Summary
Photosynthesis is the basis of all life on Earth. Surprisingly, until very recently, data on photosynthesis, photosynthetic efficiencies, and photosynthesis limitations in terrestrial land ...plants other than spermatophytes were very scarce. Here we provide an updated data compilation showing that maximum photosynthesis rates (expressed either on an area or dry mass basis) progressively scale along the land plant’s phylogeny, from lowest values in bryophytes to largest in angiosperms. Unexpectedly, both photosynthetic water (WUE) and nitrogen (PNUE) use efficiencies also scale positively through the phylogeny, for which it has been commonly reported that these two efficiencies tend to trade‐off between them when comparing different genotypes or a single species subject to different environmental conditions. After providing experimental evidence that these observed trends are mostly due to an increased mesophyll conductance to CO2 – associated with specific anatomical changes – along the phylogeny, we discuss how these findings on a large phylogenetic scale can provide useful information to address potential photosynthetic improvements in crops in the near future.
Significance Statement
The variation of maximum photosynthesis, water‐use‐efficiency and nitrogen‐use‐efficiency along the land plants' phylogeny is reviewed.
Stomatal conductance (gs) and mesophyll conductance (gm) represent major constraints to photosynthetic rate (A), and these traits are expected to coordinate with leaf hydraulic conductance (Kleaf) ...across species, under both steady‐state and dynamic conditions. However, empirical information about their coordination is scarce. In this study, Kleaf, gas exchange, stomatal kinetics, and leaf anatomy in 10 species including ferns, gymnosperms, and angiosperms were investigated to elucidate the correlation of H2O and CO2 diffusion inside leaves under varying light conditions. Gas exchange, Kleaf, and anatomical traits varied widely across species. Under light‐saturated conditions, the A, gs, gm, and Kleaf were strongly correlated across species. However, the response patterns of A, gs, gm, and Kleaf to varying light intensities were highly species dependent. Moreover, stomatal opening upon light exposure of dark‐adapted leaves in the studied ferns and gymnosperms was generally faster than in the angiosperms; however, stomatal closing in light‐adapted leaves after darkening was faster in angiosperms. The present results show that there is a large variability in the coordination of leaf hydraulic and gas exchange parameters across terrestrial plant species, as well as in their responses to changing light.
In this paper, we explored the responses of gas exchange parameters and leaf hydraulic conductance to light changes in 10 species. In this study, we found (a) a phylogenetic trend emerges from ferns to angiosperms, consisting of increasing steady‐state values for gas exchange and hydraulic capacities; (b) a similar phylogenetic trend is observed concerning the response of these parameters to varying light, with a gradual increase in the number of traits able to respond to light from none in ferns to all in angiosperms; (c) these phylogenetic trends may have exceptions, as illustrated here by the angiosperm species Centella asiatica, which behaves in all studied aspects similar to a fern; and finally, (d) differences among phylogenetic groups are also evidenced concerning in their stomatal kinetics, with stomatal opening faster in ferns and gymnosperms than angiosperms, but stomatal closing faster in angiosperms.
Abstract
The leaf economics spectrum (LES) is an ecophysiological concept describing the trade-offs of leaf structural and physiological traits, and has been widely investigated on multiple scales. ...However, the effects of the breeding process on the LES in crops, as well as the mechanisms of the trait trade-offs underlying the LES, have not been thoroughly elucidated to date. In this study, a dataset that included leaf anatomical, biochemical, and functional traits was constructed to evaluate the trait covariations and trade-offs in domesticated species, namely rice (Oryza species). The slopes and intercepts of the major bivariate correlations of the leaf traits in rice were significantly different from the global LES dataset (Glopnet), which is based on multiple non-crop species in natural ecosystems, although the general patterns were similar. The photosynthetic traits responded differently to leaf structural and biochemical changes, and mesophyll conductance was the most sensitive to leaf nitrogen (N) status. A further analysis revealed that the relative limitation of mesophyll conductance declined with leaf N content; however, the limitation of the biochemistry increased relative to leaf N content. These findings indicate that breeding selection and high-resource agricultural environments lead crops to deviate from the leaf trait covariation in wild species, and future breeding to increase the photosynthesis of rice should primarily focus on improvement of the efficiency of photosynthetic enzymes.
Leaf hydraulic conductance (K
leaf) and mesophyll conductance (g
m) both represent major constraints to photosynthetic rate (A), and previous studies have suggested that K
leaf and g
m is correlated ...in leaves. However, there is scarce empirical information about their correlation.
In this study, K
leaf, leaf hydraulic conductance inside xylem (K
x), leaf hydraulic conductance outside xylem (K
ox), A, stomatal conductance (g
s), g
m, and anatomical and structural leaf traits in 11 Oryza genotypes were investigated to elucidate the correlation of H2O and CO2 diffusion inside leaves.
All of the leaf functional and anatomical traits varied significantly among genotypes. K
leaf was not correlated with the maximum theoretical stomatal conductance calculated from stomatal dimensions (g
smax), and neither g
s nor g
smax were correlated with K
x. Moreover, K
ox was linearly correlated with g
m and both were closely related to mesophyll structural traits.
These results suggest that K
leaf and g
m are related to leaf anatomical and structural features, which may explain the mechanism for correlation between g
m and K
leaf.
A compromise between carbon assimilation and structure investment at the leaf level is broadly accepted, yet the relationship between net assimilation per area (An) and leaf mass per area has been ...elusive. We propose bulk modulus of elasticity (ε) as a suitable parameter to reflect both leaf structure and function, and an inverse relationship between ε and An and mesophyll conductance (gm) is postulated. Using data for An, gm and ε from previous studies and new measurements on a set of 20 species covering all major growth forms, a negative relationship between An or gm and ε was observed. High ε was also related to low leaf capacitance and higher diffusive limitations to photosynthesis. In conclusion, ε emerges as a key trait linked with photosynthetic capacity across vascular plants, and its relationship with gm suggests the existence of a common mechanistic basis, probably involving a key role of cell walls.
Aquaporins and plant water balance KALDENHOFF, RALF; RIBAS-CARBO, MIQUEL; SANS, JAUME FLEXAS ...
Plant, cell & environment/Plant, cell and environment,
20/May , Volume:
31, Issue:
5
Journal Article
Peer reviewed
Open access
The impact of aquaporin function on plant water balance is discussed. The significance of these proteins for root water uptake, water conductance in the xylem, including embolism refilling and the ...role of plant aquaporins in leaf physiology, is described. Emphasis is placed on certain aspects of water stress reactions and the correlation of aquaporins to abscisic acid as well as on the relation of water and CO₂ permeability in leaves.
We revisit the theory connecting chlorophyll a fluorescence to photosynthesis in the spatiotemporal context of remote sensing. Physical, physiological, and methodological factors are discussed, and a ...roadmap to future research presented.
In Antarctica, multiple stresses (low temperatures, drought and excessive irradiance) hamper photosynthesis even in summer. We hypothesize that controlled inactivation of PSII reaction centres, a ...mechanism widely studied by pioneer work of Fred Chow and co-workers, may effectively guarantee functional photosynthesis under these conditions. Thus, we analysed the energy partitioning through photosystems in response to temperature in 15 bryophyte species presenting different worldwide distributions but all growing in Livingston Island, under controlled and field conditions. We additionally tested their tolerance to desiccation and freezing and compared those with their capability for sexual reproduction in Antarctica (as a proxy to overall fitness). Under field conditions, when irradiance rules air temperature by the warming of shoots (up to 20 °C under sunny days), a predominance of sustained photoinhibition beyond dynamic heat dissipation was observed at low temperatures. Antarctic endemic and polar species showed the largest increases of photoinhibition at low temperatures. On the contrary, the variation of thermal dissipation with temperature was not linked to species distribution. Instead, maximum non-photochemical quenching at 20 °C was related (strongly and positively) with desiccation tolerance, which also correlated with fertility in Antarctica, but not with freezing tolerance. Although all the analysed species tolerated − 20 °C when dry, the tolerance to freezing in hydrated state ranged from the exceptional ability of
Schistidium rivulare
(that survived for 14 months at − 80 °C) to the susceptibility of
Bryum pseudotriquetrum
(that died after 1 day at − 20 °C unless being desiccated before freezing).
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.
Plant metabolism drives plant development and plant-environment responses, and data readouts from this cellular level could provide insights in the underlying molecular processes. Existing studies ...have already related key in vivo leaf gas-exchange parameters with structural traits and nutrient components across multiple species. However, insights in the relationships of leaf gas-exchange with leaf primary metabolism are still limited. We investigated these relationships through a multispecies meta-analysis approach based on data sets from 17 published studies describing net photosynthesis (A) and stomatal (gs
) and mesophyll (gm
) conductances, alongside the 53 data profiles from primary metabolism of 14 species grown in different experiments. Modeling results highlighted the conserved patterns between the different species. Consideration of species-specific effects increased the explanatory power of the models for some metabolites, including Glc-6-P, Fru-6-P, malate, fumarate, Xyl, and ribose. Significant relationships of A with sugars and phosphorylated intermediates were observed. While gs
was related to sugars, organic acids, myo-inositol, and shikimate, gm
showed a more complex pattern in comparison to the two other traits. Some metabolites, such as malate and Man, appeared in the models for both conductances, suggesting a metabolic coregulation between gs
and gm
. The resulting statistical models provide the first hints for coregulation patterns involving primary metabolism plus leaf water and carbon balances that are conserved across plant species, as well as species-specific trends that can be used to determine new biotechnological targets for crop improvement.