Effects of mesophyll conductance on vegetation responses to elevated CO2 concentrations in a land surface model

Mesophyll conductance (g_m) is known to affect plant photosynthesis. However, g_m is rarely explicitly considered in land surface models (LSMs), with the consequence that its role in ecosystem and large‐scale carbon and water fluxes is poorly understood. In particular, the different magnitudes of g_m across plant functional types (PFTs) are expected to cause spatially divergent vegetation responses to elevated CO₂ concentrations. Here, an extensive literature compilation of g_m across major vegetation types is used to parameterize an empirical model of g_m in the LSM JSBACH and to adjust photosynthetic parameters based on simulated A_n ? C_i curves. We demonstrate that an explicit representation of g_m changes the response of photosynthesis to environmental factors, which cannot be entirely compensated by adjusting photosynthetic parameters. These altered responses lead to changes in the photosynthetic sensitivity to atmospheric CO₂ concentrations which depend both on the magnitude of g_m and the climatic conditions, particularly temperature. We then conducted simulations under ambient and elevated (ambient + 200 μmol/mol) CO₂ concentrations for contrasting ecosystems and for historical and anticipated future climate conditions (representative concentration pathways; RCPs) globally. The g_m‐explicit simulations using the RCP8.5 scenario resulted in significantly higher increases in gross primary productivity (GPP) in high latitudes (+10% to + 25%), intermediate increases in temperate regions (+5% to + 15%), and slightly lower to moderately higher responses in tropical regions (?2% to +5%), which summed up to moderate GPP increases globally. Similar patterns were found for transpiration, but with a lower magnitude. Our results suggest that the effect of an explicit representation of g_m is most important for simulated carbon and water fluxes in the boreal zone, where a cold climate coincides with evergreen vegetation.     

Elevated CO2 effects on mesophyll conductance and its consequences for interpreting photosynthetic physiology

Mesophyll conductance (g_m) generally correlates with photosynthetic capacity, although the causal relationship between the two is unclear. The response of g_m to various CO₂ regimes was measured to determine its relationship to environmental changes that affect photosynthesis. The overall effect of CO₂ growth environment on g_m was species and experiment dependent. The data did not statistically differ from the previously shown A–g_m relationship and was unaffected by CO₂ treatment. The consequences of the CO₂ effect on g_m for interpreting photosynthesis in individual cases were investigated. Substantial effects of assumed versus calculated g_m on leaf properties estimated from gas‐exchange measurements were found. This differential error resulted in an underestimation in ratio of maximum carboxylation to electron transport, especially in plants with high photosynthetic capacity. Including g_m in the calculations also improved the agreement between maximum carboxylation rates and in vitro Rubisco measurements. It is concluded that g_m is finite and varies with photosynthetic capacity. Including g_m when calculating photosynthesis parameters from gas‐exchange data will avoid systematic errors.     

Photosynthetic responses of soybean (Glycine max L.) to heat‐induced electrical signalling are predominantly governed by modifications of mesophyll conductance for CO2

In recent years, the effect of heat‐induced electrical signalling on plant photosynthetic activity has been demonstrated for many plant species. However, the underlying triggers of the resulting transient inhibition of photosynthesis still remain unknown. To further investigate on this phenomenon, we focused in our present study on soybean (Glycine max L.) on the direct effect of signal transmission in the leaf mesophyll on conductance for CO₂ diffusion in the mesophyll (g_m) and detected a drastic decline in g_m following the electrical signal, whereas the photosynthetic electron transport rate (ETR) was only marginally affected. In accordance with the drop in net photosynthesis (A_N), energy dispersive X‐ray analysis (EDXA) revealed a shift of K, Mg, O and P on leaf chloroplasts. Control experiments under elevated CO₂ conditions proved the transient reduction of A_N, ETR, the chloroplast CO₂ concentration (C_c) and g_m to be independent of the external CO₂ regime, whereas the effect of the electrical signal on stomatal conductance for CO₂ (g_s) turned out much less distinctive. We therefore conclude that the effect of electrical signalling on photosynthesis in soybean is triggered by its immediate effects on g_m.     

基于FvCB模型的叶片光合生理对环境因子的响应研究进展

为提高叶片光合速率并更好地理解叶片光合生理对环境因子变化的响应机制,FvCB模型(C_3植物光合生化模型)常用于分析不同环境条件下CO_2响应曲线并预测叶片活体内光合系统的内在变化状况。系统介绍了FvCB模型的建立、发展过程和拟合方法等基本理论,综述了该模型在叶片光合生理对光、CO_2、水、温度和N营养等环境因子变化的响应机制中的应用研究。为进一步完善FvCB模型并更好地理解叶片活体内光合系统对环境因子变化的响应机制,未来拟加强以下研究:1)羧化速率与光合电子传递速率之间的联系;2)叶肉导度的具体组分及其对FvCB模型参数估计的影响;3)叶片气孔导度和叶肉导度对环境因子变化的调控机制。     

Coupled response of stomatal and mesophyll conductance to light enhances photosynthesis of shade leaves under sunflecks

Light gradients within tree canopies play a major role in the distribution of plant resources that define the photosynthetic capacity of sun and shade leaves. However, the biochemical and diffusional constraints on gas exchange in sun and shade leaves in response to light remain poorly quantified, but critical for predicting canopy carbon and water exchange. To investigate the CO₂ diffusion pathway of sun and shade leaves, leaf gas exchange was coupled with concurrent measurements of carbon isotope discrimination to measure net leaf photosynthesis (A_n), stomatal conductance (g_s) and mesophyll conductance (g_m) in Eucalyptus tereticornis trees grown in climate controlled whole‐tree chambers. Compared to sun leaves, shade leaves had lower A_n, g_m, leaf nitrogen and photosynthetic capacity (A_max) but g_s was similar. When light intensity was temporarily increased for shade leaves to match that of sun leaves, both g_s and g_m increased, and A_n increased to values greater than sun leaves. We show that dynamic physiological responses of shade leaves to altered light environments have implications for up‐scaling leaf level measurements and predicting whole canopy carbon gain. Despite exhibiting reduced photosynthetic capacity, the rapid up‐regulation of g_m with increased light enables shade leaves to respond quickly to sunflecks.     

Using tunable diode laser spectroscopy to measure carbon isotope discrimination and mesophyll conductance to CO₂ diffusion dynamically at different CO₂ concentrations

In C₃ leaves, the mesophyll conductance to CO₂ diffusion, g_m, determines the drawdown in CO₂ concentration from intercellular airspace to the chloroplast stroma. Both g_m and stomatal conductance limit photosynthetic rate and vary in response to the environment. We investigated the response of g_m to changes in CO₂ in two Arabidopsis genotypes (including a mutant with open stomata, ost1), tobacco and wheat. We combined measurements of gas exchange with carbon isotope discrimination using tunable diode laser absorption spectroscopy with a CO₂ calibration system specially designed for a range of CO₂ and O₂ concentrations. CO₂ was initially increased from 200 to 1000 ppm and then decreased stepwise to 200 ppm and increased stepwise back to 1000 ppm, or the sequence was reversed. In 2% O₂ a step increase from 200 to 1000 ppm significantly decreased g_m by 26–40% in all three species, whereas following a step decrease from 1000 to 200 ppm, the 26–38% increase in g_m was not statistically significant. The response of g_m to CO₂ was less in 21% O₂. Comparing wild type against the ost1 revealed that mesophyll and stomatal conductance varied independently in response to CO₂. We discuss the effects of isotope fractionation factors on estimating g_m.     

Abscisic Acid Induces Rapid Reductions in Mesophyll Conductance to Carbon Dioxide

The rate of photosynthesis (A) of plants exposed to water deficit is a function of stomatal (g_s) and mesophyll (g_m) conductance determining the availability of CO₂ at the site of carboxylation within the chloroplast. Mesophyll conductance often represents the greatest impediment to photosynthetic uptake of CO₂, and a crucial determinant of the photosynthetic effects of drought. Abscisic acid (ABA) plays a fundamental role in signalling and co-ordination of plant responses to drought; however, the effect of ABA on g_m is not well-defined. Rose, cherry, olive and poplar were exposed to exogenous ABA and their leaf gas exchange parameters recorded over a four hour period. Application with ABA induced reductions in values of A, g_s and g_m in all four species. Reduced g_m occurred within one hour of ABA treatment in three of the four analysed species; indicating that the effect of ABA on g_m occurs on a shorter timescale than previously considered. These declines in g_m values associated with ABA were not the result of physical changes in leaf properties due to altered turgor affecting movement of CO₂, or caused by a reduction in the sub-stomatal concentration of CO₂ (C_i). Increased [ABA] likely induces biochemical changes in the properties of the interface between the sub-stomatal air-space and mesophyll layer through the actions of cooporins to regulate the transport of CO₂. The results of this study provide further evidence that g_m is highly responsive to fluctuations in the external environment, and stress signals such as ABA induce co-ordinated modifications of both g_s and g_m in the regulation of photosynthesis.     

Phosphoglycerate dehydrogenase from soybean nodules : partial purification and some kinetic properties

The relationship between single leaf photosynthesis and conductance was examined in cotton (Gossypium hirsutum L.) across a range of environmental conditions. The purpose of this research was to separate and define the degree of stomatal and nonstomatal limitations in the photosynthetic process of field-grown cotton.

Photosynthetic rates were related to leaf conductance of upper canopy leaves in a curvilinear manner. Increases in leaf conductance of CO₂ in excess of 0.3 to 0.4 mole per square meter per second did not result in significant increases in gross or net photosynthetic rates. No tight coupling between environmental influences on photosynthetic rates and those affecting conductance levels was evident, since photosynthesis per unit leaf conductance did not remain constant. Slowly developing water stress caused greater reductions in photosynthesis than in leaf conductance, indicating nonstomatal limitations of photosynthesis.

Increases in external CO₂ concentration to levels above ambient did not produce proportional increases in photosynthesis even though substomatal or intercellular CO₂ concentration increased. The lack of a linear increase in photosynthetic rate in response to increases in leaf conductance and in response to increases in external CO₂ concentration demonstrated that nonstomatal factors are major photosynthetic rate determinants of cotton under field conditions.

     

Drought‐introduced variability of mesophyll conductance in Gossypium and its relationship with leaf anatomy

Mesophyll conductance (g_m) is one of the major determinants of photosynthetic rate, for which it has an impact on crop yield. However, the regulatory mechanisms behind the decline in g_m of cotton (Gossypium. spp) by drought are unclear. An upland cotton (Gossypium hirsutum) genotype and a pima cotton (Gossypium barbadense) genotype were used to determine the gas exchange parameters, leaf anatomical structure as well as aquaporin and carbonic anhydrase gene expression under well‐watered and drought treatment conditions. In this study, the decrease of net photosynthetic rate (A_N) under drought conditions was related to a decline in g_m and in stomatal conductance (g_s). g_m and g_s coordinate with each other to ensure optimum state of CO₂ diffusion and achieve the balance of water and CO₂ demand in the process of photosynthesis. Meanwhile, mesophyll limitations to photosynthesis are equally important to the stomatal limitations. Considering g_m, its decline in cotton leaves under drought was mostly regulated by the chloroplast surface area exposed to leaf intercellular air spaces per leaf area (S_c/S) and might also be regulated by the expression of leaf CARBONIC ANHYDRASE (CA1). Meanwhile, cotton leaves can minimize the decrease in g_m under drought by maintaining cell wall thickness (T_cw). Our results indicated that modification of chloroplasts might be a target trait in future attempts to improve cotton drought tolerance.     

Rapid responses of mesophyll conductance to changes of CO2 concentration,temperature and irradiance are affected by N supplements in rice

Photosynthesis in C₃ plants is significantly limited by mesophyll conductance (g_m), which can vary with leaf anatomical traits and nitrogen (N) supplements. Several studies have investigated the response of g_m to N supplements; however, none examined the implications of N supplements on the response of g_m to rapid environmental changes. Here we investigated the effect of N supplement on g_m and the response of g_m to change of CO₂, temperature and irradiance in rice. High N supplement (HN) increased mesophyll cell wall surface area and chloroplast surface area exposed to intercellular airspace per leaf area, and reduced cell wall thickness. These changes resulted in increased g_m. The g_m of leaves with HN was more sensitive to changes in CO₂ concentration, temperature and irradiance. The difference in leaf structural features between low N supplement and HN indicates that a rapid change in g_m is related to the regulation of diffusion through biological membranes rather than leaf structural features. These results will contribute to an understanding of the determinants of g_m response to rapid changes in environmental factors.     

New insights into the cellular mechanisms of plant growth at elevated atmospheric carbon dioxide concentrations

Rising atmospheric carbon dioxide concentration ([CO₂]) significantly influences plant growth, development, and biomass. Increased photosynthesis rate, together with lower stomatal conductance, has been identified as the key factors that stimulate plant growth at elevated [CO₂] (e[CO₂]). However, variations in photosynthesis and stomatal conductance alone cannot fully explain the dynamic changes in plant growth. Stimulation of photosynthesis at e[CO₂] is always associated with post‐photosynthetic secondary metabolic processes that include carbon and nitrogen metabolism, cell cycle functions, and hormonal regulation. Most studies have focused on photosynthesis and stomatal conductance in response to e[CO₂], despite the emerging evidence of e[CO₂]'s role in moderating secondary metabolism in plants. In this review, we briefly discuss the effects of e[CO₂] on photosynthesis and stomatal conductance and then focus on the changes in other cellular mechanisms and growth processes at e[CO₂] in relation to plant growth and development. Finally, knowledge gaps in understanding plant growth responses to e[CO₂] have been identified with the aim of improving crop productivity under a CO₂ rich atmosphere.     

Variations in leaf anatomical characteristics drive the decrease of mesophyll conductance in poplar under elevated ozone

Decline in mesophyll conductance (g_m) plays a key role in limiting photosynthesis in plants exposed to elevated ozone (O₃). Leaf anatomical traits are known to influence g_m, but the potential effects of O₃-induced changes in leaf anatomy on g_m have not yet been clarified. Here, two poplar clones were exposed to elevated O₃. The effects of O₃ on the photosynthetic capacity and anatomical characteristics were assessed to investigate the leaf anatomical properties that potentially affect g_m. We also conducted global meta-analysis to explore the general response patterns of g_m and leaf anatomy to O₃ exposure. We found that the O₃-induced reduction in g_m was critical in limiting leaf photosynthesis. Changes in liquid-phase conductance rather than gas-phase conductance drive the decline in g_m under elevated O_3, and this effect was associated with thicker cell walls and smaller chloroplast sizes. The effects of O₃ on palisade and spongy mesophyll cell traits and their contributions to g_m were highly genotype-dependent. Our results suggest that, while anatomical adjustments under elevated O₃ may contribute to defense against O₃ stress, they also cause declines in g_m and photosynthesis. These results provide the first evidence of anatomical constraints on g_m under elevated O₃.     

Light-harvesting in photosystem I

Improving Rubisco catalysis is considered a promising way to enhance C₃-photosynthesis and photosynthetic water use efficiency (WUE) provided the introduced changes have little or no impact on other processes affecting photosynthesis such as leaf photochemistry or leaf CO₂ diffusion conductances. However, the extent to which the factors affecting photosynthetic capacity are co-regulated is unclear. The aim of the present study was to characterize the photochemistry and CO₂ transport processes in the leaves of three transplantomic tobacco genotypes expressing hybrid Rubisco isoforms comprising different Flaveria L-subunits that show variations in catalysis and differing trade-offs between the amount of Rubisco and its activation state. Stomatal conductance (g _s) in each transplantomic tobacco line matched wild-type, while their photochemistry showed co-regulation with the variations in Rubisco catalysis. A tight co-regulation was observed between Rubisco activity and mesophyll conductance (g _m) that was independent of g _s thus producing plants with varying g _m/g _s ratios. Since the g _m/g _s ratio has been shown to positively correlate with intrinsic WUE, the present results suggest that altering photosynthesis by modifying Rubisco catalysis may also be useful for targeting WUE.     

Morphological and anatomical determinants of mesophyll conductance in wild relatives of tomato (Solanum sect. Lycopersicon,sect. Lycopersicoides; Solanaceae)

Natural selection on photosynthetic performance is a primary factor determining leaf phenotypes. The complex CO₂ diffusion path from substomatal cavities to the chloroplasts – the mesophyll conductance (g_m) – limits photosynthetic rate in many species and hence shapes variation in leaf morphology and anatomy. Among sclerophyllous and succulent taxa, structural investment in leaves, measured as the leaf dry mass per area (LMA), has been implicated in decreased g_m. However, in herbaceous taxa with high g_m, it is less certain how LMA impacts CO₂ diffusion and whether it significantly affects photosynthetic performance. We addressed these questions in the context of understanding the ecophysiological significance of leaf trait variation in wild tomatoes, a closely related group of herbaceous perennials. Although g_m was high in wild tomatoes, variation in g_m significantly affected photosynthesis. Even in these tender‐leaved herbaceous species, greater LMA led to reduced g_m. This relationship between g_m and LMA is partially mediated by cell packing and leaf thickness, although amphistomy (equal distribution of stomata on both sides of the leaf) mitigates the effect of leaf thickness. Understanding the costs of increased LMA will inform future work on the adaptive significance of leaf trait variation across ecological gradients in wild tomatoes and other systems.     

Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana: comparisons to Nicotiana tabacum

Biochemical models are used to predict and understand the response of photosynthesis to rising temperatures and CO₂ partial pressures. These models require the temperature dependency of ribulose‐1,5‐bisphosphate carboxylase/oxygenase (Rubisco) kinetics and mesophyll conductance to CO₂ (g_m). However, it is not known how the temperature response of Rubisco kinetics differs between species, and comprehensive in vivo Rubisco kinetics that include g_m have only been determined in the warm‐adapted Nicotiana tabacum. Here, we measured the temperature response of Rubisco kinetics and g_m in N. tabacum and the cold‐adapted Arabidopsis thaliana using gas exchange and ¹³CO₂ isotopic discrimination on plants with genetically reduced levels of Rubisco. While the individual Rubisco kinetic parameters in N. tabacum and A. thaliana were similar across temperatures, they collectively resulted in significantly different modelled rates of photosynthesis. Additionally, g_m increased with temperature in N. tabacum but not in A. thaliana. These findings highlight the importance of considering species‐dependent differences in Rubisco kinetics and g_m when modelling the temperature response of photosynthesis.     

A coupled model of photosynthesis-transpiration based on the stomatal behavior for maize (Zea mays L.) grown in the field

The study presents a theoretical basis of a stomatal behavior-based coupled model for estimating photosynthesis, A, and transpiration, E. Outputs of the model were tested against data observed in a maize (Zea mays L.) field. The model was developed by introducing the internal conductance, g _ic, to CO₂ assimilation, and the general equation of stomatal conductance, g _sw, to H₂O diffusion, into models of CO₂ and H₂O diffusion through the stomata of plant leaves. The coupled model is easier for practical use since the model only includes environmental variables, such as ambient CO₂ concentration, leaf temperature, humidity and photosynthetic photon flux received at the leaves within the canopy. Moreover, concept of g _ic, and factors controlling A and E were discussed, and applicability of the model was examined with the data collected in the maize field.     

Leaf anatomy does not explain apparent short‐term responses of mesophyll conductance to light and CO2 in tobacco

Mesophyll conductance to CO₂ (g_m), a key photosynthetic trait, is strongly constrained by leaf anatomy. Leaf anatomical parameters such as cell wall thickness and chloroplast area exposed to the mesophyll intercellular airspace have been demonstrated to determine g_m in species with diverging phylogeny, leaf structure and ontogeny. However, the potential implication of leaf anatomy, especially chloroplast movement, on the short‐term response of g_m to rapid changes (i.e. seconds to minutes) under different environmental conditions (CO₂, light or temperature) has not been examined. The aim of this study was to determine whether the observed rapid variations of g_m in response to variations of light and CO₂ could be explained by changes in any leaf anatomical arrangements. When compared to high light and ambient CO₂, the values of g_m estimated by chlorophyll fluorescence decreased under high CO₂ and increased at low CO₂, while it decreased with decreasing light. Nevertheless, no changes in anatomical parameters, including chloroplast distribution, were found. Hence, the g_m estimated by analytical models based on anatomical parameters was constant under varying light and CO₂. Considering this discrepancy between anatomy and chlorophyll fluorescence estimates, it is concluded that apparent fast g_m variations should be due to artefacts in its estimation and/or to changes in the biochemical components acting on diffusional properties of the leaf (e.g. aquaporins and carbonic anhydrase).     

Disentangling the contributions of ontogeny and water stress to photosynthetic limitations in almond trees

Very few studies have attempted to disentangle the respective role of ontogeny and water stress on leaf photosynthetic attributes. The relative significance of both effects on photosynthetic attributes has been investigated in leaves of field‐grown almond trees [Prunus dulcis (Mill.) D. A. Webb] during four growth cycles. Leaf ontogeny resulted in enhanced leaf dry weight per unit area (W_a), greater leaf dry‐to‐fresh weight ratio and lower N content per unit of leaf dry weight (N_w). Concomitantly, area‐based maximum carboxylation rate (V_cmax), maximum electron transport rate (J_max), mesophyll conductance to CO₂ diffusion (gm)′ and light‐saturated net photosynthesis (A_max) declined in both well‐watered and water‐stressed almond leaves. Although g_m and stomatal conductance (g_s) seemed to be co‐ordinated, a much stronger coordination in response to ontogeny and prolonged water stress was observed between g_m and the leaf photosynthetic capacity. Under unrestricted water supply, the leaf age‐related decline of A_max was equally driven by diffusional and biochemical limitations. Under restricted soil water availability, A_max was mainly limited by g_s and, to a lesser extent, by photosynthetic capacity and g_m. When both ontogeny and water stress effects were combined, diffusional limitations was the main determinant of photosynthesis limitation, while stomatal and biochemical limitations contributed similarly.     

The apoplastic antioxidant system and altered cell wall dynamics influence mesophyll conductance and the rate of photosynthesis

Mesophyll conductance (g_m), the diffusion of CO₂ from substomatal cavities to the carboxylation sites in the chloroplasts, is a highly complex trait driving photosynthesis (net CO₂ assimilation, A_N). However, little is known concerning the mechanisms by which it is dynamically regulated. The apoplast is considered as a ‘key information bridge’ between the environment and cells. Interestingly, most of the environmental constraints affecting g_m also cause apoplastic responses, cell wall (CW) alterations and metabolic rearrangements. Since CW thickness is a key determinant of g_m, we hypothesize that other changes in this cellular compartiment should also influence g_m. We study the relationship between the antioxidant apoplastic system and CW metabolism and the g_m responses in tobacco plants (Nicotiana sylvestris L.) under two abiotic stresses (drought and salinity), combining in vivo gas‐exchange measurements with analyses of antioxidant activities, CW composition and primary metabolism. Stress treatments imposed substantial reductions in A_N (58–54%) and g_m (59%), accompanied by a strong antioxidant enzymatic response at the apoplastic and symplastic levels. Interestingly, apoplastic but not symplastic peroxidases were positively related to g_m. Leaf anatomy remained mostly stable; however, the stress treatments significantly affected the CW composition, specifically pectins, which showed significant relationships with A_N and g_m. The treatments additionally promoted a differential primary metabolic response, and specific CW‐related metabolites including galactose, glucosamine and hydroxycinnamate showed exclusive relationships with g_m independent of the stress. These results suggest that g_m responses can be attributed to specific changes in the apoplastic antioxidant system and CW metabolism, opening up more possibilities for improving photosynthesis using breeding/biotechnological strategies.     

Variable mesophyll conductance revisited: theoretical background and experimental implications

The CO₂ concentration at the site of carboxylation inside the chloroplast stroma depends not only on the stomatal conductance, but also on the conductance of CO₂ between substomatal cavities and the site of CO₂ fixation. This conductance, commonly termed mesophyll conductance (g_m), significantly constrains the rate of photosynthesis. Here we show that estimates of g_m are influenced by the amount of respiratory and photorespiratory CO₂ from the mitochondria diffusing towards the chloroplasts. This results in an apparent CO₂ and oxygen sensitivity of g_m that does not imply a change in intrinsic diffusion properties of the mesophyll, but depends on the ratio of mitochondrial CO₂ release to chloroplast CO₂ uptake. We show that this effect (1) can bias the estimation of the CO₂ photocompensation point and non‐photorespiratory respiration in the light; (2) can affect the estimates of ribulose 1·5‐bisphosphate carboxylase/oxygenase (Rubisco) kinetic constants in vivo; and (3) results in an apparent obligatory correlation between stomatal conductance and g_m. We further show that the amount of photo(respiratory) CO₂ that is refixed by Rubisco can be directly estimated through measurements of g_m.