Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study

Ferns are thought to have lower photosynthetic rates than angiosperms and they lack fine stomatal regulation. However, no study has directly compared photosynthesis in plants of both groups grown under optimal conditions in a common environment. We present a common garden comparison of seven angiosperms and seven ferns paired by habitat preference, with the aims of (1) confirming that ferns do have lower photosynthesis capacity than angiosperms and quantifying these differences; (2) determining the importance of diffusional versus biochemical limitations; and (3) analysing the potential implication of leaf anatomical traits in setting the photosynthesis capacity in both groups. On average, the photosynthetic rate of ferns was about half that of angiosperms, and they exhibited lower stomatal and mesophyll conductance to CO₂ (g_m), maximum velocity of carboxylation and electron transport rate. A quantitative limitation analysis revealed that stomatal and mesophyll conductances were co‐responsible for the lower photosynthesis of ferns as compared with angiosperms. However, g_m alone was the most constraining factor for photosynthesis in ferns. Consistently, leaf anatomy showed important differences between angiosperms and ferns, especially in cell wall thickness and the surface of chloroplasts exposed to intercellular air spaces.     

Understanding down-regulation of photosynthesis under water stress: future prospects and searching for physiological tools for irrigation management

Photosynthetic down-regulation and/or inhibition under water stress conditions are determinants for plant growth, survival and yield in drought-prone areas. Current knowledge about the sequence of metabolic events that leads to complete inhibition of photosynthesis under severe water stress is reviewed. An analysis of published data reveals that a key regulatory role for Rubisco in photosynthesis is improbable under water stress conditions. By contrast, the little data available for other Calvin cycle enzymes suggest the possibility of a key regulatory role for some enzymes involved in the regeneration of RuBP. There are insufficient data to determine the role of photophosphorylation. Several important gaps in our knowledge of this field are highlighted. The most important is the remarkable scarcity of data about the regulation/inhibition of photosynthetic enzymes other than Rubisco under water stress. Consequently, new experiments are urgently needed to improve our current understanding of photosynthetic down-regulation under water stress. A second gap is the lack of knowledge of photosynthetic recovery after irrigation of plants which have been subjected to different stages of water stress. This knowledge is necessary in order to match physiological down-regulation by water stress with controlled irrigation programmes.     

Leaf anatomical properties in relation to differences in mesophyll conductance to CO2 and photosynthesis in two related Mediterranean Abies species

Abies alba and Abies pinsapo are closely related species with the same ribulose 1·5‐bisphosphate carboxylase/oxygenase (Rubisco) large subunit (rbcL) but contrasting hydraulic traits and mesophyll structure occurring in the Iberian Peninsula under contrasting conditions. As photosynthesis and hydraulic capacities often co‐scale, we hypothesize that these species differ in mesophyll conductance to CO₂ (g_m). g_m and key anatomical traits were measured in both species. Drought‐adapted population of A. pinsapo has higher photosynthesis than the more mesic population of A. alba, in agreement with its higher hydraulic capacity. However, A. alba exhibits the largest stomatal conductance (g_s), and so water use efficiency (WUE) is much higher in A. pinsapo. The differences in photosynthesis were explained by differences in g_m, indicating a correlation between hydraulic capacity and g_m. We report a case where g_m is the main factor limiting photosynthesis in one species (A. alba) when compared with the other one (A. pinsapo). The results also highlight the discrepancy between g_m estimates based on anatomical measurements and those based on gas exchange methods, probably due to the very large resistance exerted by cell walls and the stroma in both species. Thus, the cell wall and chloroplast properties in relation to CO₂ diffusion constitute a near‐future research priority.     

Leaf responses to drought stress in Mediterranean accessions of Solanum lycopersicum: anatomical adaptations in relation to gas exchange parameters

In a previous study, important acclimation to water stress was observed in the Ramellet tomato cultivar (TR) from the Balearic Islands, related to an increase in the water‐use efficiency through modifications in both stomatal (g_s) and mesophyll conductances (g_m). In the present work, the comparison of physiological and morphological traits between TR accessions grown with and without water stress confirmed that variability in the photosynthetic capacity was mostly explained by differences in the diffusion of CO₂ through stomata and leaf mesophyll. Maximization of g_m under both treatments was mainly achieved through adjustments in the mesophyll thickness and porosity and the surface area of chloroplasts exposed to intercellular airspace (S_c). In addition, the lower g_m/S_c ratio for a given porosity in drought‐acclimated plants suggests that the decrease in g_m was due to an increased cell wall thickness. Stomatal conductance was also affected by drought‐associated changes in the morphological properties of stomata, in an accession and treatment‐dependent manner. The results confirm the presence of advantageous physiological traits in the response to drought stress in Mediterranean accessions of tomato, and relate them to particular changes in the leaf anatomical properties, suggesting specific adaptive processes operating at the leaf anatomical level.     

Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves

The specificity factor of Rubisco is a measure of the relative capacities of the enzyme to catalyse carboxylation and oxygenation of ribulose 1,5-bisphosphate and hence to control the relative rates of photosynthetic carbon assimilation and photorespiration. Specificity factors of purified Rubisco from 24 species of C₃ plants found in diverse habitats with a wide range of environmental growth limitations by both water availability and temperature in the Balearic Islands were measured at 25 °C. The results suggest that specificity factors are more dependent on environmental pressure than on phylogenetic factors. Irrespective of phylogenetic relationships, higher specificity factors were found in species characteristically growing in dryer environments and in species that are hemideciduous or evergreen. Effects of temperature on specificity factor of the purified enzyme from 14 species were consistent with the concept that higher specificity factors were associated with an increase in the activation energy for oxygenation compared to carboxylation of the 2,3-enediolate of RuBP to the respective transition state intermediates. The results are discussed in terms of selection pressures leading to the differences in specificity factors and the value of the observations for identifying useful genetic manipulation to change Rubisco polypeptide subunits.     

Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends

The present study characterizes the kinetic properties of ribulose‐1,5‐bisphosphate carboxylase/oxygenase (Rubisco) from 28 terrestrial plant species, representing different phylogenetic lineages, environmental adaptations and photosynthetic mechanisms. Our findings confirm that past atmospheric CO₂/O₂ ratio changes and present environmental pressures have influenced Rubisco kinetics. One evolutionary adaptation to a decreasing atmospheric CO₂/O₂ ratio has been an increase in the affinity of Rubisco for CO₂ (K_c falling), and a consequent decrease in the velocity of carboxylation (k_cat^c), which in turn has been ameliorated by an increase in the proportion of leaf protein accounted by Rubisco. The trade‐off between K_c and k_cat^c was not universal among the species studied and deviations from this relationship occur in extant forms of Rubisco. In species adapted to particular environments, including carnivorous plants, crassulacean acid metabolism species and C₃ plants from aquatic and arid habitats, Rubisco has evolved towards increased efficiency, as demonstrated by a higher k_cat^c/K_c ratio. This variability in kinetics was related to the amino acid sequence of the Rubisco large subunit. Phylogenetic analysis identified 13 residues under positive selection during evolution towards specific Rubisco kinetic parameters. This crucial information provides candidate amino acid replacements, which could be implemented to optimize crop photosynthesis under a range of environmental conditions.