Mesophyll conductance constrains photosynthesis in three common sclerophyllous species in Central Chile
© Brito et al.; licensee Springer 2014
Received: 14 February 2014
Accepted: 18 June 2014
Published: 16 August 2014
Quillaja saponaria Mol., Cryptocarya alba Mol. Looser, and Lithraea caustica Molina Hook et Arn., are common sclerophyllous species in Mediterranean Central Chile. Mesophyll conductance, gm, may strongly limit photosynthesis in these semiarid environments.
Simultaneous measurements of gas exchange and chlorophyll fluorescence were carried out in 45 nursery plants from these species to determine diffusional and biochemical limitations to photosynthesis. Values of stomatal conductance, gs, were greater than those of mesophyll conductance, gm, while their ratio (gm/gs) was not influenced by species being on average 0.47. Relative limitations posed by mesophyll conductance to photosynthesis, Lm, (0.40 ± 0.02) were high compared to those imposed by stomata, Ls (0.07 ± 0.01). The average CO2 concentration in the intercellular air spaces (Ci) was 32 μmol mol−1 lower than in the atmosphere (Ca), while the average CO2 concentration in the chloroplasts (Cc) was 131 μmol mol−1 lower than Ci independent of species. Maximal rates of Rubisco carboxylation, Vcmax, and maximal electron transport rates driving regeneration of RuBP, Jmax, ranged from 13 to 66 μmol CO2 m−2 s−1 and from 33 to 148 μmol electrons m−2 s−1, respectively, and compare well to averages for C3 plants.
Photosynthetic performance was in the series: Q. saponaria > C. alba ≥ L. caustica, which can be attributed first to mesophyll conductance limitations, probably mediated by leaf anatomical traits and then to species specific foliage N partitioning strategies.
KeywordsChloroplastic CO2 concentration Electron transport Mesophyll conductance Rubisco carboxylation Sclerophyllous species
The biochemical model of leaf photosynthesis originally proposed by Farquhar et al. () and later improved (von Caemmerer and Farquhar, ; Sharkey, ; Harley and Sharkey, ) is widely used in ecophysiological research for describing CO2 exchange processes and to scale carbon exchange from leaves to canopies (Baldocchi and Harley ; McMurtrie et al. ; Whitehead et al. ). In this model, photosynthesis is considered to be limited by the maximal rate of ribulose-1,5-bis phosphate (RuBP) carboxylase-oxygenase (Rubisco) carboxylation, Vcmax, and by the maximal electron transport rate driving regeneration of RuBP, Jmax, and by triose phosphate utilization (TPU) (Farquhar et al. ; von Caemmerer ; von Caemmerer and Farquhar ). These parameters are fitted to the response of photosynthesis, A, to the CO2 concentration in the intercellular air spaces, Ci, known as A/Ci curves. Values of Ci, are estimated from stomatal conductance to CO2 transfer, gs, and the ambient CO2 concentration external to the leaf, Ca. This model has been used to explain the mechanisms of photosynthetic acclimation to elevated atmospheric CO2 (Griffin et al. ; Hogan et al. ; Kellomaki and Wang ; Murray et al. ; Turnbull et al. ), the influence of global warming on plant carbon budgets (Turnbull et al. ), and for identifying factors limiting photosynthesis under water stressed conditions in Mediterranean plants (Grassi and Magnani ; Gulias et al. ; Niinemets et al. [2009b]), among others.
In most studies, the mesophyll conductance of CO2 from the intercellular air spaces to the sites of Rubisco carboxylation in the chloroplasts, gm, has been considered to be sufficiently large to be negligible (Farquhar et al. ). However, there is a growing awareness that the significance of gm in limiting photosynthesis can be similar to the limitation imposed by stomata (Flexas et al. ; Harley et al. ; Loreto et al. ; von Caemmerer ; Warren and Adams ; Warren et al. ). As a result, Ci is greater than the CO2 concentration in the chloroplasts, Cc, and values of Vcmax and Jmax are underestimated when fitted to estimates of Ci rather than Cc.
Arid and semiarid lands account for 41% of Chile’s continental territory, covering about 31 million ha (Benites et al. ). Within this area, semiarid sclerophyllous (i.e. a woody plant with small coriaceous evergreen leaves dominant of the Mediterranean region) shrublands and forests extends from 32-36° S latitude (~345,000 ha) in Central Chile (Armesto et al. ; CONAF ); exhibiting high levels of endemism, and are therefore considered a priority for biodiversity conservation (Arroyo et al. ). These ecosystems are subjected to high radiative and water stresses that limit their development and reproduction (Cabrera ); and, additionally, have a long history of degradation by human activity, which may represent an important adaptive pressure (Galmes et al. ). Therefore, understanding how environmental limitations are imposed on the carbon budget is relevant to accurately estimate carbon uptake and water use by sclerophyllous species.
There is extensive work on comparisons of gm between species and plant functional groups (Loreto et al. ; De Lucia et al. ; Hassiotou et al. ; Niinemets et al. [2009b]). However, little is known about the extent to which gm regulates the rate of photosynthesis in sclerophyllous species of central Chile. Consequently we chose to work with three native sclerophyllous species: Quillaja saponaria Mol., Cryptocarya alba Mol. Looser and Lithraea caustica Molina Hook et Arn., to determine stomatal, mesophyll and biochemical limitations to photosynthesis. Specifically, we assessed whether mesophyll conductance to CO2 induces similar constrains to photosynthesis across different sclerophyllous species.
Plant material consisted of 15 randomly selected plants from each of the following species: Q. saponaria, C. alba and L. caustica, from a nursery of the Faculty of Forestry and Nature Conservation at University of Chile, Santiago, Chile. Seeds were sown in the winter 2008, and transferred during spring 2008 and spring 2009 to 12 × 15 cm (0.25 L) and 20 × 30 cm (2 L) black polyethylene bags filled with an even mixture of composted plant residues, soil and sand. No fertilizers were applied. Plants developed under 46% shading (in order to mimic the light environment experienced by saplings in their natural habitat) and received weekly irrigation during winter, and daily irrigation to field capacity in other seasons. At the time of measurements, we selected fifteen homogenous plants of Q. saponaria, C. alba and L. caustica which exhibited an average (±1 SD) plant height of 82.9 ± 14.4 cm, 63.4 ± 18.9 cm, and 47.6 ± 15.3 cm; and a collar diameter of 7.5 ± 0.8 mm, 9.1 ± 1.4 mm, and 11.0 ± 2.6 mm, respectively. All gas exchange and chlorophyll fluorescence measurements were taken in a laboratory without thermal regulation, with open windows to allow circulation of fresh air. Measurements took 45 days; with only one plant measured per day, spread in the summer period from December 20, 2010 to March 15, 2011; six months after plants were transferred from small to large containers. Gas exchange measurements for each individual plant typically took all day between 10 am and 6 pm; and followed the exact same sequence of measurements for all plants (see below). We alternated species each day in order to avoid differences brought about by day to day meteorological changes.
Gas exchange measurements
Simultaneous measurements of gas exchange and chlorophyll a fluorescence were carried out on the 45 selected plants, using a portable photosynthesis system (CIRAS-2, PP Systems, MA, USA) equipped with an integrated chlorophyll fluorescence and gas exchange chamber (PLC6-U Auto Leaf Cuvette, PP System, MA, US). Plants were shifted from the nursery to the laboratory the day before measurements were undertaken.
For each plant, a fully-developed leaf in the upper third of the plant was chosen and placed inside a circular 2.5 cm2 (18 mm in diameter) cuvette. Temperature in the cuvette (block) was maintained at 25ºC while leaf-to-air vapour pressure deficit (VPD) was maintained below 1 kPa. Each leaf was left to equilibrate inside the cuvette for 10 min at about 368 ± 3 μmol mol−1 CO2 concentration and saturating irradiance (2,000 μmol photons m−2 s−1), before measuring the response of net assimilation (A) to intercellular CO2 concentration (Ci). External CO2 concentration (Ca) was supplied with a CO2 mixer across the sequence 25, 50, 75, 100, 200, 300, 400, 500, 600, 700, 800, 900, 1000, 1200 and 1500 μmol mol−1, with saturating irradiance, Q (400–700 nm), maintained at 2,000 μmol m−2 s−1. Measurements were recorded after values of A, Ci and gs became stable but with a minimum waiting time of 3 min at each step within the sequence. At each value of Ci, measurements of fluorescence for the light-adapted leaf were made simultaneously to the gas exchange measurements. Values of F and Fm’ (the steady and maximal fluorescence respectively), were used to calculate photochemical efficiency of photosystem II, ΦPSII. The response of net assimilation to irradiance (A/Q curves) was measured immediately after each A/Ci curve ended, across the Q sequence: 0, 50, 100, 150, 200, 300, 400, 500, 800, 1000, 1200, 1400, 1600, 1800 and 2000 μmol m−2 s−1, with ambient CO2 concentration maintained at 368 ± 3 μmol mol−1 using a CO2 mixer. The A/Ci and A/Q curves were measured on the same foliage sample.
where Vcmax is the maximum rate of Rubisco carboxylation under saturating RuBP and CO2, Ci and Oi are the intercellular CO2 and O2 concentrations, Γ* is the CO2 compensation concentration in the absence of day respiration, and Kc and Ko are the Michaelis constants for CO2 and O2, respectively.
where J is the rate of electron transport at a given irradiance Q.
where θ is the convexity of the non-rectangular hyperbola, α is the initial slope of the A/Q curve (often referred as ‘apparent maximum quantum efficiency’), Asat is the light-saturated photosynthetic capacity and Rdark the respiration rate at zero irradiance. Individual A/Q response curves were fitted using Eq. 4 in order to estimate α, Asat and Rdark. The light saturation point, Qsat, was calculated as the irradiance for which 90% of Asat was achieved.
The photosynthesis model described by Farquhar et al. () (Eq. 1) was fitted to the A/Ci and A/Cc curves by non-linear least squares regression (SigmaPlot, Version 12.1, SPSS, Chicago, IL). Values of Vcmax and Rd were estimated from the lower part of the A/Ci or A/Cc curve (Ci or Cc < 220 μmol mol−1) (Eq. 1 and 2), and these values were then used to estimate Jmax over the entire range of measured Ci or Cc (Eq. 1,2 and 3). Michaelis-Menten constants of Rubisco for CO2 and O2, Kc and Ko, used in the fitting (25 °C) were 404.9 μmol mol−1 and 278.4 mmol mol−1, respectively as described by Bernacchi et al. ().
Calculations of mesophyll conductance
The photochemical efficiency of photosystem II (ΦPSII) was estimated from chlorophyll fluorescence measurements as (Fm’ – F) / Fm’, where F and Fm’ are the steady and maximal fluorescence in the light-adapted sample respectively (Schreiber et al. ). The values of ΦPSII are directly proportional to the rate of electron transport through photosystem II, and therefore can be used to determine the portion of the A/Ci curve where the rate of electron transport is constant (Genty et al. ) (Figure 2a). Optimal values for gm were resolved iteratively from three or more measurements of photosynthesis at high values of Ci that correspond with constant rates of electron transport (Singsaas et al. ; Warren ). This was done using the Generalized Reduced Gradient Nonlinear Solving Method for nonlinear optimization included in the Solver Tools of Microsoft Excel with measurements of A, Ci, Γ*, Rd* to resolve the value of gm that best explained changes in photosynthesis with changes in Ci indicated by minimum variance in J (Harley et al. ; Singsaas et al. ; Warren ) (Figure 2b).
Stomatal and mesophyll limitations to photosynthesis
A/Ci response and values for gs and gm, were used to partition stomatal, mesophyll and biochemical limitations to photosynthesis. Values of stomatal conductance to CO2 transfer were calculated by gs = A/(Ca-Ci) dividing values by 1.64 (Jones ). Relative stomatal limitations were calculated using the method of Farquhar and Sharkey () as Ls = 1 – Aa-gs / Ai-gs where Aa-gs and Ai-gs are the actual value of A and the value estimated when gs is infinite, respectively. Similarly, following Bernacchi et al. (), relative limitation to photosynthesis imposed by gm was calculated as: Lm = 1 – Aa-gm / Ai-gm where Aa-gm and Ai-gm are the actual value of A and the value estimated when gm is infinite, respectively. The CO2 concentration in the chloroplasts, Cc, was calculated from Cc = Ci – A/gm.
Foliage surface area and nutrient concentrations
Following the completion of A/Ci and A/Q curves, the leaf was carefully removed from the cuvette, scanned to determine leaf area by optical methods, dried at 70°C to constant mass and then both measurements used to calculate the foliage area to mass ratio, M. Foliage samples were finely ground, Dumas combusted and N concentrations determined by thermo conductivity (LECO, TruSpec CN, US) at the Laboratory of Soil and Foliar Analysis at Universidad Católica de Chile, Santiago, Chile. Nitrogen foliage concentrations are expressed on a hemi-surface area basis (Na) and photosynthetic nitrogen-use efficiency, EN, defined as Asat/Na.
All statistical analyses were undertaken at the plant level using The R System (R Core Team ). Variables were tested for normality and homogeneity of variance and transformations were made as necessary to meet the underlying statistical assumptions of the models used. All values are presented as means ± 1 standard error (n = 15) unless stated otherwise. A one way analysis of variance was used to compare diffusional and biochemical limitations to photosynthesis between sclerophyllous species. Tukey’s least significant difference test was used to distinguish among individual means where applicable with a confidence level of P < 0.05. Differences in slopes and intercepts in the linear relationships between photosynthetic parameters and foliar nitrogen among sclerophyllous species were tested for significance by analysis of covariance.
Results and discussion
Overall photosynthetic performance
Comparison of leaf and photosynthetic parameters for three common sclerophyll species in Central Chile
(μmol m−2 s−1)
7.8 ± 0.7 a
9.5 ± 0.4 a
14.2 ± 0.8 b
0.019 ± 0.002
0.024 ± 0.002
0.023 ± 0.002
(μmol m−2 s−1)
0.7 ± 0.1
1.0 ± 0.2
0.6 ± 0.1
(μmol m−2 s−1)
987 ± 65 a
964 ± 56 a
1168 ± 57b
(μmol m−2 s−1)
36 ± 8
51 ± 9
27 ± 4
(μmol H2O m−2 s−1)
2133 ± 447
2913 ± 476
3492 ± 654
1 / WUE
(mol H20 mol−1CO2 )
376 ± 93
347 ± 57
285 ± 60
7 ± 0.4 a
10 ± 0.7 b
8.7 ± 0.5 ab
120.2 ± 8.9 a
195.5 ± 21 b
165.8 ± 17.6 ab
(μmol mol−1 s−1)
69.8 ± 9.1 ab
56.4 ± 6.2 a
95.9 ± 8.8 b
(μmol mol−1 s−1)
12.03 ± 0.86 a
17.01 ± 0.81 b
23.81 ± 1.18 c
0.038 ± 0.003 a
0.047 ± 0.002 a
0.070 ± 0.004 b
(mol m−2 s−1 bar−1)
0.06 ± 0.005 a
0.065 ± 0.004 a
0.097 ± 0.007 b
(mol m−2 s−1)
0.221 ± 0.03
0.221 ± 0.025
0.25 ± 0.018
g m / g s
0.54 ± 0.18
0.47 ± 0.14
0.43 ± 0.06
0.07 ± 0.01
0.07 ± 0.02
0.08 ± 0.01
0.35 ± 0.03
0.42 ± 0.02
0.43 ± 0.02
368.3 ± 0.6
368.7 ± 1
368.7 ± 0.6
337.7 ± 7
336.5 ± 6.9
333.6 ± 3.7
220 ± 10.3
202.2 ± 8.2
192.8 ± 5.9
(μmol m−2 s−1)
26.8 ± 2.1 a
32.6 ± 1.1 a
49 ± 2.6 b
(μmol m−2 s−1)
56.3 ± 4.1 a
79.6 ± 3.8 a
111.4 ± 5.6 b
Jmax/ Vcmax (Ci)
2.15 ± 0.1
2.44 ± 0.07
2.29 ± 0.07
(μmol m−2 s−1)
45.5 ± 5.1 a
64.4 ± 3.8 a
98.3 ± 5.7 b
(μmol m−2 s−1)
60.4 ± 4.4 a
89.9 ± 4.2 b
126.4 ± 6.1 c
Jmax/ Vcmax (Cc)
1.41 ± 0.07
1.43 ± 0.06
1.31 ± 0.05
R d *
(μmol m−2 s−1)
1.0 ± 0.1 a
1.7 ± 0.2 b
1.5 ± 0.1 b
33 ± 4.2 ab
23.2 ± 2.3 a
34 ± 2.4 b
55.5 ± 5.4
56.8 ± 4.1
59.2 ± 5.9
The response of photosynthetic rates (A) to internal CO2 concentration (Ci) (Figure 3b), changed drastically among species for the whole range of Ci values in the series: Q. saponaria > C. alba > L. caustica. Consequently the initial slope of the A/Ci curves (dA/dCi; often referred to as ‘carboxylation efficiency’) was greater in Q. saponaria (0.070) compared with C. alba (0.047) and L. caustica (0.038). A similar trend was observed for the rate of photosynthesis near saturating Ci (800 μmol mol−1), Amax, being 12.03, 17.01 and 23.81 μmol CO2 m−2 s−1 for L. caustica, C. alba and Q. saponaria, respectively (Table 1).
Mesophyll conductance (gm) was similar between L. caustica (0.060 mol CO2 m−2 s−1 bar−1) and C. alba (0.065 mol CO2 m−2 s−1 bar−1), but collectively significantly lower than Q. saponaria (0.097 mol CO2 m−2 s−1 bar−1). Although unsignificantly, gs tended to be greater for Q. saponaria (0.250 mol CO2 m−2 s−1) compared to C. alba (0.227 mol CO2 m−2 s−1) and L. caustica (0.221 mol CO2 m−2 s−1). The ratio gm/gs was on average 0.47 ± 0.08, independent of species (Table 1). Relative limitations posed by mesophyll conductance to photosynthesis, Lm, (0.40 ± 0.02) were high compared to those imposed by stomata, Ls (0.07 ± 0.01) and not significantly influenced by species. The average CO2 concentration in the intercellular air spaces (Ci) was 31.7 μmol mol−1 lower than in the atmosphere (Ca), while the average CO2 concentration in the chloroplasts (Cc) was 130.6 μmol mol−1 lower than in Ci , independent of the species (Table 1).
The gm values found in this study were generally lower than those reported for other plant functional groups. Flexas et al. () argues that gm is associated with leaf forms and plant functional groups, rather than evolutive trends: herbaceous plants exhibit generally the largest gm values (~0.4 mol CO2 m−2 s−1 bar−1), perennial herbs and woody deciduous angiosperms display intermediate values (~0.2 mol CO2 m−2 s−1 bar−1), while woody evergreen plants exhibit gm values slightly above and below 0.1 mol CO2 m−2 s−1 bar−1 in angiosperms and gymnosperms, respectively. The mean value across all angiosperm sclerophyllous species studied was 0.073 mol CO2 m−2 s−1 bar−1, similar to those found by Niinemets et al. ([2009b]) for Australian sclerophyllous species (0.087 mol CO2 m−2 s−1 bar−1).
There seems to be a consistent pattern for sclerophyllous species to exhibit both low gm and low gm/gs values (Gulias et al. ; Niinemets et al. [2009b]; Tomas et al. ; Warren ). Consequently, differences between Ca and Ci are relatively small compared to the difference between Ci and Cc. This drawdown of CO2 implies that relative limitations imposed by mesophyll conductance to photosynthesis are much greater than those posed by stomata. Warren () found that mesophyll limitations (Lm ~ 0.19 to 0.38) were greater than stomatal limitations (Ls ~ 0.05 to 0.23) for Eucalyptus globulus which are similar to our study. Equivalent mesophyll conductance limitations were observed for other sclerophyllous species (Lm ~ 0.20-0.50) by Niinemets et al. ([2009b]). This seems to be explained by leaf anatomical traits such as thickness, density and the leaf mass to area ratio (Flexas et al. ; Niinemets et al. [2009b]; Tomas et al. ) and also by tissue and cell anatomical traits, such as chloroplast surface area exposed to the intercellular air spaces, cell wall thickness and palisade tissue path length, among others (Tomas et al. ; Flexas et al. ; Tosens et al. ; Terashima et al. ; Hassiotou et al. ).
C.albaThere are only a few studies on leaf anatomical traits for the sclerophyllous species considered in this study. Q. saponaria generally exhibits lower density palisade parenchyma and spongy mesophyll compared to C. alba and L. caustica (Gotor ); and additionally L. caustica exhibits substantially thicker cell walls compared to the other sclerophyllous species (Montenegro ). We also found L.caustica leaves to be thicker and denser, as shown by its lower foliage area to mass ratio (M) (7.0 m2 kg−1), compared to Q. saponaria (8.7 m2 kg−1) and C. alba (10 m2 kg−1). Tomas et al. () found that for sclerophyllous species gm was strongly constrained by cell wall thickness (e.g. L. caustica). Such differences in leaf, tissue and cell anatomical traits may at least partially explain why values of gm and photosynthetic rates are in the series: Q. saponaria > C. alba ≥ L. caustica.
The ‘constant J method’ used to estimate gm is sensitive to errors in both the rate of mitochondrial respiration in the light, Rd*, and the chloroplastic CO2 compensation concentration in the absence of mitochondrial respiration, Γ*. Values of Γ* in our study were very similar across sclerophyllous species (F2,41 = 0.26, P = 0.78), with a mean value of 50.7 μmol mol−1 (Table 1). In contrast, Rd*, was significantly lower (F2,41 = 9.87, P < 0.001) in L. caustica (1.0 μmol CO2 m−2 s−1) compared to C. alba (1.7 μmol CO2 m−2 s−1) and Q. saponaria (1.5 μmol CO2 m−2 s−1) (Table 1).
A recent paper by Gu and Sun () suggests that the so-called Laisk method to estimate Γ* and Rd* seems to be invalid, and hence an alternative estimate for gm in our study would reduce the uncertainty related to our results. We tested whether our results for gm withhold when using values found in the literature for Γ* and Rd*. We used values for tobacco from Brooks and Farquhar () (Set 1: Rd = 0.8 μmol m−2 s−1, Γ* = 36.9 μmol mol−1) and for spinach from Bernacchi et al. () (Set 2: Rd = 1 μmol m−2 s−1, Γ* = 42.8 μmol mol−1), which have been commonly used to calculate gm for evergreen species (Gallé et al. ; Hassiotou et al. ; Niinemets et al. [2009a]; Niinemets et al. [2009b]). We did not find significant differences within each species when comparing the three estimates of gm i.e. using our estimates using the Laisk method, Set 1 and Set 2 (Q. saponaria: P = 0.48, C. alba: P = 0.38, L. caustica: P = 0.12). Tomas et al. ([2013a], [b]) performed a similar analysis for deciduous, semideciduous and evergreen trees and herbs plants, obtaining similar values of gm independent of the values chosen for Γ*y Rd*. This shows that our results hold independent of having used the Laisk method to estimate Γ*y Rd*.
Biochemical limitations to photosynthesis
Values of Vcmax (range 13–66, mean 36 μmol m−2 s−1) and Jmax (range 33–148, mean 82 μmol m−2 s−1) in our study were within the range compiled for 109 C3 plant species by Wullschleger () (Vcmax: range 6–194, mean 64 μmol m−2 s−1; Jmax: range 17–372, mean 134 μmol m−2 s−1). Wullschleger () also provided specific values of Vcmax (range 11–119, mean 47 μmol m−2 s−1) and Jmax (range 29–237, mean 104 μmol m−2 s−1) for temperate hardwoods and sclerophyllous species (Vcmax: range 35–71, mean 53 μmol m−2 s−1; Jmax: range 94–167, mean 122 μmol m−2 s−1); which are similar to the ones found in our study. Pena-Rojas et al. () observed values of 29 μmol CO2 m−2 s−1 and 59 μmol electrons m−2 s−1 for Vcmax and Jmax, respectively for Quercus ilex. Niinemets et al. ([2009b]) observed values of 37 μmol CO2 m−2 s−1 and 89 μmol electrons m−2 s−1 for Vcmax and Jmax, respectively for different Australian sclerophyllous species. This emphasizes the fact that photosynthetic capacity in our study was more limited by gm than by biochemical limitations, as our values of Vcmax and Jmax were greater than those reported by Pena-Rojas et al. () and Niinemets et al. ([2009b]) and comparable to averages for C3 hardwoods.
The maximal rate of Rubisco carboxylation (Vcmax) calculated on a Ci basis, were significantly greater in Q. saponaria (49.0 μmol CO2 m−2 s−1) compared to C. alba (32.6 μmol CO2 m−2 s−1) and L. caustica (26.8 μmol CO2 m−2 s−1) (Table 1). Corresponding values of Vcmax on a Cc basis were 98.3, 64.4 and 45.5 μmol CO2 m−2 s−1, respectively. Therefore, values of Vcmax calculated on a Cc basis were 101%, 97% and 70% greater than those on a Ci basis for Q. saponaria, C. alba and L. caustica, respectively.
Similar to Vcmax, the maximal rate of electron transport driving regeneration of RuBP (Jmax) calculated on a Ci basis, were significantly greater in Q. saponaria (111.4 μmol electrons m−2 s−1) compared to C. alba (79.6 μmol electrons m−2 s−1) and L. caustica (56.3 μmol electrons m−2 s−1) (Table 1). Corresponding values of Jmax on a Cc basis were 126.4, 89.9 and 60.4 μmol electrons m−2 s−1, respectively. Therefore, values of Jmax were 13%, 13% and 7% greater on a Cc than a Ci basis for Q. saponaria, C. alba and L. caustica, respectively.
Most values of Vcmax and Jmax reported in the literature are calculated from A/Ci response curves, rather than A/Cc curves, with the implicit assumption that mesophyll conductance is infinitely large. When this assumption is invalid, values of Vcmax and Jmax are underestimated (Ethier and Livingston ; Ethier et al. ; Grassi and Magnani ; Harley et al. ; Long and Bernacchi ; Loreto et al. ; Manter and Kerrigan ; von Caemmerer ; Niinemets et al. [2009a]). To prove this assumption Grassi and Magnani () showed that the relationship between Vcmax,ci and Vcmax,cc values result in a slope of 1.62 (r2 = 0.94), showing that the Ci calculation underestimated the real photosynthetic capacity of the leaf. This relation is similar to the one found in our study, which resulted in a slope of 1.28 (r2 = 0.76).
There is mounting evidence that gm changes with chloroplastic CO2 concentration and irradiance, although some of that variation can be an artifact due to the mathematical methods employed (Gu and Sun ). Also Tholen et al. () suggests there are limitations in the precise estimate of gm when taking several A values from varying CO2 concentrations and rates of photorespiration to estimate gm. Taking aside artefactual responses, it seems that gm initially increases, then peaks to decline thereafter with increasing Cc; while gm seems to increase with irradiance for the same level of Cc (Flexas et al. ). We are aware that converting A/Ci into A/Cc curves assuming a constant gm can be invalid; but still useful for comparing our results with previous studies. For instance, the parameters and results found in our study were similar for the photosynthesis model stated by Farquhar et al. () with model parameters in normal scenarios of Vcmax ~ 50 μmol CO2 m−2 s−1, Jmax ~ 125 μmol electrons m−2 s−1, and dark respiration rates ~ 1.25 μmol CO2 m−2 s−1. These values were approximate to an ‘average’ C3 leaf based on Cc-derived estimates and in the range of the results for the three sclerophyllous species of our study; therefore emphasizing that our species were more limited by gm that biochemical parameters. We are also aware that using ‘standard’ Rubisco kinetics from tobacco to calculate gm, Vcmax and Jmax may lead to biases (Walker et al. ) to parameterize photosynthesis in the sclerophyllous species considered in this study. This emphasizes the need for future work to estimate Rubisco kinetics for sclerophyllous species in central Chile.
Foliar nitrogen and photosynthetic parameters
Photosynthetic rates are known to be closely related to foliar nitrogen concentrations (Field and Mooney ; Walcroft et al. ; Grassi et al. ; Ripullone et al. ). This is explained by the high proportion of total nitrogen partitioned to the carboxylating enzyme Rubisco (Sage and Pearcy ; Evans ; Warren and Adams ; Takashima et al. ) and also by the strong coupling effect among capacities Vcmax and Jmax (von Caemmerer and Farquhar ; Wullschleger ; Sharkey ).
At the plant level, observed Na ranged almost sixfold from 54 to 339 mmol N m−2 being significantly greater in C. alba (195.5 mmol m−2) compared to Q. saponaria (165.8 mmol m−2) and L. caustica (120.2 mmol m−2) (Table 1). Values of gm were uncorrelated to Na (r2 = 0.001, P = 0.40); but as expected values of Vcmax and Jmax on a Ci basis significantly increased with Na (F1,38 > 5.95, P < 0.019). Intercepts (F2,38 > 31.3, P < 0.001) but not slopes (F2,38 < 1.42, P > 0.25) of the Vcmax/Na and Jmax/Na linear relationships were significantly different between species (Vcmax = a + 0.075 Na, with a = 17.728 for L. caustica, a = 32.489 for C. alba, a = 39.204 for Q. saponaria, r2 = 0.61, P < 0.001; Jmax = a + 0.149 Na, with a = 38.349 for L. caustica, a = 85.976 for C. alba, a = 101.296 for Q. saponaria, r2 = 0.62, P < 0.001). It is worth noting that L.caustica exhibited the lowest intercept followed by C. alba and Q. saponaria consistently for both the Vcmax/Na and the Jmax/Na relationships which can be attributed to reasons other than foliage N (i.e. foliage N was accounted for in the slope of these relationships). We then may speculate that intercept differences among species can be attributed to distinct leaf N investment strategies. Consistently we found significant differences in Nitrogen use efficiency (En), being greatest in Q. saponaria (95.9 μmol CO2 mol N s−1), compared to L. caustica (69.8 μmol CO2 mol N s−1) and C. alba (56.4 μmol CO2 mol N s−1) (Table 1). Such differences in En, may suggest that Q. saponaria, that exhibits a greater photosynthetic capacity, may invest proportionally more N to Rubisco compared to L. caustica and C. alba that exhibit poorer photosynthetic performance.
In conclusion, values of stomatal conductance, gs, were greater than those of mesophyll conductance, gm, while their ratio (gm/gs) was not influenced by species, being on average 0.47. Therefore, the relative limitations imposed by gm were high (Lm ~ 0.40, Ci-Cc ~ 131 μmol mol−1) compared to those imposed by gs (Ls ~ 0.07, Ca-Ci ~ 32 μmol mol−1). Consequently photosynthetic rates in our study were mainly limited by gm as biochemical limitations Vcmax and Jmax compare well to averages for C3 plants. Photosynthetic performance was in the series: Q. saponaria > C. alba ≥ L. caustica which can be attributed first to mesophyll conductance limitations, probably mediated by leaf anatomical traits and then to species specific foliage N partitioning strategies.
light-saturated rate of photosynthesis at ambient Ca
μmol m−2 s−1
respiration rate at zero irradiance
μmol m−2 s−1
Light saturation point determined as the Q value for which assimilation is 90% of Asat
μmol m−2 s−1
Light compensation point determined as the Q value for which the rate of photosynthesis exactly matches the rate of respiration
μmol m−2 s−1
apparent maximum quantum efficiency
CO2 concentration in the air outside the leaf
CO2 concentration in intercellular air spaces
CO2 concentration in the chloroplast
chloroplastic CO2 compensation point
C i *
intercellular CO2 compensation point in the absence of day respiration
R d *
rate of mitochondrial respiration in the light
μmol m−2 s−1
instantaneous photosynthetic nitrogen use efficiency
μmol mol−1 s−1
relative stomatal (plus boundary layer) limitation to photosynthesis
relative mesophyll limitations to photosynthesis
stomatal (plus boundary layer) conductance to CO2 diffusion
mol m−2 s−1
Mesophyll transfer conductance to CO2 diffusion
mol m−2 s−1 bar−1
in vivo maximum rate of ribulose-1,5-bis phosphate (RuBP) carboxylase-oxygenase (Rubisco) carboxylation
μmol CO2 m−2 s−1
electron transport driving regeneration of RuBP
μmol electrons m−2 s−1
the rate of photosynthesis near saturating Ci (800 μmol mol−1)
μmol CO2 m−2 s−1
foliage nitrogen concentration on an area basis
Leaf area to mass ratio
Leaf-to-air vapour pressure deficit
During this work the corresponding author was supported by the National Science and Technology Commission (CONICYT) through the project FONDECYT 1090259 “Disturbance mediated water and nutrient stresses regulate carbon assimilation and allocation in sclerophyll ecosystems in Central Chile: A process-based approach”. We thank Corporación Nacional Forestal for their support to carry out FONDECYT 1090259, and for providing accommodation and technical advice within the National Reserve “Roblería de los Cobres de Loncha”. We also thank Mrs. Cristina Sáez N. (Universidad de Chile), Mr. Roberto Cerda R. (CONAF) and Mr. Eric Campos (Universidad de Chile) for their kind advice and valuable technical skills. The experiments and measurements undertaken for this paper comply with the current laws of Chile.
- Armesto JJ, Arroyo MTK, Hinojosa LF: The mediterranean environment of Central Chile. In The physical geography of South America: 184–199. Edited by: Veblen TT, Young KR, Orme AR. Oxford University Press, United State of America; 2007.Google Scholar
- Arroyo MTK, Marquet P, Marticorena C, Simonetti J, Cavieres LA, Squeo FA, Rozzi R: Chilean winter rainfall - Valdivian forests. In Hotspots revisited: earth’s biologically richest and most endangered terrestrial ecoregions: 99–103. Edited by: Mittermeier PRRA, Hoffmann M, Pilgrim J, Brooks T, Goettsch-Mittermeier C, Lamoreux J, Fonseca GAB. CEMEX, Mexico; 2004.Google Scholar
- Baldocchi DD, Harley PC: Scaling carbon dioxide and water vapour exchange from leaf to canopy in a deciduous forest: II model testing and application. Plant Cell and Environment 1995, 18: 1157–1173. 10.1111/j.1365-3040.1995.tb00626.xView ArticleGoogle Scholar
- Benites J, Saintraint D, Morimoto YK: Degradación de tierras y producción agrícola en Argentina, Bolivia, Brasil, Chile y Paraguay: Erosión de Suelos en América Latina. Oficina Regional de la FAO para América Latina y el Caribe, Santiago; 1994.Google Scholar
- Bernacchi CJ, Elsingsaas CP, Portis AR, Long SP: Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 2001, 24: 253–259. 10.1111/j.1365-3040.2001.00668.xView ArticleGoogle Scholar
- Bernacchi CJ, Portis AR, Nakano H, Von Caemmerer S, Long SP: Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiology 2002, 130: 1992–1998. 10.1104/pp.008250PubMed CentralView ArticlePubMedGoogle Scholar
- Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1, 5- bisphosphate carboxylase oxygenase and the rate of respiration in the light: estimates from gas-exchange measurements on spinach. Planta 165:397–406View ArticlePubMedGoogle Scholar
- Cabrera M: Respuestas ecofisiológicas de plantas en ecosistemas de zonas con clima mediterráneo y ambientes de alta montaña. Rev Chil Hist Nat 2002, 75: 625–637. 10.4067/S0716-078X2002000300013View ArticleGoogle Scholar
- CONAF: Catastro y Evaluación de Recursos Vegetacionales Nativos de Chile. Proyecto CONAF-CONAMA-BIRF, Santiago, Chile; 1999.Google Scholar
- De Lucia EH, Whitehead D, Clearwater MJ: The relative limitation of photosynthesis by mesophyll conductance in co-occurring species in a temperate rainforest dominated by the conifer Dacrydium cupressinum . Funct Plant Biol 2003, 30: 1197–1204. 10.1071/FP03141View ArticleGoogle Scholar
- Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant, Cell and Environment 27:137–153View ArticleGoogle Scholar
- Ethier GJ, Livingston NJ, Harrison DL, Black TA, Moran JA (2006) Low stomatal and internal conductance to CO2 versus Rubisco deactivation as determinants of the photosynthetic decline of ageing evergreen leaves. Plant, Cell andEnvironment 29:2168–2184View ArticleGoogle Scholar
- Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19View ArticleGoogle Scholar
- Farquhar GD, Sharkey TD: Stomatal conductance and photosynthesis. Annual Review of Plant Physiology. 1982, 33: 317–345. 10.1146/annurev.pp.33.060182.001533View ArticleGoogle Scholar
- Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90View ArticlePubMedGoogle Scholar
- Field C, Mooney HA: The photosynthesis - nitrogen relationship in wild plants. In The economy of plant form and function. Edited by: Givnish TJ. Cambridge University Press, Cambridge; 1986:25–55.Google Scholar
- Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD: Diffusive and metabolic limitations to photosynthesis under drought and salinity in C (3) plants. Plant Biol 2004, 6: 269–279. 10.1055/s-2004-820867View ArticlePubMedGoogle Scholar
- Flexas J, Díaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M: Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant, Cell and Environment 2007, 30: 1284–1298. 10.1111/j.1365-3040.2007.01700.xView ArticlePubMedGoogle Scholar
- Flexas J, Ribas-Carbo M, Diaz-Espejo A, Galmes J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621View ArticlePubMedGoogle Scholar
- Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriqui M, Diaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Galle A, Galmes J, Kodama N, Medrano H, Niinemets U, Peguero-Pina JJ, Pou A, Ribas-Carbo M, Tomas M, Tosens T, Warren CR: Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Science 2012, 193: 70–84. doi:10.1016/j.plantsci.2012.05.009 10.1016/j.plantsci.2012.05.009View ArticlePubMedGoogle Scholar
- Gallé A, Flórez-Sarasa I, Aououad HE, Flexas J: The Mediterranean evergreen Quercus ilex and the semi-deciduous Cistus albidus differ in their leaf gas exchange regulation and acclimation to repeated drought and re-watering cycles. J Exp Bot 2011, 62: 5207–5216. 10.1093/jxb/err233PubMed CentralView ArticlePubMedGoogle Scholar
- Galmes J, Medrano H, Flexas J: Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 2007, 175: 81–93. 10.1111/j.1469-8137.2007.02087.xView ArticlePubMedGoogle Scholar
- Genty B, Briantais JM, Baker NR: The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochimica Et Biophysica Acta 1989, 990: 87–92. 10.1016/S0304-4165(89)80016-9View ArticleGoogle Scholar
- Gotor B: Evaluación de parámetros fisiológicos y de Crecimiento en plantas de Quillaja saponaria Mol. bajo condiciones de déficit hídrico: Memoria para optar al título de Ingeniero Forestal. Facultad de Ciencias Forestales, Universidad de Chile, Santiago, Chile; 2008.Google Scholar
- Grassi G, Magnani F: Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell Environ 2005, 28: 834–849. 10.1111/j.1365-3040.2005.01333.xView ArticleGoogle Scholar
- Grassi G, Meier P, Cromer R, Tompkins D, Jarvis PG: Photosynthetic parameters in seedlings of Eucalyptus grandis as affected by rate of nitrogen supply. Plant Cell Environ 2002, 25: 1677–1688. 10.1046/j.1365-3040.2002.00946.xView ArticleGoogle Scholar
- Griffin KL, Tissue DT, Turnbull MH, Whitehead D (2000) The onset of photosynthetic acclimation to elevated CO2 partial pressure in field-grown Pinus radiata D: Don. after 4 years. Plant Cell Environ 23:1089–1098View ArticleGoogle Scholar
- Gu L, Sun Y: Artefactual responses of mesophyll conductance to CO2 and irradiance estimated with the variable J and online isotope discrimination methods. Plant, Cell and Environment 2014, 37: 1231–1249. 10.1111/pce.12232View ArticlePubMedGoogle Scholar
- Gulias J, Flexas J, Abadia A, Medrano H: Photosynthetic responses to water deficit in six Mediterranean sclerophyll species: possible factors explaining the declining distribution of Rhamnus ludovici-salvatoris , an endemic Balearic species. Tree Physiol 2002, 22: 687–697. 10.1093/treephys/22.10.687View ArticlePubMedGoogle Scholar
- Harley PC, Sharkey TD (1991) An improved model of C3 photosynthesis at high CO2 - reversed O2 sensitivity explained by lack of glycerate reentry into the chloroplast. Photosynth Res 27(3):169–178PubMedGoogle Scholar
- Harley PC, Loreto F, Di Marco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436PubMed CentralView ArticlePubMedGoogle Scholar
- Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009) Influence of leaf dry mass per area, CO2 and irradiance on mesophyll conductance in sclerophylls. J Exp Bot 60:2303–2314View ArticlePubMedGoogle Scholar
- Hogan KP, Whitehead D, Kallarackal J, Buwalda JG, Meekings J, Rogers GND (1996) Photosynthetic activity of leaves of Pinus radiata and Nothofagus fusca after 1 year of growth at elevated CO2. Aust J Plant Physiol 23(5):623–630View ArticleGoogle Scholar
- Jones HG: Plants and microclimate: a quantitative approach to environmental physiology. Cambridge University Press, Cambridge, UK; 1992.Google Scholar
- Kellomaki S, Wang KY (1996) Photosynthetic responses to needle water potentials in Scots pine after a four-year exposure to elevated CO2 and temperature. Tree Physiol 16:765–772View ArticlePubMedGoogle Scholar
- Long SP, Bernacchi CJ: Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? procedures and sources of error. J Exp Bot 2003, 54: 2393–2401. 10.1093/jxb/erg262View ArticlePubMedGoogle Scholar
- Loreto F, Harley PC, Di Marco G, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by three different methods. Plant Physiol 98:1437–1443PubMed CentralView ArticlePubMedGoogle Scholar
- Manter DK, Kerrigan J: A/C-i curve analysis across a range of woody plant species: influence of regression analysis parameters and mesophyll conductance. J Exp Bot 2004, 55: 2581–2588. 10.1093/jxb/erh260View ArticlePubMedGoogle Scholar
- Mcmurtrie RE, Leuning R, Thomson WA, Wheeler AM (1992) A model of canopy photosynthesis and water use incorporating a mechanistic formulation of leaf CO2 exchange. For Ecol Manag 52:261–278View ArticleGoogle Scholar
- Montenegro G: Atlas de anatomía de especies vegetales autóctonas de la Zona Central. Ediciones Universidad Católica de Chile, Santiago; 1984.Google Scholar
- Murray MB, Smith RI, Friend A, Jarvis PG (2000) Effect of elevated CO2 and varying nutrient application rates on physiology and biomass accumulation of Sitka spruce (Picea sitchensis). Tree Physiol 20:421–434View ArticlePubMedGoogle Scholar
- Niinemets Ü, Díaz A, Flexas J, Galmés J, Warren R: Importance of mesophyll diffusion conductance in estimation of plant photosynthesis in the field. J Exp Bot 2009, 60: 2271–2282. 10.1093/jxb/erp063View ArticlePubMedGoogle Scholar
- Niinemets Ü, Wright I, Evans J: Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation. Journal Experimental Botany 2009, 60: 24333–22449.Google Scholar
- Peisker M, Apel H (2001) Inhibition by light of CO2 evolution from dark respiration: comparison of two gas exchange methods. Photosynth Res 70:291–298View ArticlePubMedGoogle Scholar
- Pena-Rojas K, Aranda X, Fleck I (2004) Stomatal limitation to CO2 assimilation and down-regulation of photosynthesis in Quercus ilex resprouts in response to slowly imposed drought. Tree Physiol 24(7):813–822, Schreiber U, W Bilger & C Neubauer (1994) Chrorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: ED Schulze & MM Caldwell (eds) Ecophysiology of photosynthesis: 49–70. Springer Verlag, BerlinView ArticlePubMedGoogle Scholar
- Pons TL, Flexas J, von Caemmerer S, Evans JR, Genty B, Ribas-Carbo M, Brugnoli E (2009) Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations. J Exp Bot 60:2217–2234View ArticlePubMedGoogle Scholar
- Prioul JL, Chartier P (1977) Partitioning of transfer and carboxylation components of intracellular resistance to photosynthetic CO2 fixation: a critical analysis of the methods used. Ann Bot 4:789–800Google Scholar
- R Core Team: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2013.Google Scholar
- Ripullone F, Grassi G, Lauteri M, Borghetti M: Photosynthesis-nitrogen relationships: interpretation of different patterns between Pseudotsuga menziesii and Populus euroamericana in a mini-stand experiment. Tree Physiol 2003, 23: 137–144. 10.1093/treephys/23.2.137View ArticlePubMedGoogle Scholar
- Sage RF, Pearcy RW (1987) The nitrogen use efficiency of C3 and C4 plants. Plant Physiol 84:959–963PubMed CentralView ArticlePubMedGoogle Scholar
- Schreiber U, Bilger W, Neubauer C: Chrorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In Ecophysiology of photosynthesis: 49–70. Edited by: Schulze ED, Caldwell MM. Springer Verlag, Berlin; 1994.Google Scholar
- Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Rev 51:54–105View ArticleGoogle Scholar
- Singsaas EL, Ort DR, Delucia EH (2004) Elevated CO2 effects on mesophyll conductance and its consequences for interpreting photosynthetic physiology. Plant Cell Environ 27:41–50View ArticleGoogle Scholar
- Takashima T, Hikosaka K, Hirose T: Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 2004, 27: 1047–1054. 10.1111/j.1365-3040.2004.01209.xView ArticleGoogle Scholar
- Terashima I, Hanba YT, Tholen D, Niinemets Ü: Leaf functional anatomy in relation to photosynthesis. Plant Physiol 2011, 155: 108–116. 10.1104/pp.110.165472PubMed CentralView ArticlePubMedGoogle Scholar
- Tholen D, Ethier G, Genty B, Pepin S, Zhu XG: Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ 2012, 35: 2087–2103. 10.1111/j.1365-3040.2012.02538.xView ArticlePubMedGoogle Scholar
- Tomas M, Flexas J, Copolovici L, Galmes J, Hallik L, Medrano H, Ribas-Carbo M, Tosens T, Vislap V, Niinemets U: Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. Journal of Experimental Botany 2013,64(8):2269–2281. doi:10.1093/jxb/ert086 10.1093/jxb/ert086PubMed CentralView ArticlePubMedGoogle Scholar
- Tosens T, Niinemets Ü, Westoby M, Wright IJ: Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path. J Exp Bot 2012, 63: 5105–5119. 10.1093/jxb/ers171PubMed CentralView ArticlePubMedGoogle Scholar
- Turnbull MH, Tissue DT, Griffin KL, Rogers GND, Whitehead D (1998) Photosynthetic acclimation to long-term exposure to elevated CO2 concentration in Pinus radiata D: Don. is related to age of needles. Plant Cell Environ 21:1019–1028View ArticleGoogle Scholar
- Turnbull MH, Murthy R, Griffin KL: The relative impacts of daytime and night-time warming on photosynthetic capacity in Populus deltoides . Plant, Cell and Environment 2002, 25: 1729–1737. 10.1046/j.1365-3040.2002.00947.xView ArticleGoogle Scholar
- von Caemmerer S: Biochemical models of leaf photosynthesis. Victoria, Australia, CSIRO Publishing, Collingwood; 2000.Google Scholar
- von Caemmerer S, Evans JR (1991) Determination of the average partial pressure of CO2 in chloroplasts from leaves of several C3 plants. Aust J Plant Physiol 18:287–305View ArticleGoogle Scholar
- von Caemmerer S, Farquhar GD: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 1981, 153: 376–387. 10.1007/BF00384257View ArticlePubMedGoogle Scholar
- Walcroft AS, Whitehead D, Silvester WB, Kelliher FM: The response of photosynthetic model parameters to temperature and nitrogen concentration in Pinus radiata D. Don Plant, Cell & Environment 1997, 20: 1338–1348. 10.1046/j.1365-3040.1997.d01-31.xView ArticleGoogle Scholar
- Walker B, Ariza LS, Kaines S, Badger MR, Cousins AB: Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana : comparisons to Nicotiana tabacum . Plant Cell Environ 2013, 36: 2108–2119. 10.1111/pce.12166View ArticlePubMedGoogle Scholar
- Warren CR (2004) The photosynthetic limitation posed by internal conductance to CO2 movement is increased by nutrient supply. J Exp Bot 55:2313–2321View ArticlePubMedGoogle Scholar
- Warren CR: Why does photosynthesis decrease with needle age in Pinus pinaster ? Trees 2006, 20: 157–164. 10.1007/s00468-005-0021-7View ArticleGoogle Scholar
- Warren CR, Adams MA: Phosphorus affects growth and partitioning of nitrogen to Rubisco in Pinus pinaster . Tree Physiol 2002, 22: 11–19. 10.1093/treephys/22.1.11View ArticlePubMedGoogle Scholar
- Warren CR, Adams MA: Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant Cell Environ 2006, 29: 192–201. 10.1111/j.1365-3040.2005.01412.xView ArticlePubMedGoogle Scholar
- Warren CR, Ethier GJ, Livingston NJ, Grant NJ, Turpin DH, Harrison DL, Black TA: Transfer conductance in second growth Douglas-fir ( Pseudotsuga menziesii (Mirb.)Franco) canopies. Plant Cell Environ 2003, 26: 1215–1227. 10.1046/j.1365-3040.2003.01044.xView ArticleGoogle Scholar
- Whitehead D, Walcroft AS, Griffin KL, Tissue DT, Turnbull MH, Engel VC, Brown KJ, Schuster WSF: Scaling carbon uptake from leaves to canopies: insights from two forests with contrasting properties.In Forests at the land-atmosphere interface: 231–254 Edited by: Mencuccini JGM, Moncrieff J, McNaughton KG. CAB International, U.K. CABI; 2004. [http://arrow.uws.edu.au:8080/vital/access/manager/Repository/uws:2660] http://arrow.uws.edu.au:8080/vital/access/manager/Repository/uws:2660Google Scholar
- Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants - a retrospective analysis of the A/Ci curves from 109 species. J Exp Bot 44:907–920View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.