Mesophyll Conductance Research Articles

Dynamic changes in cell wall composition of mature sunflower leaves under distinct water regimes affect photosynthesis.

In previous work, we identified that exposure to limited water availability induced changes in cell wall composition of mature Helianthus annuus L. leaves that affected mesophyll conductance to CO2 diffusion (gm). However, it is unclear on which timescale these changes in cell wall composition occurred. Here, we subjected H. annuus to control (i.e. water availability), different levels of short-term water deficit stress (ST), long-term water deficit stress (LT), and long-term water deficit stress followed by gradual recoveries addressed at different timescales (LT-Rec) to evaluate the dynamics of modifications in the main composition of cell wall (cellulose, hemicelluloses, pectins and lignins) affecting photosynthesis. During gradual ST treatments, pectins enhancement was associated with gm decline. However, during LT-Rec, pectins content decreased significantly after only 5 h, while hemicelluloses and lignins amounts changed after 24 h, all being uncoupled from gm. Surprisingly, lignins increased by around 200% compared with control and were related to stomatal conductance to gas diffusion (gs) during LT-Rec. Although we suspect that the accuracy of the protocols to determine cell wall composition should be re-evaluated, we demonstrate for the first time that a highly dynamic cell wall composition turnover differently affects photosynthesis in plants subjected to distinct water regimes.

Adjustments in photosynthesis and leaf water relations are related to changes in cell wall composition in Hordeum vulgare and Triticum aestivum subjected to water deficit stress

In the current climate change scenario, understanding crops’ physiological performance under water shortage is crucial to overcome drought periods. Although the implication of leaf water relations maintaining leaf turgor and stomatal functioning under water deprivation has been suggested, the relationships between photosynthesis and osmotic and elastic adjustments remain misunderstood. Similarly, only few studies in dicotyledonous analysed how changes in cell wall composition affected photosynthesis and leaf water relations under drought. To induce modifications in photosynthesis, leaf water relations and cell wall composition, Hordeum vulgare and Triticum aestivum were subjected to different water regimes: control (CL, full irrigation), moderate and severe water deficit stress (Mod WS and Sev WS, respectively). Water shortage decreased photosynthesis mainly due to stomatal conductance (gs) declines, being accompanied by reduced osmotic potential at full turgor (πo) and increased bulk modulus of elasticity (ε). Whereas both species enhanced pectins when intensifying water deprivation, species-dependent adjustments occurred for cellulose and hemicelluloses. From these results, we showed that πo and ε influenced photosynthesis, particularly, gs. Furthermore, the (Cellulose+Hemicelluloses)/Pectins ratio determined ε and mesophyll conductance (gm) in grasses, presenting the lowest pectins content within angiosperms. Thus, we highlight the relevance of cell wall composition regulating grasses physiology during drought acclimation.

Mesophyll conductance modulates photosynthetic rate in cotton crops exposed to heat stress under field conditions

AbstractCotton is often exposed to high temperatures during the reproductive stage, which can negatively affect its productivity. The objectives were to: i) test whether heat stress impacts during the reproductive stage on photosynthesis are due to instant temperature effects or to acclimation produced during the heat stress period, ii) evaluate the role of stomatal and mesophyll conductance on net photosynthetic rate and iii) identify possible interactions between heat stress and different source/sink ratios during the reproductive period. Two field experiments were carried out in 2016 (Exp. 1) and 2017 (Exp. 2). Two heating treatment periods were imposed as follows: pre‐flowering between 15 days before flower bud and flowering (H1) and post‐flowering between flowering and 15 days later (H2). Each treatment had a control group (C1 and C2, respectively). In Exp. 1, two genotypes with contrasting crop cycles were compared. In Exp. 2, 50% defoliated plants (D‐) were compared with intact plants (D+) under the same temperature treatments using one genotype. Average daily maximum temperature of heated treatments for both experiments was 37.9 ± 0.79ºC, 5.8ºC higher than the controls. Independently of the period, thermal stress had a negative impact on photosynthesis in both genotypes through an acclimation response, reducing it up to 35% compared with controls when heath‐stressed and control plants were measured at the same temperature. Instant responses to temperature were not observed. This decrease was mainly determined by mesophyll conductance, and no recovery was observed 15 days after the end of treatments. Photosynthesis depletion was conditioned by the source/sink ratio, showing a complete recovery only in defoliated plants. It is concluded that thermal stress had a negative acclimation impact on photosynthesis, without responses to changes in instant temperature, and this acclimation is modulated mainly by mesophyll conductance.

Mesophyll conductance variability of rice aquaporin knockout lines at different growth stages and growing environments.

The plasma membrane subfamily of aquaporins [plasma membrane intrinsic proteins (PIPs)], which facilitates the CO2 diffusion across membranes, is proposed to play an important role in mesophyll conductance to CO2 (gm ), a major limiting factor of photosynthesis. However, recent studies implied no causal relationship between gm and PIPs because they failed to repeat the previous observed differences in gm between PIP knockout lines and their wild-type. The contrasting results on the role of PIPs in gm were interpreted as the different growth conditions among studies, which has never been tested. Here, we assessed whether the differences in gm between wild-type and PIP knockout lines, Ospip1;1, Ospip1;2 and Ospip2;1, varied with growth condition (field versus pot condition) and growth stages in rice. Under field conditions, no differences were observed in plant performance, photosynthetic rate (A) and gm between PIP knockout lines and the wild-type. However, in agreement with previous studies, two out of three knockout lines showed significant declines in tiller number, plant height, A and gm under pot conditions. Moreover, we found that the differences in A and gm between PIP knockout lines and the wild-type varied with the growth stage of the plants. Our results showed that the differences in gm between PIP knockout lines and wild-type were depending on the growth environments and stage of the plants, and further efforts are required to reveal the underlying mechanisms.

Potassium supply modulates Eucalyptus leaf water-status under PEG-induced osmotic stress: integrating leaf gas exchange, carbon and nitrogen isotopic composition and plant growth.

The objective of this study was to quantify the effect of potassium (K) supply on osmotic adjustment and drought avoidance mechanisms of Eucalyptus seedlings growing under short-term water stress. The effects of K supply on plant growth, nutritional status, leaf gas exchange parameters, leaf water potential (Ψw), leaf area (LA), stomatal density (SD), leaf carbon (C) and nitrogen (N) isotopic compositions (δ13C and δ15N ‰) and leaf C/N ratio under polyethylene glycol (PEG)-induced water deficit were measured. Under both control (non-PEG) and osmotic stress (+PEG) conditions, K supply increased plant growth, boosting dry matter yield with decreased C/N leaf ratio and δ15N ‰ values. The +PEG significantly reduced LA, plant growth, dry matter yield, Ψw, number of stomata per plant and leaf gas exchange, relative to non-PEG condition. Potassium supply alleviated osmotic-induced alterations in Eucalyptus seedlings by better regulating leaf development as well as SD, thus improving the rate of leaf gas exchange parameters, mesophyll conductance to CO2 (lower δ13C ‰ values) and water use efficiency (WUE). Consequently, K-supplied plants under drought better acclimated to osmotic stress than K-deficient plants, which in turn induced lower CO2 assimilation and dry matter yield, as well as higher leaf δ13C ‰ and δ15N ‰ values. In conclusion, management practices should seek to optimize K-nutrition to improve WUE, photosynthesis-related parameters and plant growth under water deficit conditions.

Reduced mesophyll conductance induces photosynthetic acclimation of japonica rice under elevated CO2

The foliar photosynthetic acclimation to prolonged elevated CO2 has been studied in many ways, but the quantification of photosynthetic acclimation through the limitation of stomatal conductance (gs), mesophyll conductance (gm) and biochemical capacity (Vcamx) is scarce. To quantify photosynthetic acclimation under elevated CO2, a japonica rice cultivar ‘Nanjing 9108’ was grown at two CO2 levels—ambient CO2 (a[CO2]) and a[CO2] +200 μmol mol−1 (e[CO2]) using open top chamber facility. We measured the response of net photosynthetic rate (An) to CO2 at Rubisco (Cc) at jointing, flowering and filling stages based a biochemical C3‐photosynthesis model. Measurements at the same CO2 concentration showed that the An under e[CO2] was significantly lower than that under a[CO2] at three developmental stages, suggesting the occurrence of acclimation of photosynthesis. The photosynthetic acclimation is associated with the decrease in gm, gs and Vcmax, and gm mainly limits photosynthesis. The contribution of gm, gs and Vcamx limitation to photosynthetic acclimation averaged 65 %, 25 % and 10 % of the total reduction in An. Our findings demonstrate gm is the major driver of photosynthetic acclimation and highlight the role of gm under e[CO2] in rice.

Mesophyll conductance in two cultivars of wheat grown in glacial to super-elevated CO2 concentrations.

Mesophyll conductance (gm) is an important factor limiting photosynthesis. However, gm response to long-term growth in variable [CO2] is not well understood, particularly in crop plants. Here, we grew two cultivars of wheat (Halberd and Cranbrook), known to differ in gm under current environmental conditions, in four [CO2] treatments: glacial (206 μmol mol-1), pre-industrial (344 μmol mol-1), current ambient (489 μmol mol-1), and super-elevated (1085 μmol mol-1), and two water treatments (well-watered and moderate water limitation), to develop an evolutionary and future climate perspective on gm control of photosynthesis and water-use efficiency (WUE). In the two wheat genotypes, gm increased with rising [CO2] from glacial to ambient [CO2], but declined at super-elevated [CO2]. The responses of gm to different growth [CO2] also depend on water stress; however, the specific mechanism of gm response to [CO2] remains unclear. Although gm and gm/gsc (mesophyll conductance/stomatal conductance) were strongly associated with the variability of photosynthetic rates (A) and WUE, we found that plants with higher gm may increase A without increasing gsc, which increased WUE. These results may be useful to inform plant breeding programmes and cultivar selection for Australian wheat under future environmental conditions.

Photosynthesis research under climate change.

Increasing global population and climate change uncertainties have compelled increased photosynthetic efficiency and yields to ensure food security over the coming decades. Potentially, genetic manipulation and minimization of carbon or energy losses can be ideal to boost photosynthetic efficiency or crop productivity. Despite significant efforts, limited success has been achieved. There is a need for thorough improvement in key photosynthetic limiting factors, such as stomatal conductance, mesophyll conductance, biochemical capacity combined with Rubisco, the Calvin-Benson cycle, thylakoid membrane electron transport, nonphotochemical quenching, and carbon metabolism or fixation pathways. In addition, the mechanistic basis for the enhancement in photosynthetic adaptation to environmental variables such as light intensity, temperature and elevated CO2 requires further investigation. This review sheds light on strategies to improve plant photosynthesis by targeting these intrinsic photosynthetic limitations and external environmental factors.

Mesophyll conductance, photoprotective process and optimal N partitioning are essential to the maintenance of photosynthesis at N deficient condition in a wheat yellow-green mutant (Triticum aestivum L.)

The major effect of nitrogen (N) deficiency is the inhibition on CO2 assimilation regulated by light energy absorption, transport and conversion, as well as N allocation. In this study, a yellow-green wheat mutant (Jimai5265yg) and its wild type (Jimai5265, WT) were compared between 0 mM N (N0) and 14 mM N (N14) treatments using hydroponic experiments. The mutant exhibited higher photosynthetic efficiency (An) than WT despite low chlorophyll (Chl) content in non-stressed conditions. The photosynthetic advantages of the mutant were maintained under N deficient condition. The quantitative analysis of limitations to photosynthesis revealed that CO2 diffusion associated with mesophyll conductance (gm) was the dominant limitation. Relative easiness to gain CO2 in the chloroplast contributed to the higher An of Jimai5265yg. N deficiency induced the photoinhibition of PSII, but the cyclic electron transport and photochemical activity of PSI was higher in Jimai5265yg compared to Jimai5265, which was a protective mechanism to avoid photodamage. Because of the sharp drop of An, N deficient seedlings had much lower photosynthetic N use efficiency (PNUE). However, N deficiency increased the relative content of photosynthetic N (Npsn) and decreased the relative content of storage N (Nstore). The range of change in N partitioning induced by N deficiency was smaller for Jimai5265yg compared to WT. The less insensitive to N deficiency for the mutant in terms of photosynthetic property and N partitioning suggested that gm, cyclic electron transport around PSI and more optimal N partitioning pattern is necessary to sustain photosynthesis under N deficient condition.

Updating the steady-state model of C4 photosynthesis.

C4 plants play a key role in world agriculture. For example, C4 crops such as maize and sorghum are major contributors to food production in both developed and developing countries, and the C4 grasses sugarcane, miscanthus, and switchgrass are major plant sources of bioenergy. In the challenge to manipulate and enhance C4 photosynthesis, steady-state models of leaf photosynthesis provide an important tool for gas exchange analysis and thought experiments that can explore photosynthetic pathway changes. Here a previous C4 photosynthetic model developed by von Caemmerer and Furbank has been updated with new kinetic parameterization and temperature dependencies added. The parameterization was derived from experiments on the C4 monocot, Setaria viridis, which for the first time provides a cohesive parameterization. Mesophyll conductance and its temperature dependence have also been included, as this is an important step in the quantitative correlation between the initial slope of the CO2 response curve of CO2 assimilation and in vitro phosphoenolpyruvate carboxylase activity. Furthermore, the equations for chloroplast electron transport have been updated to include cyclic electron transport flow, and equations have been added to calculate the electron transport rate from measured CO2 assimilation rates.

Leaf anatomical characteristics are less important than leaf biochemical properties in determining photosynthesis responses to nitrogen top-dressing.

The photosynthetic capacity of leaves is dramatically influenced by nitrogen (N) availability in the soil, as CO2 concentration in chloroplasts and photosynthetic biochemical capacity are related to leaf N content. The relationship between mesophyll conductance (gm) and leaf N content was expected to be shaped by leaf anatomical traits. However, the increased gm in mature leaves achieved by N top-dressing is unlikely to be caused by changes in leaf anatomy. Here, we assessed the impacts of N supply on leaf anatomical, biochemical, and photosynthetic features, specifically, the dynamic responses of leaf anatomy, biochemistry, and photosynthesis to N top-dressing in tobacco. Plant performance was substantially affected by soil N status. In comparison with the leaves of plants subjected to low N treatment, leaves of plants with high N treatment photosynthesized significantly more, due to higher CO2 diffusion conductance and photosynthetic biochemical capacity. The high gm in high N-treated leaves apparently related to modifications in the leaf anatomy; however, the rapid response of gm to N top-dressing cannot be fully explained by leaf anatomical modifications.

Stomatal and mesophyll conductance are dominant limitations to photosynthesis in response to heat stress during severe drought in a temperate and a tropical tree species

Stomatal and mesophyll conductance are dominant limitations to photosynthesis in response to heat stress during severe drought in a temperate and a tropical tree species

The Importance of Non-Diffusional Factors in Determining Photosynthesis of Two Contrasting Quinoa Ecotypes (Chenopodium quinoa Willd.) Subjected to Salinity Conditions.

The broad distribution of quinoa in saline and non-saline environments is reflected in variations in the photosynthesis-associated mechanisms of different ecotypes. The aim of this study was to characterize the photosynthetic response to high salinity (0.4 M NaCl) of two contrasting Chilean genotypes, Amarilla (salt-tolerant, salares ecotype) and Hueque (salt-sensitive, coastal ecotype). Our results show that saline stress induced a significant decrease in the K+/Na+ ratio in roots and an increase in glycine betaine in leaves, particularly in the sensitive genotype (Hueque). Measurement of the photosynthesis-related parameters showed that maximum CO2 assimilation (Amax) in control plants was comparable between genotypes (ca. 9–10 μmol CO2 m−2 s−1). However, salt treatment produced different responses, with Amax values decreasing by 65.1% in the sensitive ecotype and 37.7% in the tolerant one. Although both genotypes maintained mesophyll conductance when stomatal restrictions were removed, the biochemical components of Amarilla were impaired to a lesser extent under salt stress conditions: for example, the maximum rate of ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO; Vcmax) was not as affected in Amarilla, revealing that this enzyme has a higher affinity for its substrate in this genotype and, thus, a better carboxylation efficiency. The present results show that the higher salinity tolerance of Amarilla was also due to its ability to control non-diffusional components, indicating its superior photosynthetic capacity compared to Hueque, particularly under salt stress conditions.

The contribution of PIP2-type aquaporins to photosynthetic response to increased vapour pressure deficit.

The roles of different plasma membrane aquaporins (PIPs) in leaf-level gas exchange of Arabidopsis thaliana were examined using knockout mutants. Since multiple Arabidopsis PIPs are implicated in CO2 transport across cell membranes, we focused on identifying the effects of the knockout mutations on photosynthesis, and whether they are mediated through the control of stomatal conductance of water vapour (gs), mesophyll conductance of CO2 (gm), or both. We grew Arabidopsis plants in low and high humidity environments and found that the contribution of PIPs to gs was larger under low air humidity when the evaporative demand was high, whereas any effect of a lack of PIP function was minimal under higher humidity. The pip2;4 knockout mutant had 44% higher gs than wild-type plants under low humidity, which in turn resulted in an increased net photosynthetic rate (Anet). We also observed a 23% increase in whole-plant transpiration (E) for this knockout mutant. The lack of functional plasma membrane aquaporin AtPIP2;5 did not affect gs or E, but resulted in homeostasis of gm despite changes in humidity, indicating a possible role in regulating CO2 membrane permeability. CO2 transport measurements in yeast expressing AtPIP2;5 confirmed that this aquaporin is indeed permeable to CO2.

Role of Hydraulic Signal and ABA in Decrease of Leaf Stomatal and Mesophyll Conductance in Soil Drought-Stressed Tomato.

Drought reduces leaf stomatal conductance (gs) and mesophyll conductance (gm). Both hydraulic signals and chemical signals (mainly abscisic acid, ABA) are involved in regulating gs. However, it remains unclear what role the endogenous ABA plays in gm under decreasing soil moisture. In this study, the responses of gs and gm to ABA were investigated under progressive soil drying conditions and their impacts on net photosynthesis (An) and intrinsic water use efficiency (WUEi) were also analyzed. Experimental tomato plants were cultivated in pots in an environment-controlled greenhouse. Reductions of gs and gm induced a 68–78% decline of An under drought conditions. While soil water potential (Ψsoil) was over −1.01 MPa, gs reduced as leaf water potential (Ψleaf) decreased, but ABA and gm kept unchanged, which indicating gs was more sensitive to drought than gm. During Ψsoil reduction from −1.01 to −1.44 MPa, Ψleaf still kept decreasing, and both gs and gm decreased concurrently following to the sustained increases of ABA content in shoot sap. The gm was positively correlated to gs during a drying process. Compared to gs or gm, WUEi was strongly correlated with gm/gs. WUEi improved within Ψsoil range between −0.83 and −1.15 MPa. In summary, gs showed a higher sensitivity to drought than gm. Under moderate and severe drought at Ψsoil ≤ −1.01 MPa, furthermore from hydraulic signals, ABA was also involved in this co-ordination reductions of gs and gm and thereby regulated An and WUEi.

Engineering of Crassulacean Acid Metabolism.

Crassulacean acid metabolism (CAM) has evolved from a C3 ground state to increase water use efficiency of photosynthesis. During CAM evolution, selective pressures altered the abundance and expression patterns of C3 genes and their regulators to enable the trait. The circadian pattern of CO2 fixation and the stomatal opening pattern observed in CAM can be explained largely with a regulatory architecture already present in C3 plants. The metabolic CAM cycle relies on enzymes and transporters that exist in C3 plants and requires tight regulatory control to avoid futile cycles between carboxylation and decarboxylation. Ecological observations and modeling point to mesophyll conductance as a major factor during CAM evolution. The present state of knowledge enables suggestions for genes for a minimal CAM cycle for proof-of-concept engineering, assuming altered regulation of starch synthesis and degradation are not critical elements of CAM photosynthesis and sufficient malic acid export from the vacuole is possible.

Acclimation of mesophyll conductance and anatomy to light during leaf aging in Arabidopsis thaliana.

Mesophyll conductance (gm ), a key limitation to photosynthesis, is strongly driven by leaf anatomy, which is in turn influenced by environmental growth conditions and ontogeny. However, studies examining the combined environment × age effect on both leaf anatomy and photosynthesis are scarce, and none have been carried out in short-lived plants. Here, we studied the variation of photosynthesis and leaf anatomy in the model species Arabidopsis thaliana (Col-0) grown under three different light intensities at two different leaf ages. We found that light × age interaction was significant for photosynthesis but not for anatomical characteristics. Increasing growth light intensities resulted in increases in leaf mass per area, thickness, number of palisade cell layers, and chloroplast area lining to intercellular airspace. Low and moderate-but not high-light intensity had a significant effect on all photosynthetic characteristics. Leaf aging was associated with increases in cell wall thickness (Tcw ) in all light treatments and in increases in leaf thickness in plants grown under low and moderate light intensities. However, gm did not vary with leaf aging, and photosynthesis only decreased with leaf age under moderate and high light, suggesting a compensatory effect between increased Tcw and decreased chloroplast thickness on the total CO2 diffusion resistance.

Cell wall thickness and composition are involved in photosynthetic limitation.

The key role of cell walls in setting mesophyll conductance to CO2 (gm) and, consequently, photosynthesis is reviewed. First, the theoretical properties of cell walls that can affect gm are presented. Then, we focus on cell wall thickness (Tcw) reviewing empirical evidence showing that Tcw varies strongly among species and phylogenetic groups in a way that correlates with gm and photosynthesis; that is, the thicker the mesophyll cell walls, the lower the gm and photosynthesis. Potential interplays of gm, Tcw, dehydration tolerance, and hydraulic properties of leaves are also discussed. Dynamic variations of Tcw in response to the environment and their implications in the regulation of photosynthesis are discussed, and recent evidence suggesting an influence of cell wall composition on gm is presented. We then propose a hypothetical mechanism for the influence of cell walls on photosynthesis, combining the effects of thickness and composition, particularly pectins. Finally, we discuss the prospects for using biotechnology for enhancing photosynthesis by altering cell wall-related genes.

Differences in leaf anatomy determines temperature response of leaf hydraulic and mesophyll CO2 conductance in phylogenetically related C4 and C3 grass species.

Leaf hydraulic and mesophyll CO2 conductance are both influenced by leaf anatomical traits, however it is poorly understood how the temperature response of these conductances differs between C4 and C3 species with distinct leaf anatomy. This study investigated the temperature response of leaf hydraulic conductance (Kleaf ), stomatal (gs ) and mesophyll (gm ) conductance to CO2 , and leaf anatomical traits in phylogenetically related Panicum antidotale (C4 ) and P.bisulcatum (C3 ) grasses. The C4 species had lower hydraulic conductance outside xylem (Kox ) and Kleaf compared with the C3 species. However, the C4 species had higher gm compared with the C3 species. Traits associated with leaf water movement, Kleaf and Kox , increased with temperature more in the C3 than in the C4 species, whereas traits related to carbon uptake, Anet and gm , increased more with temperature in the C4 than the C3 species. Our findings demonstrate that, in addition to a CO2 concentrating mechanism, outside-xylem leaf anatomy in the C4 species P.antidotale favours lower water movement through the leaf and stomata that provides an additional advantage for greater leaf carbon uptake relative to water loss with increasing leaf temperature than in the C3 species P.bisulcatum.

Effects of the interaction between vapor-pressure deficit and potassium on the photosynthesis system of tomato seedlings under low temperature

Both vapour pressure deficit (VPD) and potassium (K) have been widely studied in regulating leaf photosynthesis and plant growth. A close correlation between VPD and plant nutrient absorption has also been observed for diverse plant species under various environmental conditions. However, the interactive effect of VPD and K on plant photosynthesis remains unclear, especially at low temperatures. Here, we investigated the role of VPD in plant K uptake and the effects of VPD × K on plant photosynthesis system under chilling stress. Plants were subjected to different levels of K nutrient solution supply (2, 4, 8 mmol/L) with contrasting VPD levels (high vs. low). Compared to high VPD, low VPD increased plant transpiration, but there was no significant difference in leaf K content between different VPD treatments; K accumulation under low VPD increased significantly, which can be partly attributed to enhanced biomass production. Meanwhile, an increase in stomatal density and size occurred under low VPD conditions. Stomatal conductance and mesophyll conductance tended to increase with K level under low VPD condition, which was beneficial to the diffusion of carbon dioxide and thus increased photosynthesis. In terms of photosynthetic performance, low VPD and elevated K increased the utilization of light energy and reduced heat dissipation, which specifically manifested as up-regulated photosynthetic pigment content and chlorophyll fluorescence parameters and down-regulated Car/Chl ratio, NPQ, and ROS content. In summary, reducing VPD and adding K promoted photosynthetic performance and can alleviate the low-temperature stress of tomato plants.