting complete acclimation
of photosynthesis to the light environment in some instances
762
RODRÍGUEZ-CALCERRADA ET AL.
(Tognetti et al. 1998, Oguchi et al. 2003, 2005).
The rate and extent of photosynthetic acclimation to increased irradiance differ among species with contrasting adaptive strategies. For example, drought-adaptive traits may constrain acclimation of photosynthesis to increasing irradiance
(cf. Valladares et al. 2000), whereas shade-adaptation may involve traits that limit light processing at high irradiances (Seemann et al. 1987, Strauss-Debenedetti and Bazzaz 1991).
Here, we studied light acclimation in foliage of sympatric
and closely related oak species, the temperate Quercus petraea
(Matt.) Liebl. and the sub-Mediterranean marcescent Quercus
pyrenaica Willd., which coexist in scattered stands throughout
central and midwestern Spain, where Q. petraea is at the
southern extreme of its distribution. The acclimatory responses of these seedlings to light may help account for differences in their recruitment patterns in the Mediterranean
(Gómez-Aparicio et al. 2006).
We hypothesized that, during long-term acclimation to increased irradiance, there are physiological changes reflected
in leaf nitrogen fractionation, and leaf morphological changes,
particularly in the structure of mesophyll tissue. We postulated
that acclimatory responses to increased irradiance depend on
species and when during leaf development the change in light
environment occurs.
(and LL-HLBF and LL-HLAF) plants, at a leaf temperature of
25.8 ± 0.1 °C, and over a broad range of intercellular CO2 concentrations (Ci ) generated by increasing the CO2 supply in
twelve steps from 50 to 1800 ppm. After 30 min at saturating
light and 380 ppm of CO2, the CO2 concentration was reduced
step-wise to minimum values, then increased to 380 ppm CO2
again, and lastly increased to high values. Photosynthetic capacity on a leaf area basis (Amax,a) was estimated as the mean of
the three measurements made at 1800 ppm and saturating
light. A nonlinear least squares fitting procedure was performed to estimate the maximum rates of carboxylation
(Vcmax,a) and electron transport (Jmax,a ) from the An –Ci curves.
Regression models were constructed according to equations of
Farquhar et al. (1980), in which An is modeled as the minimum
of Rubisco-limited (Ac) or RuBP-limited (Aj ) photosynthetic
rate:
An = min( Ac , Aj ) − Rd
A c = V cmax , a
Aj = J
Materials and methods
Experimental design and treatments
In spring 2004, Q. petraea and Q. pyrenaica seeds from a
mixed forest at the southern extreme of the distribution of
Q. petraea (41°7′ N, 3°30′ W) were sown in plastic pots
(400-cm3 in volume, 35-cm deep) filled with a 3:1 (v/v) peat
and sand mixture supplemented with slow-release fertilizer
(5 g dm – 3 ). Germinated seedlings were raised in a greenhouse
either without shading except by the greenhouse structure
(HL, 70% of full midday ambient photosynthetic photon flux
(PPF) on a sunny day = 1050 ± 28 µmol m – 2 s –1 ), or beneath a
shade cloth (LL, 5.3% of full midday ambient PPF on a sunny
day = 80 ± 7 µmol m – 2 s –1 ). At the end of the growing season,
seedlings were transplanted individually to cylindrical PVC
containers (3000 cm3, 40 cm deep), in the same medium newly
supplemented with slow-release fertilizer. Night–day ranges
in temperature and relative humidity were 15–39 °C and
50–90%, respectively. All seedlings were well watered during
the experiment.
The next year, six plants per species were moved from LL to
HL either 1 week before leaf flushing (February 27; LLHLBF) or after full leaf expansion (June 6, 3 months after leaf
emergence; LL-HLAF). First-flush leaves from LL, LLHLBF, LL-HLAF and HL plants were measured, or harvested
for measurement on July 3–7. Photosynthesis was measured
the week ending May 30.
Gas exchange measurements
Net CO2 assimilation rate (An ) was measured with an infrared
gas analyzer (LC pro Analytical Development, U.K.) in a PPF
of 1000 µmol m – 2 s –1 for HL and 700 µmol m – 2 s –1 for LL
Ci − Γ*
1+ O 
C i + Kc 

 Ko 
Ci − Γ*
O

4 C i + 
τ

(1)
(2)
(3)
where Rd is mitochondrial respiration rate, which was estimated from Ac. The concentration of oxygen (O) was considered to be 20 kPa. Temperature-dependent parameters Kc (Michaelis-Menten constant of Rubisco for CO2 ) and Ko (Michaelis-Menten constant of Rubisco for O2 ) were calculated for the
leaf temperature of each curve following the equations derived
by Bernacchi et al. (2001); temperature dependency of the
CO2 specificity factor (τ) was accounted for by the equation
derived by Harley et al. (1992). The CO2 compensation point
in the absence of mitochondrial respiration in light (Γ* ) was
calculated as O/ 2τ. The light dependence of the rate of electron transport (J ) was calculated as:
J=
αQ
 αQ 
1+ 

 Jmax, a 
(4)
2
where α is the efficiency of light utilization (0.24 mol e – (mol
quanta) – 1 ) and Q is the incident photon flux.
All parameters were entered for modeling functions. Estimates of Vcmax,a and Jmax,a at 25 °C were obtained by rearranging the temperature-dependent equations of Vcmax,a and Jmax,a
given by Dreyer et al. (2001) for Q. petraea. Mass-based estimates (Amax,m, Vcmax,m and Jmax,m ) were obtained by dividing
area-based values by leaf dry mass per unit area (MA ).
Nitrogen concentration and fractioning among leaf proteins
Values of Vcmax,a and Jmax,a at 25 °C were used to calculate leaf
TREE PHYSIOLOGY VOLUME 28, 2008
LEAF RESPONSES TO LIGHT IN TWO CO-OCCURRING WHITE OAKS
nitrogen fractions in Rubisco (Pr) and in photosynthetic electron transport proteins (Pb ), respectively, following equations
in Niinemets and Tenhunen (1997):
Pr =
Pb =
V cmax, a
(5)
6.25 Vcr M A Nm
Jmax, a
rescence signal approached steady-state (Fs ) in actinic light, a
similar flash was applied to obtain a value of the maximum
fluorescence in light (Fm′). The minimum fluorescence in light
(Fo′) was measured at each PPF by applying a 5-s far-red light
pulse in temporary darkness to drain electrons from the electron acceptors of PSII. The redox state of the primary electron
acceptor QA of PSII (qL ) was calculated according to Kramer
et al. (2004):
(6)
8.06 Jmc M A Nm
–1
where the value 6.25 g Rubisco (g N in Rubisco) converts nitrogen concentration to Rubisco protein concentration, the
value 8.06 µmol cytochrome f (g N in bioenergetics) – 1 is a conversion factor based on the assumption that there is a constant
1:1:1.2 cytochrome f:ferredoxin NADP reductase:coupling
factor stoichiometry controlling electron transport, Vcr is specific activity of Rubisco at 25 °C (20.5 µmol CO2 (g Rubisco) – 1
s –1 ) and Jmc is the capacity of electron transport per unit of
cytochrome f at 25 °C (156 mol e– (mol cytochrome f) – 1 s – 1 ).
Leaf nitrogen concentration per unit dry mass (Nm ) was measured, excluding petioles, by the Kjeldahl procedure (Bradstreet 1965). We used MA to express nitrogen concentration on
an area basis (Na = Nm MA ).
Values of leaf chlorophyll concentration per unit dry mass
(Cm ) (determined following Barnes et al. 1992) were used to
calculate the fractions of chlorophyll associated with photosystem (PS) I, PSII and light harvesting complex II. Previously, we calculated the concentration of these protein complexes on a leaf area basis according to equations in Hikosaka
and Terashima (1995) and Niinemets and Tenhunen (1997).
The proportion of nitrogen in light-harvesting components
(Pl ) was computed as:
Pl =
763
Cm
(7)
Nm C B
where CB is the weighted average of chlorophyll binding of the
three protein complexes (see Hikosaka and Terashima 1995).
The proportion of structural nitrogen was calculated as Ps =
100 – Pl – Pr – Pb. Photosynthetic nitrogen-use efficiency
(PNUE) was estimated as Amax,m /Nm.
Chlorophyll fluorescence measurements
Light response curves of chlorophyll fluorescence parameters
were measured with a portable pulse-modulated fluorometer
(FMS 2, Hansatech Instruments, Norfolk, U.K.) to examine
PSII acclimation. Attached leaves of five plants per treatment
of Q. petraea and Q. pyrenaica were alternately measured between 1100 and 1400 h over 3 days. Measurements were made
in a growth chamber with leaf temperature kept around 25 °C
by setting the air temperature to 23.5 °C and relative humidity
to 65%. For the two highest PPFs, a fan was used to prevent
leaf temperature from rising above 28 °C. Leaves were darkened for 20 min before measurements to obtain minimum (Fo )
and maximum (Fm ) values of fluorescence by applying a 0.8-s
saturating pulse (PPF = 6600 µmol m – 2 s –1 ). When the fluo-
qL =
Fm ′ − Fs Fo ′
Fm ′ − Fo ′ Fs
(8)
The yield of the three competing pathways of de-excitation of
chlorophyll in PSII, i.e., the yields of photochemistry of PSII
(ΦPSII), down-regulatory non-photochemical quenching (ΦNPQ )
and other energy losses (ΦNO ) were also calculated (Kramer et
al. 2004):
Φ PSII =
Fm ′ − Fs
(9)
Fm ′
Φ NPQ = 1 − Φ PSII − Φ NO
Φ ΝΟ =
1
 Fm ′ 

NPQ + 1 + q L 
 Fo − 1 


(10)
(11)
where NPQ is non-photochemical quenching of absorbed energy at each PPF:
NPQ =
Fm − Fm ′
Fm ′
(12)
The rate of electron transport through PSII (ETR) was calculated following Rosenqvist and van Kooten (2003):
ETR = 0. 5Φ PSII PPF 0.84
(13)
Nonlinear regression models were fitted to describe the variations in photochemical and non-photochemical yields with
PPF for each seedling. The light response of ETR was modeled by a single exponential function (Rascher et al. 2000) to
estimate the maximum electron transport rate (JETR ). Steadystate was estimated from the Fs value, rather than from Fm′,
which requires more time to reach a true steady state. The
curves thus resemble rapid light response curves where the apparent rate of electron transport is slightly underestimated
(White and Critchley 1999). The presence of the experimenter
in the growth chamber increased the CO2 concentration from
380 to 550 ppm. Hence, we could not assess mesophyll conductance from combined gas exchange and chlorophyll fluorescence measurements.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
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RODRÍGUEZ-CALCERRADA ET AL.
Anatomical variables
Sections of leaf blades held in fresh carrot pith were cut around
the middle region and immersed in formalin:acetic acid:ethanol (FAA; 5:5:90, v/v) for 24 h. The FAA was then replaced
by 70% ethanol until analysis. Measurements were made, with
a light microscope, on sections taken halfway between the
mid-rib and the edge. The cell content was destroyed with sodium hypochlorite and further stained to better distinguish tissues. The thicknesses of adaxial plus abaxial epidermis, palisade parenchyma, spongy parenchyma and leaf lamina were
measured at three locations on five leaves per species per light
treatment.
Statistical analysis
Most variables were transformed to meet assumptions of parametric analysis. We performed two-way analyses of variance
(ANOVA) to test for the significance of light treatment and
species on each variable. To test the hypothesis that acclimation differs between species, we included the interaction term
between light treatment and species in the variance model. We
used Tukey’s Honestly Significant Difference (HSD) test to
explore differences (at P < 0.05) between treatments.
Results
Gas exchange parameters
Parameters expressed on an area basis were higher in HL
plants than in LL plants. For both species, Amax,a increased on
exposure to high light in LL-HLAF and LL-HLBF plants to
values slightly lower than, but not significantly different from,
values in HL plants, and significantly higher (50%) than values in LL plants. Values of Jmax,a and Vcmax,a increased on exposure to high light in LL-HLBF and LL-HLAF plants compared
with LL plants (Table 1). On a mass basis, Amax,m, Vcmax,m and
Jmax,m did not differ between LL and HL plants. Among treatments, Amax,m was higher in LL-HLAF plants, but it did not differ significantly among LL, HL and LL-HLBF plants. Both
Vcmax,m and Jmax,m were higher in LL-HLAF plants than in
LL-HLBF plants and were generally at intermediate values in
LL and HL plants (Table 1). There were clear differences between species irrespective of light treatment, but both species
responded similarly to the treatments. Quercus petraea had
higher Amax,m, Vcmax,m and Jmax,m than Q. pyrenaica, but there
were no differences when the variables were expressed on an
area basis (Table 1). There was no effect of species or light
treatment on Jmax /Vcmax. Mesophyll resistances to CO2 diffusion, ignored in this study, would have lowered estimates of
Vcmax, but would have barely affected Jmax, resulting in the large
Jmax /Vcmax ratios observed across treatments (Piel et al. 2002).
Chlorophyll fluorescence parameters
In both species, JETR and qL were higher in HL plants than in
LL plants (Table 2). Values of JETR and qL were similar in
LL-HLAF and LL-HLBF plants, but significantly higher than
in LL plants and lower than, but not significantly different
from, values in HL plants (Table 2). The relative contributions
of photochemical (ΦPSII) and down-regulatory non-photochemical (ΦNPQ ) mechanisms for processing absorbed light
were similar among LL-HLBF, LL-HLAF and HL plants, and
different from those of LL plants (Table 2, Figure 1). In LL
plants, ΦPSII was lower and ΦNPQ higher than in plants in the
other treatments. Accordingly, the PPF at which ΦNPQ was
greater than ΦPSII was lowest in LL plants (about 225 µmol
m – 2 s – 1 ) and higher (about 700 µmol m – 2 s – 1 ) in LL-HLBF,
LL-HLAF and HL plants of Q. pyrenaica, and the corresponding values for Q. petraea ranged from about 350 µmol m – 2 s – 1
in LL plants to about 500 –550 µmol m – 2 s – 1 in LL-HLBF,
LL-HLAF and HL plants (Figure 1). The pattern of ΦNO did
not vary between species or among light treatments. Quercus
pyrenaica seedlings had higher JETR and ΦPSII(1100) than
Q. petraea seedings. Between LL-HLAF and LL plants,
ΦNPQ(1100) and the curvature of the light-response curves of
ΦPSII and ΦNPQ (parameter b of the nonlinear regression models; Figure 1) were similar in Q. petraea but differed in Q. pyrenaica (Table 1; Pinteraction (Pint ) < 0.05 considering only the
LL and LL-HLAF treatments).
Biochemical parameters
Mass-based leaf nitrogen concentration was lower in HL and
LL-HLBF plants than in LL plants, whereas it was intermediate in LL-HLAF plants. In contrast, Na was similar and higher
in HL and LL-HLBF plants than in plants in the other treatments (Table 3). The LL plants had a higher Pl than the HL and
LL-HLAF plants, with LL-HLBF plants having intermediate
values. Values of Pb were slightly higher in HL plants than in
LL plants, LL-HLAF plants had the highest values, and values
in LL-HLBF plants were closer to LL values than to HL values. Light treatment had a weak effect on Pr (P = 0.048), being
higher in LL-HLAF plants than in LL-HLBF plants and similar in LL and HL plants. There was no significant effect of
light treatment on Ps ; however, there was a tendency for a
higher Ps in LL-HLBF plants. When nitrogen fractions were
calculated per unit of photosynthetic nitrogen, LL and LLHLBF plants had less nitrogen in Rubisco [Pr /(Pr + Pb + Pl )]
than LL-HLAF and HL plants, and nitrogen in bioenergetics
[Pb /(Pr + Pb + Pl )] was similar and higher in HL, LL-HLBF
and LL-HLAF plants than in LL plants (data not shown).
Photosynthetic nitrogen-use efficiency was highest in LLHLAF plants, and intermediate in HL plants and similar in
both species. Both Nm and Pl were significantly higher in
Q. petraea than in Q. pyrenaica, independent of light treatment, whereas the reverse was true for Na and Ps.
There was a clear tendency for seedlings having a greater
fraction of nitrogen in photosynthetic components to have a
higher photosynthetic capacity (Figure 2). In both species,
Amax,m was positively correlated with both Pr and Pb (Figures 2a and 2b). As a result, there was a negative relationship
between Amax,m and Ps (Figure 2d). No significant relationship
was observed between Amax,m and Pl or Nm (Figures 2c and 2e).
Similar results were obtained with Vcmax,m and Jmax,m, in place
of Amax,m (data not shown). There were weak positive correlations between MA and Ps (r 2 = 0.19, P < 0.1 for Q. pyrenaica
and r 2 = 0.26, P < 0.05 for Q. petraea).
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765
Table 1. Means (± SE) of gas exchange parameters (n = 4–5), and F values and their significance (denoted by asterisks: * = P < 0.05; ** = P < 0.01;
and *** = P < 0.001) from two-way ANOVAs. Different letters indicate significantly different treatment means at P < 0.05 (Tukey’s HSD test following ANOVA), for both species combined when Pint = 0.05. Abbreviations: LL, plants in low light; LL-HLBF, LL plants transferred to high
light before leaf flushing; LL-HLAF, LL plants transferred to high light after leaf flushing; HL, plants in high light; Amax,a and Amax,m,
photosynthetic capacities per unit area (µmol m – 2 s –1 ) and per unit mass (µmol g – 1 s – 1 ), respectively; Vcmax,a and Vcmax,m maximum rates of
carboxylation per unit area (µmol m – 2 s –1 ) and per unit mass (µmol g – 1 s – 1 ), respectively; Jmax,a and Jmax,m maximum rates of electron transport
per unit area (µmol m – 2 s –1 ) and per unit mass (µmol g – 1 s – 1 ), respectively; and Jmax /Vcmax, ratio of maximum electron transport to maximum
carboxylation.
Treatment
Amax,a
Amax,m
Vcmax,a
Vcmax,m
Jmax,a
Jmax,m
Jmax /Vcmax
Quercus pyrenaica
LL
20.5 ± 1.5 a
LL-HLBF
33.9 ± 2.7 b
LL-HLAF
36.2 ± 2.2 b
HL
41.9 ± 5.0 b
0.50 ± 0.04 a
0.46 ± 0.04 a
0.73 ± 0.06 b
0.61 ± 0.11 a
54.0 ± 4.4 a
70.8 ± 5.8 ab
72.9 ± 8.5 b
77.2 ± 4.8 b
1.32 ± 0.08 ab
0.97 ± 0.08 a
1.47 ± 0.20 b
1.12 ± 0.13 ab
87 ± 9 a
144 ± 12 b
156 ± 14 b
183 ± 22 b
2.14 ± 0.22 a
1.96 ± 0.14 a
3.15 ± 0.36 b
2.68 ± 0.49 ab
1.63 ± 0.15
2.04 ± 0.16
2.19 ± 0.14
2.37 ± 0.21
Quercus petraea
LL
24.8 ± 1.5 a
LL-HLBF
34.1 ± 2.0 b
LL-HLAF
34.8 ± 2.3 b
HL
35.4 ± 1.3 b
0.68 ± 0.06 a
0.59 ± 0.04 a
0.85 ± 0.03 b
0.60 ± 0.04 a
57.9 ± 3.9 a
70.5 ± 1.2 ab
76.9 ± 9.7 b
86.3 ± 10.6 b
1.58 ± 0.12 ab
1.22 ± 0.06 a
1.89 ± 0.23 b
1.48 ± 0.22 ab
106 ± 5 a
149 ± 9 b
151 ± 13 b
158 ± 11 b
2.89 ± 0.21 a
2.57 ± 0.18 a
3.70 ± 0.20 b
2.71 ± 0.26 ab
1.86 ± 0.16
2.11 ± 0.14
2.01 ± 0.14
1.87 ± 0.13
F value
Treatment
Species
Interaction
8.94***
7.01*
0.91
5.35**
0.70
0.08
5.52**
9.77**
0.08
11.93***
0.04
1.01
7.24**
8.54**
0.73
2.66
0.75
2.03
14.66***
0.21
1.47
Morphological and anatomical parameters
As expected, MA was lower in LL plants than in HL plants. For
transferred plants, leaves that developed in high light
(LL-HLBF) had similar MA as HL plants, with MA being intermediate in LL-HLAF plants (Table 4). Across all light treat-
ments, MA was higher in Q. pyrenaica than in Q. petraea.
Lamina thickness changed with light treatment mainly because of changes in the palisade parenchyma (Table 4, Figure 3). Leaves of HL and LL-HLBF plants were thicker and
had thicker palisade parenchyma (generally with two layers of
Table 2. Means (± SE) of chlorophyll fluorescence parameters (n = 4–5), and F values and their significance (denoted by asterisks: * = P < 0.05;
** = P < 0.01; and *** = P < 0.001) from two-way ANOVAs. Different letters indicate significantly different treatment means at P < 0.05 (Tukey’s
HSD test following ANOVA), for both species combined when Pint = 0.05. Abbreviations: LL, plants in low light; LL-HLBF, LL plants transferred
to high light before leaf flushing; LL-HLAF, LL plants transferred to high light after leaf flushing; HL, plants in high light; JETR (µmol m – 2 s – 1 ),
maximum electron transport rate from fluorescence; qL(1100), photochemical quenching at 1100 µmol m – 2 s – 1 PPF; ΦPSII(1100), effective photochemical quantum yield of PSII at 1100 µmol m – 2 s –1 PPF; ΦNPQ(1100), yield of downregulatory non-photochemical quenching at 1100 µmol
m – 2 s –1 PPF; bΦPSII and bΦNPQ, curvature of light responses of ΦPSII and ΦNPQ, respectively.
Treatment
JETR
qL(1100)
ΦPSII(1100)
ΦNPQ(1100)
bΦPSII (10 –3 )
bΦNPQ (10 –3 )
Quercus pyrenaica
LL
LL-HLBF
LL-HLAF
HL
53 ± 9 a
123 ± 12 b
123 ± 12 b
140 ± 16 b
0.13 ± 0.02 a
0.25 ± 0.03 b
0.23 ± 0.02 b
0.27 ± 0.03 b
0.12 ± 0.01 a
0.26 ± 0.02 b
0.26 ± 0.02 b
0.29 ± 0.03 b
0.63 ± 0.01 b
0.50 ± 0.04 a
0.50 ± 0.02 ab
0.50 ± 0.04 a
4.30 ± 0.60 b
1.74 ± 0.17 a
1.47 ± 0.14 a
1.57 ± 0.17 a
4.11 ± 0.56 b
1.29 ± 0.15 a
1.12 ± 0.17 a
1.35 ± 0.22 a
Quercus petraea
LL
LL-HLBF
LL-HLAF
HL
61 ± 6 a
93 ± 16 b
93 ± 13 b
107 ± 20 b
0.12 ± 0.01 a
0.19 ± 0.03 b
0.23 ± 0.03 b
0.25 ± 0.06 b
0.13 ± 0.01 a
0.20 ± 0.03 b
0.20 ± 0.03 b
0.23 ± 0.04 b
0.59 ± 0.02 b
0.55 ± 0.03 a
0.58 ± 0.03 ab
0.53 ± 0.02 a
2.89 ± 0.51 b
2.26 ± 0.45 a
2.41 ± 0.55 a
1.84 ± 0.56 a
2.69 ± 0.52 b
1.74 ± 0.35 a
2.08 ± 0.51 a
1.70 ± 0.61 a
F value
Treatment
Species
Interaction
8.38***
4.74*
0.95
6.40**
1.13
0.39
9.31**
4.38*
0.94
4.61**
2.27
1.65
9.02***
1.09
1.58
7.38**
0.49
2.70
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RODRÍGUEZ-CALCERRADA ET AL.
Figure 1. Photochemical and non-photochemical yields of absorbed energy with photosynthetic photon flux (PPF) [ΦPSII = m +
aexp(–bPPF); ΦNPQ = m(1 – exp(–bPPF));
ΦNO = m – aexp(–bPPF)] in seedlings of
Quercus pyrenaica and Q. petraea. Treatments: (a, b) low light; (c, d) plants transferred
to high light 1 week before leaf flushing; (e, f )
plants transferred to high light 3 months after
leaf flushing; and (g, h) high light. Symbols:
ΦPSII, 䉱 and 䉭; ΦNPQ, 䊏 and 䊐; and ΦNO, 䊉
and 䊊. Vertical lines indicate PPF at which
ΦPSII = ΦNPQ. Values are means (n = 4–5) ±
SE.
palisade cells) than LL and LL-HLAF plants, with some differences between species in these patterns (Pint < 0.05). Quercus pyrenaica seedlings generally had thicker palisade parenchyma in the HL treatment and thinner palisade parenchyma
in the LL treatment than Q. petraea seedlings. Leaves of LLHLAF plants barely altered their anatomy on exposure to high
light, although two out of the five samples of Q. pyrenaica
(none of Q. petraea) had a double layer of palisade cells, resulting in a slight increase in lamina thickness compared with
LL samples, which had a single layer of palisade cells. There
were no significant effects of light or species on the thickness
of epidermal and spongy parenchyma tissues. Therefore, the
ratio of palisade to spongy parenchyma thickness was similar
and higher in LL-HLBF (1.63) and HL (1.46) plants compared
with LL (0.67) and LL-HLAF (0.87) plants (Pspecies > 0.15,
Pint > 0.15).
Discussion
Leaf plasticity to light in long-term acclimated plants
Quercus petraea and Q. pyrenaica leaves acclimated both
functionally and structurally to the prevailing irradiance. The
HL plants had thicker leaves, with a thicker palisade parenchyma, and greater Vcmax, Jmax and Amax,a than the LL plants (cf.
Ellsworth and Reich 1992, Evans and Poorter 2001). Such
changes enabled HL plants to exploit high irradiances more efficiently than LL plants, because they can regenerate more
NADP and ADP to alleviate the over-reduction of PSII centers
at high PPFs and minimize the risk of photoinhibition (Chow
1994, Baker and Oxborough 2004). This functional difference
would partly explain the gentler decline in ΦPSII with increasing PPF in HL plants compared with LL plants (Figure 1), although differences in the rate of photosynthetic induction between LL and HL plants cannot be ignored.
Some acclimatory changes in the fractionation of nitrogen
among pools increased photosynthetic capacity in HL plants
(Hikosaka and Terashima 1995, Niinemets and Tenhunen 1997,
Niinemets et al. 1998). Values of Pr were similar among treatments, although Pb tended to be higher in HL than in LL plants
at the expense of lower Pl (Table 3). Nitrogen fractions in Rubisco and bioenergetics expressed per unit of photosynthetic
nitrogen were also higher in HL plants than in LL plants.
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LEAF RESPONSES TO LIGHT IN TWO CO-OCCURRING WHITE OAKS
767
Table 3. Means (± SE) of biochemical parameters (n = 4–5), and F values and their significance (denoted by asterisks: * = P < 0.05; ** = P < 0.01;
and *** = P < 0.001) from two-way ANOVAs. Different letters indicate significantly different treatment means at P < 0.05 (Tukey's HSD test following ANOVA), for both species combined when Pint = 0.05. Abbreviations: LL, plants in low light; LL-HLBF, plants transferred to high light
before leaf flushing; LL-HLAF, plants transferred to high light after leaf flushing; HL, plants in high light; Nm (mg g – 1 ), nitrogen concentration
per unit leaf mass; Na (g m – 2 ), nitrogen concentration per unit leaf area; Pl (%), nitrogen fraction in light-harvesting components; Pb (%), nitrogen
fraction in electron transport proteins; Pr (%), nitrogen fraction in Rubisco; Ps (%), nitrogen fraction in structural components; and PNUE (µmol
g –1 s –1 ), photosynthetic nitrogen-use efficiency.
Treatment
Nm
Na
Pl
Quercus pyrenaica
LL
29.9 ± 1.8 b
LL-HLBF
27.5 ± 1.4 a
LL-HLAF
28.8 ± 1.0 ab
HL
26.9 ± 0.9 a
1.23 ± 0.10 a
1.99 ± 0.10 b
1.44 ± 0.07 a
1.93 ± 0.11 b
24.9 ± 2.5 b
19.9 ± 2.8 ab
18.5 ± 1.4 a
18.2 ± 1.7 a
5.7 ± 0.4 a
5.8 ± 0.6 a
8.8 ± 1.1 b
7.7 ± 1.3 b
34.4 ± 0.9 ab
28.2 ± 3.5 a
39.9 ± 5.5 b
31.8 ± 3.8 ab
35.0 ± 2.9
46.0 ± 6.2
32.8 ± 7.4
42.4 ± 5.7
16.9 ± 1.4 a
17.1 ± 1.3 a
25.3 ± 2.2 b
22.1 ± 3.5 ab
Quercus petraea
LL
35.1 ± 1.8 b
LL-HLBF
28.5 ± 1.8 a
LL-HLAF
32.2 ± 1.8 ab
HL
27.2 ± 1.8 a
1.29 ± 0.05 a
1.61 ± 0.11 b
1.33 ± 0.15 a
1.61 ± 0.11 b
30.7 ± 1.2 b
23.9 ± 2.3 ab
25.2 ± 2.7 a
20.3 ± 1.8 a
6.5 ± 0.3 a
7.1 ± 0.4 a
9.2 ± 0.4 b
8.0 ± 0.8 b
35.2 ± 3.2 ab
33.5 ± 2.6 a
45.7 ± 4.4 b
42.9 ± 6.5 ab
27.6 ± 4.4
35.4 ± 3.2
19.9 ± 5.6
28.8 ± 7.8
19.2 ± 1.2 a
20.6 ± 1.4 a
26.8 ± 1.5 b
22.4 ± 1.7 ab
F value
Treatment
Species
Interaction
12.51***
4.97*
1.48
5.27**
9.15**
0.42
7.12***
3.32
0.33
2.93*
3.60
0.46
2.32
7.24*
0.11
7.71***
1.92
0.24
6.43**
6.58*
1.16
Pb
Pr
Ps
PNUE
Figure 2. Relationships between leaf nitrogen
estimated in (a) Rubisco (Pr ), (b) photosynthetic electron transport (Pb ), (c) light harvesting (Pl ) and (d) structural components (Ps ),
and (e) mass-based leaf nitrogen concentration
(Nm ), with mass-based photosynthesis in seedlings of Q. petraea (open symbols, dashed
lines) and Q. pyrenaica (filled symbols, continuous lines) treated with low light (䊊, 䊉),
high light (䊐, 䊏), plants transferred to high
light 1 week before leaf flushing (䉭, 䉱) and
plants transferred to high light 3 months after
leaf flushing (䉫, 䉬) . Regression lines are (a):
y = 0.45 lnx – 0.73 for Q. pyrenaica and y =
0.28 lnx – 0.17 for Q. petraea, (b): y = 0.49
lnx – 0.25 for Q. pyrenaica and y = 0.57 lnx –
0.36 for Q. petraea, (d): y = –0.49 lnx + 2.58
for Q. pyrenaica and y = –0.36 lnx + 2.07 for
Q. petraea; regression lines indicated when
P < 0.1.
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768
RODRÍGUEZ-CALCERRADA ET AL.
Table 4. Means (± SE) of morphological parameters (n = 4–5), and F values and their significance (denoted by asterisks: * = P < 0.05; ** =
P < 0.01; and *** = P < 0.001) from two-way ANOVAs. Different letters indicate significantly different treatment means at P < 0.05 (Tukey’s
HSD test following ANOVA), for both species combined when Pint = 0.05. Abbreviations: LL, plants in low light; LL-HLBF, LL plants transferred to high light before leaf flushing; LL-HLAF, LL plants transferred to high light after leaf flushing; HL, plants in high light; MA (g m – 2 ), leaf
dry mass per area; TL (µm), leaf thickness; TE (µm), epidermis thickness; TPP (µm), palisade parenchyma thickness; and TSP (µm), spongy parenchyma thickness.
Treatment
MA
TL
TE
TPP
TSP
Quercus pyrenaica
LL
LL-HLBF
LL-HLAF
HL
40.9 ± 1.0 c
72.6 ± 1.5 a
50.3 ± 2.2 b
67.9 ± 3.7 a
91 ± 3 a
132 ± 8 bc
112 ± 6 ab
154 ± 13 c
24.2 ± 1.3
28.3 ± 1.3
27.0 ± 0.9
28.5 ± 2.5
26.3 ± 1.0 a
59.1 ± 6.2 bc
41.7 ± 5.7 ab
75.1 ± 7.0 c
40.3 ± 2.0
44.4 ± 3.3
43.2 ± 1.4
50.0 ± 4.3
Quercus petraea
LL
LL-HLBF
LL-HLAF
HL
37.4 ± 1.4 c
56.6 ± 2.2 a
40.9 ± 2.9 b
58.7 ± 2.5 a
101 ± 4 a
134 ± 7 b
99 ± 3 a
128 ± 4 b
25.0 ± 0.9
27.4 ± 1.2
25.9 ± 1.5
26.4 ± 0.7
30.5 ± 1.1 a
69.5 ± 5.6 b
30.9 ± 1.9 a
59.1 ± 2.9 b
45.3 ± 2.3
37.5 ± 3.6
41.7 ± 1.2
42.1 ± 2.3
F value
Treatment
Species
Interaction
62.04***
29.64***
1.07
22.73***
1.21
2.89*
1.91
0.61
0.37
52.70***
0.87
3.57*
1.02
2.38
2.42
Light-induced increases in MA (i.e., increased mesophyll tissue) are sometimes more important in enhancing photosynthetic capacity than variations in nitrogen allocation within
leaves (Ellsworth and Reich 1992, Evans and Poorter 2001,
Parelle et al. 2006, Katahata et al. 2007), as is supported by our
finding of a constant amount of photosynthetic machinery per
unit dry mass in LL and HL seedlings of both species (i.e.,
similar values of Vcmax,m, Jmax,m and Amax,m; Table 1).
Hence, Q. petraea and Q. pyrenaica seedlings acclimated to
the prevailing irradiance, but did so in slightly different ways.
Quercus petraea seedlings had greater plasticity in leaf nitrogen concentration and partitioning to light-harvesting pigments, whereas Q. pyrenaica seedlings had greater plasticity
in mesophyll thickness, chlorophyll fluorescence parameters
and area-based gas exchange parameters. These results are
consistent with the slightly superior shade tolerance of Q. petraea (Rodríguez-Calcerrada et al. 2007a, 2007b) as discussed
elsewhere (Niinemets 1997, Cao 2000, Niinemets and Valladares 2004).
ditional layer, thereby increasing the proportion of HLadapted palisade chloroplasts relative to chloroplasts in the
spongy mesophyll (Terashima and Inoue 1984).
Thus, leaf acclimation to HL is governed by the accumulation of photosynthetic tissue per unit area. Area-based photosynthetic parameters of LL-HLBF leaves increased as much as
in LL-HLAF leaves, and did not differ significantly from those
of HL leaves. In contrast, mass-based estimates (Vcmax,m, Jmax,m
and Amax,m ) in LL-HLBF leaves were similar or slightly lower
than in LL and HL leaves, but lower than in LL-HLAF leaves
(Table 1). Nitrogen redistribution among photosynthetic components on transfer from LL to HL would have contributed to
reduced photosynthetic efficiency per unit dry mass in LLHLBF plants. A higher MA in LL-HLBF leaves is likely due to
a greater mesophyll cell wall thickness, which would explain
the tendency for a greater quantity of structural nitrogen components in these leaves, which might limit CO2 diffusion into
the chloroplasts (Miyazawa and Terashima 2001) and reduce
PNUE (Table 3).
Acclimation of leaves of shade-developed plants to high light
before flushing
High-light acclimation in shade-developed leaves
Leaf dry mass per unit area of LL-HLBF leaves increased to
HL values 5 months after transfer to the HL treatment, corresponding at least in part to an increase in thickness of the palisade parenchyma (Table 4). Others have reported significant
increases in lamina thickness in tree species of various successional positions and shade-tolerances when irradiance increased before bud break (Goulet and Bellefleur 1986, Aranda
et al. 2001), indicating considerable anatomical flexibility in
shade-induced primordia (cf. Eschrich et al. 1989). It is likely
that, in LL-HLBF leaves, palisade parenchyma cells enlarged
while developing in high light and then divided to form an ad-
Leaves of both oak species acclimated to HL after flushing
in LL, as observed in both evergreen and deciduous trees
(Strauss-Debenedetti and Bazzaz 1991, Naidu and DeLucia
1997b, 1998). Oguchi et al. (2003) reported that a limited capacity for change in thickness of mature shade-developed
leaves limits photosynthetic acclimation to increased irradiance. In our study, however, after only 4 weeks of HL exposure, and despite little anatomical change, Amax,a, Vcmax,a, Jmax,a
and PNUE all increased in leaves of LL-grown plants transferred to HL. On a dry mass basis, key photosynthetic traits,
Vcmax,m and Jmax,m , increased rapidly following transfer from
LL to HL (Tables 1–3). We suggest that rapid reorganization
TREE PHYSIOLOGY VOLUME 28, 2008
LEAF RESPONSES TO LIGHT IN TWO CO-OCCURRING WHITE OAKS
769
Figure 3. Transverse sections of
leaves of seedlings of Q. pyrenaica (a–d) and Q. petraea (e–h).
Depth of sections is 20–30 µm.
Treatments: (a, e) high light; (b, f)
plants transferred to high light
1 week before leaf flushing; (c, g)
plants transferred to high light
3 months after leaf flushing; and
(d, h) high light. Bars respresent
50 µm.
in the protein pool largely accounted for this pattern (Yamashita et al. 2000, Frak et al. 2001, Han et al. 2006) and counteracted the carry-over effects of anatomical shade acclimation of
the LL-grown plants.
On exposure to HL, Pl decreased in parallel with increased
Pr and Pb, suggesting a rapid remobilization of nitrogen among
photosynthetic components. The degradation of chlorophyllbinding proteins in response to high irradiances can facilitate
the synthesis of Rubisco and compounds involved in electron
transport (Yang et al. 1998, Walters 2005). These responses increase photosynthetic light-use efficiency and reduce ΦNPQ
(Naidu and DeLucia 1997b, Müller et al. 2001, RodríguezCalcerrada et al. 2007a) by reducing the excess energy to be
dissipated (Rosenqvist and van Kooten 2003, Baker and Oxborough 2004; Figure 1, Table 2). Other factors may have contributed to the increased photosynthetic capacity of the LLHLAF plants. For instance, Oguchi et al. (2003 and 2005)
found that the surface of chloroplasts facing the intercellular
spaces increased after transfer from low to high light as a result
of increased chloroplast volume.
Interspecific differences in leaf acclimation of shadedeveloped plants
We saw differences between species in many leaf traits.
Whereas Q. pyrenaica seedlings had a greater capacity for
electron transport at high PPF (ΦPSII(1100) and JETR ), Q. petraea seedlings had higher Amax,m, Vcmax,m, Jmax,m and Pl, and
lower MA and Ps (Tables 1–4). Lower Amax,m in Q. pyrenaica
than in Q. petraea was partly attributable to the greater proportion of non-photosynthetic nitrogen, although differences in
photorespiration and internal diffusion of CO2 cannot be ruled
out. Additionally, the slower growth of Q. pyrenaica in the
month preceding photosynthetic measurements (66% lower
height growth than in Q. petraea for all treatments pooled;
data not shown) may have caused end-product inhibition of
photosynthesis (Paul and Foyer 2001).
Overall, these results point to greater shade tolerance and
competitive ability of Q. petraea seedlings compared with
Q. pyrenaica seedlings (Reich et al. 1999), although PNUE
was similar between species (Wright et al. 2001, Lusk et al.
2003). Notwithstanding the poorer photosynthetic perfor-
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770
RODRÍGUEZ-CALCERRADA ET AL.
mance per unit dry mass of Q. pyrenaica seedlings, no differences in the mechanisms of acclimation and negligible differences in the extent of acclimation were observed for a plethora
of leaf traits, perhaps because ecological differences between
the species are small enough that distinct patterns of acclimation of photosynthesis under conditions of optimal nutrient
and water availability do not occur. The only differences in acclimation response between species were in LL-HLAF seedlings, which, in Q. pyrenaica but not Q. petraea, tended to
have thicker leaves and palisade parenchyma than LL plants. It
is likely that the second layer of palisade cells was already
formed before transfer from LL to HL in some Q. pyrenaica
seedlings. Significant enlargement of mesophyll cells has been
observed in mature leaves of the deciduous species Acer
rufinerve Siebold & Zucc. on exposure to high light (Oguchi et
al. 2005).
In conclusion, leaves of Q. petraea and Q. pyrenaica seedlings acclimated to increased irradiance by an increase in
photosynthetic capacity resulting from adjustments in both
physiological and morphological traits. The extent of these
changes, which were similar in both species, depended on
whether the increase in irradiance occurred before or after leaf
expansion.
Acknowledgments
This work was supported by the Consejería de Medio Ambiente y
Desarrollo General de la Comunidad Autónoma de Madrid. JR-C was
supported by a scholarship from the Consejería de Educación de la
Comunidad de Madrid (C.M.) and the Fondo Social Europeo (F.S.E.),
and PBR participation was supported in part by the National Science
Foundation LTER Program.
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