ALBERT

Notes: Abstract  Variations in the partitioning of foliar carbon and nitrogen in combination with changes in needle and shoot structure were studied in trees of Picea abies along a vertical gradient of relative irradiance (RI). RI was the major determinant of needle morphology, causing all needle linear parameters – width, thickness and length – to increase. Due to the different responsiveness of needle thickness and width in respect of RI, the ratio of total to projected needle area increased with RI. Furthermore, shoot structure was also influenced by RI, and the ratio of shoot silhouette area to total needle area, which characterises the packing of needles and needle area within the shoot, was greater at lower values of irradiance. Needle dry weight per total needle area (LWAt) was also increased by RI. Similarly, irrespective of the measure for surface area, needle nitrogen content per area, as the product of needle dry weight per area and nitrogen content per needle dry weight (Nm), scaled quasi-linearly with needle weight per area. Thus, the changes in needle and shoot morphology made it possible to invest more photosynthesising weight per unit light-intercepting surface there, where the pay-back due to elevated irradiances was the highest. However, Nm behaved in an entirely different manner, decreasing hyperbolically with LWAt. Since non-structural (carbon in non-structural carbohydrates), and structural (total minus non-structural) needle carbon per dry weight also increased with LWAt, Nm was inversely correlated with both non-structural and structural carbon. Total tree height, increasing significantly LWAt, also influenced needle structure. It appeared that total height did not affect needle thickness or width, but larger trees had greater needle density (dry weight per volume). Because needle density was positively correlated with needle carbon content per dry weight, it was assumed that the greater values of needle carbon content can be attributed to increased lignification and thickening of needle cell walls. Thus, it appeared that the proportion of supporting structures was greater in needles of larger trees. Inasmuch as an increased fraction of supporting structures dilutes other leaf substances, including also leaf compounds responsible for CO2-assimilation, enhanced requirement for supporting structures may be responsible for lower rates of carbon assimilation per foliage dry weight observed in large trees. Increasing water limitation with increasing tree size is discussed as a possible cause for increased needle supporting costs in large trees.

Notes: Leaf gas-exchange and chemical composition were investigated in seedlings of Quercus suber L. grown for 21 months either at elevated (700 μmol mol–1) or normal (350 μmol mol–1) ambient atmospheric CO2 concentrations, [CO2], in a sandy nutrient-poor soil with either ‘high’ N (0.3 mol N m–3 in the irrigation solution) or with ‘low’ N (0.05 mol N m–3) and with a constant suboptimal concentration of the other macro- and micronutrients. Although elevated [CO2] yielded the greatest total plant biomass in ‘high’ nitrogen treatment, it resulted in lower leaf nutrient concentrations in all cases, independent of the nutrient addition regime, and in greater nonstructural carbohydrate concentrations. By contrast, nitrogen treatment did not affect foliar N concentrations, but resulted in lower phosphorus concentrations, suggesting that under lower N, P use-efficiency in foliar biomass production was lower. Phosphorus deficiency was evident in all treatments, as photosynthesis became CO2 insensitive at intercellular CO2 concentrations larger than ≈ 300 μmol mol–1, and net assimilation rates measured at an ambient [CO2] of 350 μmol mol–1 or at 700 μmol mol–1 were not significantly different. Moreover, there was a positive correlation of foliar P with maximum Rubisco (Ribulose-1,5-bisphosphate carboxylase/oxygenase) carboxylase activity (Vcmax), which potentially limits photosynthesis at low [CO2], and the capacities of photosynthetic electron transport (Jmax) and phosphate utilization (Pmax), which are potentially limiting at high [CO2]. None of these potential limits was correlated with foliar nitrogen concentration, indicating that photosynthetic N use-efficiency was directly dependent on foliar P availability. Though the tendencies were towards lower capacities of potential limitations of photosynthesis in high [CO2] grown specimens, the effects were statistically insignificant, because of (i) large within-treatment variability related to foliar P, and (ii) small decreases in P/N ratio with increasing [CO2], resulting in balanced changes in other foliar compounds potentially limiting carbon acquisition. The results of the current study indicate that under P-deficiency, the down-regulation of excess biochemical capacities proceeds in a similar manner in leaves grown under normal and elevated [CO2], and also that foliar P/N ratios for optimum photosynthesis are likely to increase with increasing growth CO2 concentrations. Symbols: A, net assimilation rate (μmol m–2 s–1); Amax, light-saturated A (μmol m–2 s–1); α, initial quantum yield at saturating [CO2] and for an incident Q (mol mol–1); [CO2], atmospheric CO2 concentration (μmol mol–1); Ci, intercellular CO2 concentration (μmol mol–1); Ca, CO2 concentration in the gas-exchange cuvette (μmol mol–1); FB, fraction of leaf N in ‘photoenergetics’; FL, fraction of leaf N in light harvesting; FR, fraction of leaf N in Rubisco; Γ*, CO2 compensation concentration in the absence of Rd (μmol mol–1); Jmax*, capacity for photosynthetic electron transport; Jmc, capacity for photosynthetic electron transport per unit cytochrome f (mol e–[mol cyt f]–1 s–1); Kc, Michaelis-Menten constant for carboxylation (μmol mol–1); Ko, Michaelis-Menten constant for oxygenation (mmol mol–1); MA, leaf dry mass per area (g m–2); O, intercellular oxygen concentration (mmol mol–1); [Pi], concentration of inorganic phosphate (mM); Pmax*, capacity for phosphate utilization; Q, photosynthetically active quantum flux density (μmol m–2 s–1); Rd*, day respiration (CO2 evolution from nonphotorespiratory processes continuing in the light); Rubisco, ribulose-1,5-bisphosphate carboxylase/oxygenase; RUBP, ribulose-1,5-bisphosphate; Tl, leaf temperature (°C); UTPU*, rate of triose phosphate utilization; Vcmax*, maximum Rubisco carboxylase activity; Vcr, specific activity of Rubisco (μmol CO2[g Rubisco]–1 s–1]*given in either μmol m–2 s–1 or in μmol g–1 s–1 as described in the text.

Notes: The present study investigated the interaction of growth irradiance (Qint) with leaf capacity for and kinetics of adjustment of the pool size of xanthophyll cycle carotenoids (sum of violaxanthin, antheraxanthin and zeaxanthin; VAZ) and photosynthetic electron transport rate (Jmax) after changes in leaf light environment. Individual leaves of lower-canopy/lower photosynthetic capacity species Tilia cordata Mill. and upper canopy/higher photosynthetic capacity species Populus tremula L. were either illuminated by additional light of 500–800 µmol m−2 s−1 for 12 h photoperiod or enclosed in shade bags. The extra irradiance increased the total amount of light intercepted by two-fold for the upper and 10–15-fold for the lower canopy leaves, whereas the shade bags transmitted 45% of incident irradiance. In control leaves, VAZ/area, VAZ/Chl and Jmax were positively associated with leaf growth irradiance (Qint). After 11 d extra illumination, VAZ/Chl increased in all cases due to a strong reduction in foliar chlorophyll, but VAZ/area increased in the upper canopy leaves of both species, and remained constant or decreased in the lower canopy leaves of T. cordata. The slope for VAZ/area changes with cumulative extra irradiance was positively associated with Qint only in T. cordata, but not in P. tremula. Nevertheless, all leaves of P. tremula increased VAZ/area more than the most responsive leaves of T. cordata. Shading reduced VAZ content only in P. tremula, but not in T. cordata, again demonstrating that P. tremula is a more responsive species. Compatible with the hypothesis of the role of VAZ in photoprotection, the rates of photosynthetic electron transport declined less in P. tremula than in T. cordata after the extra irradiance treatment. However, foliar chlorophyll contents of the exposed leaves declined significantly more in the upper canopy of P. tremula, which is not consistent with the suggestion that the leaves with the highest VAZ content are more resistant to photoinhibition. This study demonstrates that previous leaf light environment may significantly affect the adaptation capacity of foliage to altered light environment, and also that species differences in photosynthetic capacity and acclimation potentials importantly alter this interaction.

Notes: A process-based leaf gas exchange model for C3 plants was developed which specifically describes the effects observed along light gradients of shifting nitrogen investment in carboxylation and bioenergetics and modified leaf thickness due to altered stacking of photosynthetic units. The model was parametrized for the late-successional, shade-tolerant deciduous species Acer saccharum Marsh. The specific activity of ribulose-1,5-bisphosphate carboxylase (Rubisco) and the maximum photosynthetic electron transport rate per unit cytochrome f (cyt f) were used as indices that vary proportionally with nitrogen investment in the capacities for carboxylation and electron transport. Rubisco and cyt f per unit leaf area are related in the model to leaf dry mass per area (MA), leaf nitrogen content per unit leaf dry mass (Nm), and partitioning coefficients for leaf nitrogen in Rubisco (PR) and in bioenergetics (PB). These partitioning coefficients are estimated from characteristic response curves of photosynthesis along with information on lear structure and composition. While PR and PB determine the light-saturated value of photosynthesis, the fraction of leaf nitrogen in thylakoid light-harvesting components (PL) and the ratio of leaf chlorophyll to leaf nitrogen invested in light harvesting (CB), which is dependent on thylakoid stoichiometry, determine the initial photosynthetic light utilization efficiency in the model. Carbon loss due to mitochondrial respiration, which also changes along light gradients, was considered to vary in proportion with carboxylation capacity. Key model parameters - Nm, PR, PB, PLCB and stomatal sensitivity with respect to changes in net photosynthesis (Gr) – were examined as a function of MA, which is linearly related to irradiance during growth of the leaves. The results of the analysis applied to A. saccharum indicate that PB and PR increase, and Gf, PL and CB decrease with increasing MA. As a result of these effects of irradiaiice on nitrogen partitioning, the slope of the light-saturated net photosynthesis rate per unit leaf dry mass (Ammax) versus Nm relationship increased with increasing growth irradiance in mid-season. Furthermore, the nitrogen partitioning coefficients as well as the slopes of Ammax versus Nm were independent of season, except during development of the leaf photosynthetic apparatus. Simulations revealed that the acclimation to high light increased Ammax by 40% with respect to the low light regime. However, light-saturated photosynthesis per leaf area (Aamax) varied 3-fold between these habitats, suggesting that the acclimation to high light was dominated by adjustments in leaf anatomy (Aamax=AmmaxMA) rather than in foliar biochemistry. This differed from adaptation to low light, where the alterations in foliar biochemistry were predicted to be at least as important as anatomical modifications. Due to the light-related accumulation of photosynthetic mass per unit area, Aamax depended on MA and leaf nitrogen per unit area (Na). However, Na conceals the variation in both MA and Nm (Na=NmMA), and prevents clear separation of anatomical adjustments in foliage structure and biochemical modifications in foliar composition. Given the large seasonal and site nutrient availability-related variation in Nm, and the influences of growth irradiance on nitrogen partitioning, the relationship between Aamax and Na is universal neither in time nor in space and in natural canopies at mid-season is mostly driven by variability in MA. Thus, we conclude that analyses of the effects of nitrogen investments on potential carbon acquisition should use mass-based rather than area-based expressions.

Notes: Responses of foliar light-saturated net assimilation rate (Amax), capacity for photosynthetic electron transport (Jmax) and mitochondrial respiration rate (Rd) to long-term canopy light and temperature environment were investigated in a temperate deciduous canopy composed of Populus tremula L. in the upper (17–28 m) and of Tilia cordata Mill. in the lower canopy layer (4–17 m). Climatic measurements indicated that seasonal average daily maximum air temperature (Tmax) was 5·5 °C (range 0·7–10·5 °C) higher in the top than in the bottom of the canopy, and strong positive correlations were observed between Tmax and seasonal average integrated quantum flux density (Qint), as well as between seasonal average daily mean temperature and Qint. Because of changes in leaf dry mass and nitrogen per unit area, Amax, Jmax, and Rd scaled positively with Qint in both species at a common leaf temperature (T). According to Jmax versus T response curves and dark chlorophyll fluorescence transients, photosynthetic electron transport was less heat resistant in P. tremula with optimum temperature of Jmax, Topt, of 33·5 ± 0·6 °C than in T. cordata with Topt of 40·7 ± 0·6 °C. This difference was suggested to manifest evolutionary adaptation of photosynthetic electron transport to cooler environments in P. tremula, the range of which extends farther north than that in T. cordata. Possibly because of acclimation to long-term canopy temperature environment, Topt was positively related to Qint in P. tremula, foliage of which was also exposed to higher irradiances and temperatures, but not in T. cordata, in the canopy of which quantum flux densities and temperatures were lower, and gradients in the environmental factors less pronounced. Parallel to changes in Topt, the activation energy for photosynthetic electron transport decreased with increasing Qint in P. tremula, indicating that Jmax of leaves acclimated to colder environment was more responsive to T in lower temperatures than that of high T acclimated leaves. Similar alterations in the activation energy for mitochondrial respiration rate were also observed, indicating that acclimation to temperature of mitochondrial and chloroplastic electron transport proceeds in a co-ordinated manner, and possibly involves long-term changes in membrane fluidity properties. We conclude that, because of correlations between temperature and light, the shapes of Jmax versus T, and Rd versus T response curves vary within tree canopies, and this needs to be taken account in modelling whole canopy photosynthesis.

Notes: We present a physiological model of isoprene (2-methyl-1,3-butadiene) emission which considers the cost for isoprene synthesis, and the production of reductive equivalents in reactions of photosynthetic electron transport for Liquidambar styraciflua L. and for North American and European deciduous temperate Quercus species. In the model, we differentiate between leaf morphology (leaf dry mass per area, MA, g m−2) altering the content of enzymes of isoprene synthesis pathway per unit leaf area, and biochemical potentials of average leaf cells determining their capacity for isoprene emission. Isoprene emission rate per unit leaf area (μmol m−2 s−1) is calculated as the product of MA, the fraction of total electron flow used for isoprene synthesis (ɛ, mol mol−1), the rate of photosynthetic electron transport (J) per unit leaf dry mass (Jm, μmol g−1 s−1), and the reciprocal of the electron cost of isoprene synthesis [mol isoprene (mol electrons−1)]. The initial estimate of electron cost of isoprene synthesis is calculated according to the 1-deoxy- D-xylulose-5-phosphate pathway recently discovered in the chloroplasts, and is further modified to account for extra electron requirements because of photorespiration. The rate of photosynthetic electron transport is calculated by a process-based leaf photosynthesis model. A satisfactory fit to the light-dependence of isoprene emission is obtained using the light response curve of J, and a single value of ɛ, that is dependent on the isoprene synthase activity in the leaves. Temperature dependence of isoprene emission is obtained by combining the temperature response curves of photosynthetic electron transport, the shape of which is related to long-term temperature during leaf growth and development, and the specific activity of isoprene synthase, which is considered as essentially constant for all plants. The results of simulations demonstrate that the variety of temperature responses of isoprene emission observed within and among the species in previous studies may be explained by different optimum temperatures of J and/or limited maximum fraction of electrons used for isoprene synthesis. The model provides good fits to diurnal courses of field measurements of isoprene emission, and is also able to describe the changes in isoprene emission under stress conditions, for example, the decline in isoprene emission in water-stressed leaves.

Notes: To understand the role of leaf-level plasticity and variability in species invasiveness, foliar characteristics were studied in relation to seasonal average integrated quantum flux density (Qint) in the understorey evergreen species Rhododendron ponticum and Ilex aquifolium at two sites. A native relict population of R. ponticum was sampled in southern Spain (Mediterranean climate), while an invasive alien population was investigated in Belgium (temperate maritime climate). Ilex aquifolium was native at both sites. Both species exhibited a significant plastic response to Qint in leaf dry mass per unit area, thickness, photosynthetic potentials, and chlorophyll contents at the two sites. However, R. ponticum exhibited a higher photosynthetic nitrogen use efficiency and larger investment of nitrogen in chlorophyll than I. aquifolium. Since leaf nitrogen (N) contents per unit dry mass were lower in R. ponticum, this species formed a larger foliar area with equal photosynthetic potential and light-harvesting efficiency compared with I. aquifolium. The foliage of R. ponticum was mechanically more resistant with larger density in the Belgian site than in the Spanish site. Mean leaf-level phenotypic plasticity was larger in the Belgian population of R. ponticum than in the Spanish population of this species and the two populations of I. aquifolium. We suggest that large fractional investments of foliar N in photosynthetic function coupled with a relatively large mean, leaf-level phenotypic plasticity may provide the primary explanation for the invasive nature and superior performance of R. ponticum at the Belgian site. With alleviation of water limitations from Mediterranean to temperate maritime climates, the invasiveness of R. ponticum may also be enhanced by the increased foliage mechanical resistance observed in the alien populations.

Notes: The present study was undertaken to test for the hypothesis that the rate of development in the capacity for photosynthetic electron transport per unit area (Jmax;A), and maximum carboxylase activity of Rubisco (Vcmax;A) is proportional to average integrated daily quantum flux density (Qint) in a mixed deciduous forest dominated by the shade-intolerant species Populus tremula L., and the shade-tolerant species Tilia cordata Mill. We distinguished between the age-dependent changes in net assimilation rates due to modifications in leaf dry mass per unit area (MA), foliar nitrogen content per unit dry mass (NM), and fractional partitioning of foliar nitrogen in the proteins of photosynthetic electron transport (FB), Rubisco (FR) and in light-harvesting chlorophyll-protein complexes (Vcmax;A ∝ MANMFR; Jmax;A ∝ MANMFB). In both species, increases in Jmax;A and Vcmax;A during leaf development were primarily determined by nitrogen allocation to growing leaves, increases in leaf nitrogen partitioning in photosynthetic machinery, and increases in MA. Canopy differences in the rate of development of leaf photosynthetic capacity were mainly controlled by the rate of change in MA. There was only small within-canopy variation in the initial rate of biomass accumulation per unit Qint (slope of MA versus leaf age relationship per unit Qint), suggesting that canopy differences in the rate of development of Jmax;A and Vcmax;A are directly proportional to Qint. Nevertheless, MA, nitrogen, Jmax;A and Vcmax;A of mature leaves were not proportional to Qint because of a finite MA in leaves immediately after bud-burst (light-independent component of MA). MA, leaf chlorophyll contents and chlorophyll : N ratio of mature leaves were best correlated with the integrated average quantum flux density during leaf development, suggesting that foliar photosynthetic apparatus, once developed, is not affected by day-to-day fluctuations in Qint. However, for the upper canopy leaves of P. tremula and for the entire canopy of T. cordata, there was a continuous decline in N contents per unit dry mass in mature non-senescent leaves on the order of 15–20% for a change of leaf age from 40 to 120 d, possibly manifesting nitrogen reallocation to bud formation. The decline in N contents led to similar decreases in leaf photosynthetic capacity and foliar chlorophyll contents. These data demonstrate that light-dependent variation in the rate of developmental changes in MA determines canopy differences in photosynthetic capacity, whereas foliar photosynthetic apparatus is essentially constant in fully developed leaves.

Notes: Intercellular CO2 mole fractions (Ci) are lower in the upper canopy relative to the lower canopy leaves. This canopy gradient in Ci has been associated with enhanced rates of carbon assimilation at high light, and concomitant greater draw-downs in Ci. However, increases in irradiance in the canopy are generally also associated with decreases in leaf water availability. Thus, stress effects on photosynthesis rates (A) and stomatal conductance (G), may provide a further explanation for the observed Ci gradients. To test the hypotheses of the sources of canopy variation in Ci, and quantitatively assess the influence of within-canopy differences in stomatal regulation on A, the seasonal and diurnal variation in G was studied in relation to seasonal average daily integrated quantum flux density (Qint) in tall shade-intolerant Populus tremula L. trees. Daily time-courses of A were simulated using the photosynthesis model of Farquhar et al. (Planta 149, 78–90, 1980). Stable carbon isotope composition of a leaf carbon fraction with rapid turnover rate was used to estimate canopy gradient in Ci during the simulations. Daily maximum G (Gmax) consistently increased with increasing Qint. However, canopy differences in Gmax decreased as soil water availability became limiting during the season. In water-stressed leaves, there were strong mid-day decreases in G that were poorly associated with vapour pressure deficits between the leaf and atmosphere, and the magnitude of the mid-day decreases in G occasionally interacted with long-term leaf light environment. Simulations indicated that the percentage of carbon lost due to mid-day stomatal closure was of the order of 5–10%, and seasonal water stress increased this percentage up to 20%. The percentage of carbon lost due to stomatal closure increased with increasing Qint. Canopy differences in light environment resulted in a gradient of daily average Ci of approximately 20 µmol mol−1. The canopy variation in seasonal and diurnal reductions in G led to a Ci gradient of approximately 100 µmol mol−1, and the actual canopy Ci gradient was of the same magnitude according to leaf carbon isotope composition. This study demonstrates that stress effects influence Ci more strongly than within-canopy light gradients, and also that leaves acclimated to different irradiance and water stress conditions may regulate water use largely independent of foliar photosynthetic potentials.

Notes: To test the hypothesis that in temperate deciduous trees acclimation to potentially damaging high irradiances occurs via long-term adjustments in foliar photosynthetic capacity, and short-term changes in xanthophyll cycle pool size in response to weather fluctuations, nitrogen concentration and pigment composition were examined along a canopy light gradient in three species –Betula pendula, Populus tremula and Tilia cordata (from most shade intolerant to tolerant), and foliage photosynthetic potentials in P. tremula and T. cordata. Integrated quantum flux density (Qi) incident on leaves was estimated with a method combining hemispherical photography and light measurements with quantum sensors made over the growing season. Long- and short-term light indices – average total seasonal daily integrated quantum flux density (Ts, mol m–2 d–1) and that of the 3 d preceding foliage sampling (T3d) – were calculated for each sampled leaf. In addition to total integrated quantum flux density, the part of Qi attributable to direct flux was also computed. Strong linear relationships between the capacity for photosynthetic electron transport per area (Jamax), estimated from in situ measurements of effective quantum yield of photosystem II (PS II), and Qi averaged over the season and over the preceding 3 d were found for all studied species. However, the major determinant of Jamax, the product of electron transport capacity per leaf dry mass (Jmmax) and leaf dry mass per area (MA), was MA rather than Jmmax, which was relatively constant along the light gradient. There was evidence that Jamax is more tightly related to Ts, which characterizes the light climate during foliar development, than to short-term integrated light, possibly because there is little flexibility in adjustments in MA after the completion of foliar growth. Leaf chlorophyll concentrations and the investment of leaf nitrogen in chlorophyll (Chl/N) were negatively related to Qi– an investment pattern which improves light harvesting in low light. Xanthophyll cycle pool size (VAZ, violaxanthin + antheraxanthin + zeaxanthin) either expressed per unit chlorophyll (VAZ/Chl) or as a fraction of total carotenoids (VAZ/Car) increased with increasing Qi in all species. However, contrary to Jamax, it tended to correlate more strongly with short-term than with long-term average integrated light. There were few interspecific differences in Jamax, Chl/N, VAZ/Chl and VAZ/Car when the variability in light level incident to the leaves was accounted for, indicating that the foliage of both shade-intolerant and -tolerant temperate tree species possesses considerable phenotypic flexibility. Collectively these results support the view that rapid adjustment of the xanthophyll cycle pool size provides an important means for acclimation to light fluctuations in a time scale of days, during which the potential for photosynthetic quenching of excitation energy is not likely to change appreciably.