Journal of Experimental Botany, Vol. 53, No. 379, pp. 2423-2430,
December 1, 2002
© 2002 Oxford University Press
Effect of local irradiance on CO2 transfer conductance of mesophyll in walnut
Received 4 March 2002; Accepted 12 July 2002
1 Laboratoire d’Ecophysiologie Végétale, UPRESA 8079 CNRS-Université Paris Sud, F-91405 Orsay, France
2 UMR-PIAF Integrated Tree Physiology (INRA-University Blaise Pascal), 234 avenue du Brézet, F-63039 Clermont-Ferrand Cedex 02, France
3 Present address and to whom correspondence should be sent: Laboratoire d’Ecophysiologie de la Photosynthèse, UMR 163 CNRS-CEA, DEVM, CEA Cadarache, F-13108 St Paul lez Durance, France. Fax: +33 4 42 25 62 65. E-mail: bernard.genty{at}cea.fr
4 Present address: Laboratoire d’Ecophysiologie de la Photosynthèse, UMR 163 CNRS-CEA, DEVM, CEA Cadarache, F-13108 St Paul lez Durance, France.
5 Present address: Laboratoire d’Ecologie Microbienne, UMR 5557 CNRS-Université Lyon I, bat 741, 43 bd du 11 novembre 1918, F-69622 Villeurbanne, France.
Abbreviations: An, Anmax, net assimilation rate, and maximal net assimilation rate, respectively; Ca, Ces, Cc, CO2 mole fraction in ambient air, at evaporating surfaces within the leaf and at the carboxylation sites of Rubisco, respectively; fias, volume fraction of intercellular air spaces within the leaf; gi, mesophyll conductance to CO2 transfer; gias, conductance to CO2 transfer in the mesophyll intercellular air spaces; gscmax, maximal stomatal conductance to CO2 transfer; J, Jmax, rate of electron transport, and maximal rate of electron transport, respectively; LMA, leaf mass per area; Na, leaf nitrogen content; PPFD, photosynthetic photon flux density; Rlight, Robs: leaf respiration rate in the light, and in the dark, respectively; Rubisco, ribulose-1,5-bisphosphate carboxylase-oxygenase; Vcmax, maximal rate of carboxylation; 
*, CO2 compensation point in the absence of mitochondrial respiration; 
, mean effective pathlength for CO2 transfer from the substomatal cavity to the uppermost mesophyll surface.
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
The acclimation responses of walnut leaf photosynthesis to the irradiance microclimate were investigated by characterizing the photosynthetic properties of the leaves sampled on young trees (Juglans nigraxregia) grown in simulated sun and shade environments, and within a mature walnut tree crown (Juglans regia) in the field. In the young trees, the CO2 compensation point in the absence of mitochondrial respiration (
*), which probes the CO2 versus O2 specificity of Rubisco, was not significantly different in sun and shade leaves. The maximal net assimilation rates and stomatal and mesophyll conductances to CO2 transfer were markedly lower in shade than in sun leaves. Dark respiration rates were also lower in shade leaves. However, the percentage inhibition of respiration by light during photosynthesis was similar in both sun and shade leaves. The extent of the changes in photosynthetic capacity and mesophyll conductance between sun and shade leaves under simulated conditions was similar to that observed between sun and shade leaves collected within the mature tree crown. Moreover, mesophyll conductance was strongly correlated with maximal net assimilation and the relationships were not significantly different between the two experiments, despite marked differences in leaf anatomy. These results suggest that photosynthetic capacity is a valuable parameter for modelling within-canopies variations of mesophyll conductance due to leaf acclimation to light. Key words: Leaf anatomy, light acclimation, mesophyll conductance, photosynthetic capacity, Rubisco specificity, walnut.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Leaf anatomy and photosynthetic characteristics generally vary in response to the heterogeneous light regime encountered within canopies and individual tree crowns (see Boardman, 1977, for a review). Tree leaves grown in a shade environment exhibit modified shape, changes in the organization of mesophyll cells together with changes in biochemical and photosynthetic characteristics (Boardman, 1977; Chazdon and Kaufmann, 1993). Lower leaf area, leaf thickness, and leaf mass per area together with lower amounts of nitrogen and Rubisco per leaf area, lower photosynthetic capacity on a leaf area basis, and lower stomatal conductance have commonly been reported in shade leaves as compared with leaves grown in high light environments (Boardman, 1977; Kappel and Flore, 1983; Anten et al., 1996; Niinemets and Tenhunen, 1997; Le Roux et al., 1999a, b, 2001a).
Because CO2 diffusion inside the mesophyll depends on leaf anatomy and mesophyll organization (Rand, 1978; Nobel, 1991; Parkhurst, 1994), the conductance for CO2 transfer between the substomatal cavities and the Rubisco carboxylation sites, the so-called mesophyll conductance, is also expected to vary in response to the irradiance gradient within the foliage. However, the variation of mesophyll conductance in response to irradiance has been poorly documented (see Evans and Loreto, 2000, for a recent review). Most studies on mesophyll conductance have focused on interspecific comparisons and various compilations of data have shown that it was positively correlated with photosynthetic capacity, and was in the same order of magnitude as stomatal conductance (Evans and Loreto, 2000). These studies have also revealed that many ligneous species have lower mesophyll conductance than herbaceous species (Evans and Loreto, 2000). Fewer studies have documented the intraspecific variability in mesophyll conductance. Mesophyll conductance has been shown to respond to growth irradiance (Lloyd et al., 1992; Evans et al., 1994), leaf age (Loreto et al., 1994; Scartazza et al., 1998; Miyazawa and Terashima, 2001), drought (Lauteri et al., 1997), and salinity stress (Delfine et al., 1998, 1999). In the single set of data available on the irradiance effect on mesophyll conductance in ligneous species (Lloyd et al., 1992), the leaf anatomy of young Prunus persica (peach) and Citrus paradisi (grapefruit) was only slightly responsive to shading during growth, and mesophyll conductance slightly decreased (by approximately 20–25%). Data are still missing on tree species showing extensive leaf acclimation to light.
The objectives of the present work were (1) to investigate the variability of leaf photosynthetic and anatomical traits in response to local irradiance using walnut trees, with particular interest on mesophyll conductance, and (2) to identify an easily accessible leaf trait for parametrizing the variations in mesophyll conductance. Walnut leaves exhibit large anatomical and photosynthetic modifications in response to local irradiance within individual tree crowns in the field (Le Roux et al., 1999a, b). In the present study, differences between shade and sun leaves were investigated using two contrasted sun and shade light environments applied to the foliage of potted walnut trees grown outdoors. The results were compared to data obtained on sun and shade leaves sampled within a mature walnut crown growing in the field.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Plant material
Three-year-old trees: The study was carried out during July 1999 using 3-year-old hybrid walnut trees (Juglans nigraxregia) in the INRA experimental site in Clermont-Ferrand (France). Trees were grown outdoors in 35 dm3 pots filled with a soil–peat mixture (1/2 v/v), and watered once or twice a day according to evaporative demand. A few days after bud burst, one branch was placed in a tunnel made with altuglass screens. Two types of screen that mimicked high light and deep shade conditions were used. For high light, neutral screen transmitted 90±0.5% of incident radiation without significant modification of the spectrum (red/far red=1.25±0.01) as measured in five locations under each screen with a spectroradiometer (LI-1800, Li-Cor Inc., Lincoln, NE, USA). For shade, green screen transmitted 10±1% of incident radiation (red/far red=0.22±0.01). Moreover, each treated branch was placed into a branch-bag which allowed the local microclimate experienced by the treated branch to be controlled and monitored. Branch bag CO2 mole fraction was set to ambient. Each treatment was applied to four plants (four replicates). A full description of the experimental method is given in Frak et al. (2002).
20-year-old tree: The experiment was carried out during August 1996 on a 20-year-old walnut tree (Juglans regia). The selected tree was 7.7 m high, and the crown had 6 m diameter and 5 m height. Total leaf area was 144 m2 for a 95 m3 crown volume. The tree was located in the middle of a 1.5 ha orchard, planted in 1976 in Plauzat (France) at a density of 100 ha–1. A scaffolding around the tree and a platform inside the crown gave access to the major parts of crown volume. A complete experimental site description is given by Le Roux et al. (1999a).
Gas exchange and chlorophyll fluorescence measurements
Three-year-old trees: Gas exchange measurements were performed using a Li-6400 (Licor, Li-Cor Inc., Lincoln, NE, USA) system. Chlorophyll fluorescence measurements were performed concurrently with gas exchange measurements using a home-made leaf head in order to measure fluorescence over all the 6 cm2 adaxial leaf surface in the chamber. Red-light-emitting diodes (Stanley KR5005S, peak wavelength at 663 nm) provided both actinic illumination and a saturating pulse. Plastic optical fibres evenly distributed between the LEDs were used to guide modulated light and fluorescence, respectively, from and to the optical port of a Mini-PAM (Walz, Heinz Walz GmbH, Effeltrich, Germany). In order to minimize the CO2 diffusion leaks through the gaskets clamping the leaf, the CO2 mole fraction gradient between the inside and the outside of the chamber was minimized by enclosing the leaf head in a closed plastic bag circulated with the air exhausted from the chamber and the reference analysing cells of the instrument.
Detached fully expanded leaves were used, with the petiole kept in distilled water. Leaf temperature was controlled at 25 °C, and leaf-to-air vapour pressure deficit was maintained between 1 and 1.3 kPa. Leaves were first dark-adapted for 30 min for the dark respiration measurement (Robs). Light in the chamber was turned on for 2 h and maximal net assimilation (Anmax) and maximal stomatal conductance to CO2 (gscmax) were measured at high irradiance (1500 µmol photon m–2 s–1). Then a response curve of net assimilation (An) and fluorescence parameters to ambient CO2 mole fraction (Ca) ranging from 500–200 µmol mol–1 was carried out at low irradiance (100–150 µmol photon m–2 s–1) for mesophyll conductance (gi) estimation. For a set of leaves, this protocol was immediately followed by measurements of An response to Ca ranging from 60–120 µmol mol–1 at three irradiance levels (between 100 and 600 µmol photons m–2 s–1) to estimate the CO2 compensation point without mitochondrial respiration (*) and respiration in the light (Rlight). Another set of leaves was used for the estimation of maximal rates of carboxylation (Vcmax) and maximal rates of electron transport (Jmax) using the An response curve of CO2 mole fraction at the evaporating surfaces within the leaf (Ces) or the CO2 mole fraction at the carboxylation sites of Rubisco (Cc) at high irradiance (1200 µmol photon m–2 s–1) obtained at Ca ranging from 1900–100 µmol mol–1.
20-year-old tree: Gas exchange measurements were carried out as described above with a Li-6400 system. Measurements were made under natural irradiance, and the photosynthetic photon flux density (PPFD) was adjusted using neutral filters. Chlorophyll fluorescence measurements were carried out simultaneously with gas exchanges using a Mini-PAM (Walz, Germany) and the 6400–10 Mini-PAM adapter (Licor, Li-Cor Inc., Lincoln, NE, USA) for the Li-6400 leaf chamber.
Measurements were performed on attached fully expanded leaves with a healthy appearance. Leaves were sampled at the centre of the crown for the shade leaves (four replicates), and at the southern edge of the crown for sun leaves (six replicates). The estimation of mesophyll conductance was performed at high PPFD (900 µmol photon m–2 s–1 on average).
Estimation of CO2 compensation point without respiration, respiration in the light, mesophyll conductance, maximal rates of carboxylation, and maximal rates of electron transport
Gas exchange parameters were calculated according to Von Caemmerer and Farquhar (1981). The apparent CO2 compensation point in the absence of mitochondrial respiration (*app) and Rlight were estimated according to Brooks and Farquhar (1985).
For the 3-year-old tree leaves, gi and Cc were estimated according to Harley et al. (1992a) using the ‘constant J method’. *app and Rlight that were estimated for the same leaf were used to correct the CO2 compensation point for the gi effect according to Von Caemmerer et al. (1994) as:
where * is the ‘true’ CO2 compensation point in the absence of mitochondrial respiration. After substituting * by its expression in Equation (1) in the equation used for the ‘constant J method’, gi and Cc were estimated following Harley et al. (1992a).
For the mature tree leaves, the ‘variable J method’ (Harley et al., 1992a) was used to estimate gi and Cc, using parametrization of * and Rlight/Rdark that was obtained for the 3-year-old tree leaves. The rate of electron flow (J) was calculated as:
J = 
PSII x a x I x ß(2)
where PSII is the photochemical yield of photosystem II, a the leaf absorbance, I the incident PPFD and ß the fraction of absorbed quanta that reached photosystem II. a was 0.84 for walnut (Combes et al., 2000) and ß was assumed to be 0.5.
The parameters Vcmax and Jmax of the Farquhar et al. (1980) model were estimated according to Harley et al. (1992b). Apparent parameters were determined using An versus Ces relationships, while parameters corrected for internal conductance (corrected parameters) were determined using An versus Cc relationships according to Epron et al. (1995).
Leaf mass per area, leaf nitrogen, and Rubisco
The leaves of the potted trees and of the mature tree were sampled just after the gas exchange and chlorophyll fluorescence measurements. Leaf area was measured using a leaf area-meter (Delta T devices, Hoddesdon, UK) before the leaves were dried and the dry mass measured for leaf mass per area (LMA) estimation. Total leaf nitrogen concentration (Na, 16 replicates) was determined on a dry mass basis using an elemental analyser (Carlo Erba Instruments, Milan, Italy).
For 12 leaves of the potted trees in each treatment, Rubisco quantification was performed on one 5 cm2 disc sampled on each treated branch. Discs were frozen immediately in liquid N2 and stored at –80 °C. Rubisco content was determined using an Elisa assay following a Rubisco extraction as described in Catt and Millard (1988) and Frak et al. (2001).
Leaf thickness, volume fraction of intercellular air space, pathlength for CO2 transfer and conductance to CO2 transfer in the mesophyll air spaces
Leaf thickness (seven replicates) was measured using a digital calliper (Mitutoyo CD-15DC, UK). The fraction of leaf volume occupied by air space (three replicates) was estimated by vacuum infiltration using distilled water with 1
Triton X-100 (Sigma Chemicals). Leaf discs were collected in the area used for gas exchange measurements. Disc mass was measured before and immediately after infiltration. Leaf volume fraction of airspace was calculated as:
where fias is the fraction of total leaf volume occupied by air space, IW is the infiltrated weight and FW the fresh weight before infiltration.
The mean effective pathlength for CO2 transfer from the substomatal cavity to cell surfaces at the uppermost mesophyll surface between the two epiderms () was calculated according to Syvertsen et al. (1995) as:
where L is the leaf thickness, 
the fraction of leaf thickness occupied by epidermis, and fias/(1–) is the fraction of mesophyll volume occupied by intercellular air spaces. was estimated using optical microscopy with hand-made leaf sections on fresh sun and shade leaves sampled on an independent set of young walnut trees and in a mature walnut tree in Clermont-Ferrand. was not significantly different between the mature tree and the young tree, and between sun and shade leaves, and average value were 0.098±0.013 (n=26).
An estimation of the conductance to CO2 transfer in the mesophyll intercellular air spaces can be calculated according to Syvertsen et al. (1995) as:
gias = (
)–1(5)
with equal to 1.63 m s µmol–1.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Effects of irradiance on leaves of 3-year-old trees
In comparison with sun leaves, shade leaves had 46% lower LMA, 33% lower thickness, and 27% larger fias (Table 1). The amounts of nitrogen and Rubisco per leaf area were, respectively, 43% and 51% lower for shade leaves compared with sun leaves. Shade leaves exhibited a 42% lower Anmax, 53% lower gsc and 55% lower gi than sun leaves (Table 2). Rdark and Rlight of shade leaves were 2-fold lower than for sun leaves (Table 3). The inhibition of Rdark by light was similar in sun and shade leaves (approximately 40%).
* was significantly different after correction for gi whatever the leaf treatment (Table 3) and * was 3 µmol mol–1 higher than *app. Moreover, both * and *app were not significantly affected by leaf treatments, and the average * value (50.6 µmol mol–1) has been used for gi calculation.
|
|
|
Ces/Ca and Cc/Ca were around 0.77 and 0.5, respectively, and were similar in sun and shade leaves (Table 2). Apparent Vcmax was significantly higher than Vcmax corrected for gi, whereas taking gi into account did not affect Jmax (Fig. 1). Vcmax and Jmax were both significantly lower for shade than sun leaves. The Jmax/Vcmax ratio was significantly lower when corrected for gi than the apparent value (Fig. 1). The apparent Jmax/Vcmax ratio was 17% higher for shade leaves than for sun leaves. The corrected Jmax/Vcmax ratio was not different between shade and sun leaves.
|
Sun and shade leaves within the mature tree crown
In the mature tree crown, shade leaves exhibited a 39% lower LMA and 48% lower Na than sun leaves (Table 4). Leaf photosynthetic characteristics were also markedly changed and An at high PPFD and gi were 59% and 64% lower for shade than sun leaves, respectively. As the PPFD under which An was measured (900 µmol photons m–2 s–1) was not fully saturating for sun leaves, it was estimated that An was around 7% lower than Anmax based on An versus PPFD curves in sun leaves (data not shown).
|
Relationships between gi and leaf characteristics
gi was positively correlated with LMA, Na and Anmax (Fig. 2). gi versus LMA and gi versus Na relationships (Fig. 2) significantly differed among leaves of the 3-year-old trees and the leaves of the mature tree crown. By contrast, a common relationship was observed between gi and Anmax for the two data sets.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Marked anatomical and photosynthetic responses of leaves to the irradiance microclimate were observed in walnut. In the experimental sun and shade treatments, the 2-fold lower LMA, and 30% lower fias and thickness observed on shade leaves relative to sun leaves suggest the occurrence of large modifications of mesophyll structure and organization and a less densely packed mesophyll. Concurrently with anatomical changes, leaf gas exchanges were strongly affected, and Anmax, gi and gscmax were approximately 2-fold lower in shade than in sun leaves. Na and Rubisco content were also strongly affected by shade. A similar extent of acclimation response was observed for sun and shade leaves in the mature tree crown compared with the foliage of young trees. These results confirm that walnut leaves are highly responsive to the light environment and, importantly, that these treatments induced similar modifications of leaf characteristics to those observed in local sun and shade conditions in a mature tree crown (Le Roux et al., 1999a, b). However, LMA and Na were 40–50% higher in the mature tree than in the 3-year-old tree for a given light environment. These differences of LMA and Na for a rather similar range of acclimation of photosynthetic capacity were probably due to changes in leaf structure and composition and to a change in the fraction of nitrogen allocated to the photosynthetic apparatus, which may result from the differences in age and genotype between the materials. Moreover, the leaves of the mature tree may have been exposed to environmental stresses which can give rise to more dense and sclerified tissue, as well as modifications in mesophyll organization (Castro-Diez et al., 2000).
Strong positive correlations were found between gi and Anmax in response to these treatments and inside the tree crown, and those relationships were not significantly different. Thus, despite the large shift in LMA and differences in leaf anatomy between the two experiments, a similar relationship was evident between photosynthetic capacity and mesophyll conductance. A similar positive relationship between photosynthetic capacity and mesophyll conductance has been reported for several studies using various mesophytic and sclerophyllous species (Evans and Loreto, 2000). Importantly, this implies that a common robust relationship between photosynthetic capacity and mesophyll conductance can describe the intraspecific variability during light acclimation in walnut as well as interspecific variability. Therefore, a steady relationship may be predicted between mesophyll conductance and Vcmax. For the experiment on the 3-year-old trees where Vcmax data were available, mesophyll conductance can be scaled to Vcmax using gi=(4.49 Vcmax –20.6)10–3 (n=14, r2=0.59) for apparent Vcmax. A similar scaling by apparent Vcmax has been used recently to parametrize gi in a photosynthetic model for walnut (see Le Roux et al., 2001b).
Positive correlations were found for gi versus LMA, and those relationships were parallel and clearly distinct between the 3-year-old trees and the mature tree. A positive correlation between gi and LMA was also reported by Evans et al. (1994) for tobacco leaves grown under two different irradiances. Syvertsen et al. (1995) found a negative correlation between gi and LMA during an interspecific comparison, and a positive one when comparing irradiance effects within each species. Acclimation to irradiance levels resulted in a positive correlation between gi and mesophyll thickness of the leaves in those studies as well as in this one (r2=0.74, n=7, data not shown) and in a negative one with fias (r2=0.80, n=5, this experiment). Grapefruit was an exception as no correlation was observed between gi and fias (Syvertsen et al., 1995). As a consequence in all these studies, estimated mean effective pathlength for CO2 transfer from the substomatal cavity to the chloroplasts of the uppermost mesophyll surface positively correlated to gi (r2=0.77, n=6, in this experiment). In walnut, this value markedly decreased from 1.45 mm to 0.72 mm in sun and shade leaves, respectively. This suggests that the conductance for CO2 transfer in the gaseous intercellular space, gias should be lower in the sun than in the shade leaves. gias was estimated according to Syvertsen et al. (1995) as 0.43 and 0.83 mol m–2 s–1 in sun and shade leaves, respectively. Therefore, gias is likely to be a minor constraint on mesophyll conductance in shade leaves, but should represent a more significant constraint on CO2 transfer in sun leaves. However, considering the low mesophyll conductance of sun and shade walnut leaves if the gaseous phase transfer is more limiting in sun leaves, it is offset by changes in the liquid phase components of mesophyll conductance during light acclimation. These data support the earlier conclusion that, in many leaves, even sclerophyllous ones, the limitation of CO2 transfer in leaf air spaces should be a minor component of mesophyll conductance (Genty et al., 1998; Evans and Loreto, 2000). Overall, these data confirm that even if LMA and gi may reflect light acclimation-driven changes of leaf anatomy (i.e. thickness, porosity), the relationship between gi and LMA would be strongly dependent on species, age and growth conditions. Therefore, assuming that the relationship between gi and photosynthetic capacity remains unchanged, the relationship between gi and LMA would be likely to be poor when photosynthetic capacity is not closely related to LMA, which is a well-documented situation during leaf ageing and acclimation to a changing light environment (for example, Frak et al., 2001). Similarly, when photosynthetic capacity is not closely related to leaf nitrogen (for example, Frak et al., 2001), the correlation between gi and leaf nitrogen would also probably be poor.
*, which probes the Rubisco specificity factor was not significantly changed during light acclimation. However, in view of the low number of repetitions, the hypothesis of a change of * in response to irradiance cannot be excluded. The mean * was higher than the range of published values of * measured in vivo (between 33 and 46.6 µmol mol–1; Evans and Loreto, 2000). However, all except one (see Von Caemmerer et al., 1994) of the published studies using the Brooks and Farquhar (1985) in vivo method did not take into account the effect of mesophyll conductance, and underestimated *. For species with low gi such as walnut, * was underestimated by 3 µmol mol–1 without mesophyll conductance correction, but this shift cannot explain the causes of the high * values of walnut. Comparative measurements in tobacco (Nicotiana tabacum L. cv. W38) for which * is well-documented were carried out, and these results (*=40.3±2.1 µmol mol–1, n=4, at standard atmospheric pressure) were not different from those previously reported by Von Caemmerer et al. (1994). Determining gi for walnut with the gas exchange and fluorescence method using the commonly used * of tobacco would lead to an unrealistic and a more than 2-fold underestimated gi (data not shown). This shows that * has to be measured systematically when using the gas exchange and fluorescence method for gi determination (see also Evans and Loreto, 2000, for a discussion).
Respiration was strongly responsive to growth irradiance, and a similar degree of instantaneous inhibition of respiration by light (approximately 40% of dark respiration) was observed whatever the growth irradiance. In both sun and shade leaves, maximum inhibition was reached at the two lowest irradiances used for * measurements (100 and 200 µmol photons m–2 s–1). This indicated that the rate of respiration in the light is less than the rate of respiration in darkness as previously reported (Brooks and Farquhar, 1985; Villar et al., 1994; Atkin et al., 2000) and maximal light inhibition did not depend on leaf acclimation to irradiance in walnut.
Vcmax was largely enhanced by taking gi into account whereas Jmax remained nearly constant. Those results confirmed previous data (Lloyd et al., 1992; Epron et al., 1995). Therefore Jmax/Vcmax increased when taking gi into account, but importantly no significant differences were observed during light acclimation. This result confirmed that changes of Jmax and Vcmax are closely correlated under various growth conditions (Von Caemmerer and Farquhar, 1981). The resulting constancy of Jmax/Vcmax during light acclimation indicates that the Cc at which Rubisco and photosynthetic electron transport equally limit CO2 assimilation remained unchanged during light acclimation, as previously inferred in studies where gi was not taken into account (studies on the basis of Ces) (Von Caemmerer and Farquhar, 1981). This is a likely consequence of the strong positive correlation between gi and photosynthetic capacity during light acclimation which results in a relatively invariant gradient between Ces and Cc at light saturation.
|
Conclusion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
The strong variations of walnut leaf anatomy and photosynthesis response to irradiance were accompanied by a strong effect on mesophyll CO2 transfer conductance. The tight interspecific correlation between mesophyll conductance versus photosynthetic capacity pointed out in previous studies is conserved for sun and shade walnut leaves and accurately describes the strong intraspecific variability with light acclimation in walnut. This suggests that photosynthetic capacity and, presumably, maximal rate of carboxylation can be used to scale within-canopy variations of mesophyll conductance due to leaf acclimation to irradiance. In this context, basic studies are required to describe the temperature dependencies of mesophyll conductance versus photosynthetic capacity, together with the temperature dependencies of Rubisco kinetics parameters.
|
Acknowledgements |
|---|
We acknowledge financial support from the Groupement de Recherche ‘FLUOVEG’ (GDR 1536, CNRS). The PhD fellowship of CP was funded by the French Ministry of National Education and Research (MENRT). We thanks Dr Sylvie Meyer (LURE, Université Paris-Sud) for helpful discussion, and Dr Laurent Nussaume (CEA-Cadarache) for help with the optical microscopy.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Anten NPR, Hernandez R, Medina EM. 1996. The photosynthetic capacity and leaf nitrogen concentration as related to light regime in shade leaves of a montane tropical forest tree, Tetrorchidium rubrivenium. Functional Ecology 10, 491–500.[Web of Science]
Atkin OK, Evans JR, Ball MC, Lambers H, Pons TL. 2000. Leaf respiration of Snow Gum in the light and dark. Interactions between temperature and irradiance. Plant Physiology 122, 915–923.
Boardman NK. 1977. Comparative photosynthesis of sun and shade plants. Annual Review of Plant Physiology 28, 355–377.[Web of Science]
Brooks A, Farquhar GD. 1985. Effects of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165, 397–406.[Web of Science]
Castro-Dìez P, Puyravaud JP, Cornelissen JHC. 2000. Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plants species and types. Oecologia 124, 476–486.[Web of Science]
Catt JW, Millard P. 1988. The measurement of ribulose-1,5-bisphosphate carboxylase/oxygenase concentration in the leaves of potato plants by enzyme linked immunosorbtion assays. Journal of Experimental Botany 39, 157–164.
Chazdon RL, Kaufmann S. 1993. Plasticity of leaf anatomy of two rain forest shrubs in relation to photosynthetic light acclimation. Functional Ecology 7, 385–394.[Web of Science]
Combes D, Sinoquet H, Varlet-Grancher C. 2000. Preliminary measurements and simulation of the spatial distribution of the morphogenetically active radiation (MAR) within an isolated tree canopy. Annals of Forest Sciences 57, 497–511.
Delfine S, Alvino A, Zacchini M, Loreto F. 1998. Consequences of salt stress on conductance to CO2 diffusion, RubisCO characteristics and anatomy of spinach leaves. Australian Journal of Plant Physiology 25, 395–402.[Web of Science]
Delfine S, Alvino A, Concetta-Villani M, Loreto F. 1999. Restriction to carbon dioxide conductance and photosynthesis in spinach leaves recovering from salt stress. Plant Physiology 119, 1101–1106.
Epron D, Godard D, Cornic G, Genty B. 1995. Limitation of net CO2 assimilation rate by internal resistances to CO2 transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.). Plant, Cell and Environment 18, 43–51.
Evans JR, Loreto F. 2000. Acquisition and diffusion of CO2 in higher plant leaves. In: Leegood RC, Sharkey TD, Von Caemmerer S, eds. Photosynthesis: physiology and metabolism. Dordrecht: Kluwer Academic Publishers, 321–351.
Evans JR, Von Caemmerer S, Stetchell BA, Hudson GS. 1994. The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Australian Journal of Plant Physiology 21, 475–495.[Web of Science]
Farquhar GD, Von Caemmerer S, Berry JA. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 179, 78–90.
Frak E, Le Roux X, Millard P, Adam B, Dreyer E, Escuit C, Sinoquet H, Vandame M, Varlet-Grancher C. 2002. Spatial distribution of leaf nitrogen and photosynthetic capacity within the foliage of individual trees: disentangling the effects of local light quality, leaf irradiance and transpiration. Journal of Experimental Botany 53, 2207–2216.
Frak E, Le Roux X, Millard P, Dreyer E, Jaouen G, Saint-Joanis B, Wendler R. 2001. Changes in total leaf nitrogen drive photosynthetic acclimation to light in fully developed walnut leaves. Plant, Cell and Environment 24, 1279–1288.
Genty B, Meyer S, Piel C, Badeck FW, Liozon R. 1998. CO2 diffusion inside leaf mesophyll of ligneous plants. In: Garab G, ed. Photosynthesis: mechanism and effects. Dordrecht: Kluwer Academic Publishers, 3961–3966.
Harley PC, Loreto F, Di Marco G, Sharkey TD. 1992a. Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiology 98, 1429–1436.
Harley PC, Thomas JF, Reynolds JF, Strain BR. 1992b. Modelling photosynthesis of cotton grown in elevated CO2. Plant, Cell and Environment 15, 271–282.
Kappel F, Flore JA. 1983. Effect of shade on photosynthesis, specific leaf weight, leaf chlorophyll content, and morphology of young peach trees. Journal of the American Society for Horticultural Science 108, 541–544.[Web of Science]
Lauteri M, Scartazza A, Guido MC, Brugnoli E. 1997. Genetic variation in photosynthetic capacity, carbon isotope discrimination and mesophyll conductance in provenances of Castanea sativa adapted to different environments. Functional Ecology 11, 675–683.[Web of Science]
Le Roux X, Bariac T, Sinoquet H, Genty B, Piel C, Mariotti A, Richard P. 2001b. Spatial distribution of leaf water-use efficiency and carbon isotope discrimination within an isolated tree crown: field observation and model simulation. Plant, Cell and Environment 10, 1021–1033.
Le Roux X, Grand S, Dreyer E, Daudet FA. 1999b. Parameterization and testing of a biochemically based photosynthesis model for walnut (Juglans regia) trees and seedlings. Tree Physiology 19, 481–492.
Le Roux X, Sinoquet H, Vandame M. 1999a. Spatial distribution of leaf dry weight per area and leaf nitrogen concentration in relation to local radiation regime within an isolated tree crown. Tree Physiology 19, 181–188.
Le Roux X, Walcroft AS, Daudet FA, Sinoquet H, Chaves MM, Rodriguez A, Osorio L. 2001a. Photosynthetic light acclimation in peach leaves: importance of changes in mass:area ratio, nitrogen concentration, and leaf nitrogen partitioning. Tree Physiology 21, 377–386.
Lloyd J, Syvertsen JP, Kriedemann PE, Farquhar GD. 1992. Low conductance for CO2 diffusion from stomata to the sites of carboxylation in leaves of woody species. Plant, Cell and Environment 15, 873–899.
Loreto F, Di Marco G, Tricoli D, Sharkey TD. 1994. Measurement of mesophyll conductance, photosynthetic electron transport and alternative electron sinks of field-grown wheat leaves. Photosynthesis Research 41, 397–403.
Miyazawa S-I, Terashima I. 2001. Slow development of leaf photosynthesis in an evergreen broad-leaved tree, Castanopsis sieboldii: relationships between leaf anatomical characteristics and photosynthetic rate. Plant, Cell and Environment 24, 279–291.
Niinemets Ü, Tenhunen JD. 1997. A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant, Cell and Environment 20, 845–866.
Nobel PS. 1991. Physicochemical and environmental plant physiology. San Diego: Academic Press.
Parkhurst DF. 1994. Tansley review no. 65: Diffusion of CO2 and other gases inside leaves. New Phytologist 126, 449–479.[Web of Science]
Rand RH. 1978. A theoretical analysis of CO2 absorption in sun versus shade leaves. Journal of Biomechanical Engineering 100, 20–24.[Web of Science]
Scartazza A, Lauteri M, Guido MC, Brugnoli E. 1998. Carbon isotope discrimination in leaf and stem sugars, water use efficiency and mesophyll conductance during different developmental stages in rice subjected to drought. Australian Journal of Plant Physiology 25, 489–498.[Web of Science]
Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD. 1995. On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant, Cell and Environment 18, 149–157.
Villar R, Held AA, Merino J. 1994. Comparison of methods to estimate dark respiration in the light in leaves of two woody species. Plant Physiology 105, 167–172.[Abstract]
Von Caemmerer S, Evans JR, Hudson GS, Andrews TJ. 1994. The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of trangenic tobacco. Planta 195, 88–97.[Web of Science]
Von Caemmerer S, Farquhar GD. 1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.[Web of Science]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Monti, G. Bezzi, and G. Venturi Internal conductance under different light conditions along the plant profile of Ethiopian mustard (Brassica carinata A. Brown.) J. Exp. Bot., May 1, 2009; 60(8): 2341 - 2350. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Niinemets, I. J. Wright, and J. R. Evans Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation J. Exp. Bot., May 1, 2009; 60(8): 2433 - 2449. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Niinemets, A. Diaz-Espejo, J. Flexas, J. Galmes, and C. R. Warren Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field J. Exp. Bot., May 1, 2009; 60(8): 2249 - 2270. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. R. Warren Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer J. Exp. Bot., May 1, 2008; 59(7): 1475 - 1487. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. R. Warren Soil water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not J. Exp. Bot., February 1, 2008; 59(2): 327 - 334. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||