The leaf economics spectrum (LES) represents a suite of intercorrelated leaf traits concerning construction costs per unit leaf area, nutrient concentrations, and rates of carbon fixation and tissue ...turnover. Although broad trade-offs among leaf structural and physiological traits have been demonstrated, we still do not have a comprehensive view of the fundamental constraints underlying the LES trade-offs.
Here, we investigated physiological and structural mechanisms underpinning the LES by analysing a novel data compilation incorporating rarely considered traits such as the dry mass fraction in cell walls, nitrogen allocation, mesophyll CO2 diffusion and associated anatomical traits for hundreds of species covering major growth forms.
The analysis demonstrates that cell wall constituents are major components of leaf dry mass (18–70%), especially in leaves with high leaf mass per unit area (LMA) and long lifespan. A greater fraction of leaf mass in cell walls is typically associated with a lower fraction of leaf nitrogen (N) invested in photosynthetic proteins; and lower within-leaf CO2 diffusion rates, as a result of thicker mesophyll cell walls.
The costs associated with greater investments in cell walls underpin the LES: long leaf lifespans are achieved via higher LMA and in turn by higher cell wall mass fraction, but this inevitably reduces the efficiency of photosynthesis.
Foliage photosynthetic and structural traits were studied in 15 species with a wide range of foliage anatomies to gain insight into the importance of key anatomical traits in the limitation of ...diffusion of CO2 from substomatal cavities to chloroplasts. The relative importance of different anatomical traits in constraining CO2 diffusion was evaluated using a quantitative model. Mesophyll conductance (g m) was most strongly correlated with chloroplast exposed surface to leaf area ratio (S c/S) and cell wall thickness (T cw), but, depending on foliage structure, the overall importance of g m in constraining photosynthesis and the importance of different anatomical traits in the restriction of CO2 diffusion varied. In species with mesophytic leaves, membrane permeabilities and cytosol and stromal conductance dominated the variation in g m. However, in species with sclerophytic leaves, g m was mostly limited by T cw. These results demonstrate the major role of anatomy in constraining mesophyll diffusion conductance and, consequently, in determining the variability in photosynthetic capacity among species.
Mesophyll conductance is thought to be an important photosynthetic limitation in gymnosperms, but they currently constitute the most understudied plant group in regard to the extent to which ...photosynthesis and intrinsic water use efficiency are limited by mesophyll conductance. A comprehensive analysis of leaf gas exchange, photosynthetic limitations, mesophyll conductance (calculated by three methods previously used for across-species comparisons), and the underlying ultra-anatomical, morphological and chemical traits in 11 gymnosperm species varying in evolutionary history was performed to gain insight into the evolution of structural and physiological controls on photosynthesis at the lower return end of the leaf economics spectrum. Two primitive herbaceous species were included in order to provide greater evolutionary context. Low mesophyll conductance was the main limiting factor of photosynthesis in the majority of species. The strongest sources of limitation were extremely thick mesophyll cell walls, high chloroplast thickness and variation in chloroplast shape and size, and the low exposed surface area of chloroplasts per unit leaf area. In gymnosperms, the negative relationship between net assimilation per mass and leaf mass per area reflected an increased mesophyll cell wall thickness, whereas the easy-to-measure integrative trait of leaf mass per area failed to predict the underlying ultrastructural traits limiting mesophyll conductance.
In sclerophylls, photosynthesis is particularly strongly limited by mesophyll diffusion resistance from substomatal cavities to chloroplasts (r
m), but the controls on diffusion limits by integral ...leaf variables such as leaf thickness, density, and dry mass per unit area and by the individual steps along the diffusion pathway are imperfectly understood. To gain insight into the determinants ofr
min leaves with varying structure, the full CO₂ physical diffusion pathway was analysed in 32 Australian species sampled from sites contrasting in soil nutrients and rainfall, and having leaf structures from mesophytic to strongly sclerophyllous.r
mwas estimated based on combined measurements of gas exchange and chlorophyll fluorescence. In addition,r
mwas modelled on the basis of detailed anatomical measurements to separate the importance of different serial resistances affecting CO₂ diffusion into chloroplasts. The strongest sources of variation inr
mwereS
c/S, the exposed surface area of chloroplasts per unit leaf area, and mesophyll cell wall thickness,t
cw. The strong correlation ofr
mwitht
cwcould not be explained by cell wall thickness alone, and most likely arose from a further effect of cell wall porosity. The CO₂ drawdown from intercellular spaces to chloroplasts was positively correlated witht
cw, suggesting enhanced diffusional limitations in leaves with thicker cell walls. Leaf thickness and density were poorly correlated withS
c/S, indicating that widely varying combinations of leaf anatomical traits occur at given values of leaf integrated traits, and suggesting that detailed anatomical studies are needed to predictr
mfor any given species.
Finite mesophyll diffusion conductance (gm) significantly constrains net assimilation rate (An), but gm variations and variation sources in response to environmental stresses during leaf development ...are imperfectly known. The combined effects of light and water limitations on gm and diffusion limitations of photosynthesis were studied in saplings of Populus tremula L. An one‐dimensional diffusion model was used to gain insight into the importance of key anatomical traits in determining gm. Leaf development was associated with increases in dry mass per unit area, thickness, density, exposed mesophyll (Smes/S) and chloroplast (Sc/S) to leaf area ratio, internal air space (fias), cell wall thickness and chloroplast dimensions. Development of Smes/S and Sc/S was delayed under low light. Reduction in light availability was associated with lower Sc/S, but with larger fias and chloroplast thickness. Water stress reduced Sc/S and increased cell wall thickness under high light. In all treatments, gm and An increased and CO2 drawdown because of gm, Ci–Cc, decreased with increasing leaf age. Low light and drought resulted in reduced gm and An and increased Ci–Cc. These results emphasize the importance of gm and its components in determining An variations during leaf development and in response to stress.
► The intention of the present review is to update the consensus knowledge on gm. ► Gaps in knowledge and research priorities are indicated for the near future. ► In particular, how has gm evolved ...among phylogenetically distant groups? ► Can gm be uncoupled from the water path regulation? ► Mechanistic models of gm incorpored in photosynthesis models are needed.
Mesophyll diffusion conductance to CO2 is a key photosynthetic trait that has been studied intensively in the past years. The intention of the present review is to update knowledge of gm, and highlight the important unknown and controversial aspects that require future work. The photosynthetic limitation imposed by mesophyll conductance is large, and under certain conditions can be the most significant photosynthetic limitation. New evidence shows that anatomical traits, such as cell wall thickness and chloroplast distribution are amongst the stronger determinants of mesophyll conductance, although rapid variations in response to environmental changes might be regulated by other factors such as aquaporin conductance.
Gaps in knowledge that should be research priorities for the near future include: how different is mesophyll conductance among phylogenetically distant groups and how has it evolved? Can mesophyll conductance be uncoupled from regulation of the water path? What are the main drivers of mesophyll conductance? The need for mechanistic and phenomenological models of mesophyll conductance and its incorporation in process-based photosynthesis models is also highlighted.
Ferns and fern allies have low photosynthetic rates compared with seed plants. Their photosynthesis is thought to be limited principally by physical CO2 diffusion from the atmosphere to chloroplasts.
...The aim of this study was to understand the reasons for low photosynthesis in species of ferns and fern allies (Lycopodiopsida and Polypodiopsida). We performed a comprehensive assessment of the foliar gas-exchange and mesophyll structural traits involved in photosynthetic function for 35 species of ferns and fern allies. Additionally, the leaf economics spectrum (the interrelationships between photosynthetic capacity and leaf/frond traits such as leaf dry mass per unit area or nitrogen content) was tested.
Low mesophyll conductance to CO2 was the main cause for low photosynthesis in ferns and fern allies, which, in turn, was associated with thick cell walls and reduced chloroplast distribution towards intercellular mesophyll air spaces.
Generally, the leaf economics spectrum in ferns follows a trend similar to that in seed plants. Nevertheless, ferns and allies had less nitrogen per unit DW than seed plants (i.e. the same slope but a different intercept) and lower photosynthesis rates per leaf mass area and per unit of nitrogen.
The photosynthetic efficiency of plants in different environments is controlled by stomata, hydraulics, biochemistry, and mesophyll conductance (gm). Recently, gm was demonstrated to be the key ...limitation of photosynthesis in gymnosperms. Values of gm across gymnosperms varied over 20-fold, but this variation was poorly explained by robust structure-bound integrated traits such as leaf dry mass per area. Understanding how the component structural traits control gm is central for identifying the determinants of variability in gm across plant functional and phylogenetic groups. Here, we investigated the structural traits responsible for gm in 65 diverse gymnosperms. Although the integrated morphological traits, shape, and anatomical characteristics varied widely across species, the distinguishing features of all gymnosperms were thick mesophyll cell walls and low chloroplast area exposed to intercellular airspace (Sc/S) compared with angiosperms. Sc/S and cell wall thickness were the fundamental traits driving variations in gm across gymnosperm species. Chloroplast thickness was the strongest limitation of gm among liquid-phase components. The variation in leaf dry mass per area was not correlated with the key ultrastructural traits determining gm. Thus, given the absence of correlating integrated easy-to-measure traits, detailed knowledge of underlying component traits controlling gm across plant taxa is necessary to understand the photosynthetic limitations across ecosystems.
Photosynthesis in bryophytes and lycophytes has received less attention than terrestrial plant groups. In particular, few studies have addressed the nonstomatal diffusion conductance to CO₂ g
nsd of ...these plant groups.
Their lower photosynthetic rate per leaf mass area at any given nitrogen concentration compared with vascular plants suggested a stronger limitation by CO₂ diffusion. We hypothesized that bryophyte and lycophyte photosynthesis is largely limited by low g
nsd. Here, we studied CO₂ diffusion inside the photosynthetic tissues and its relationships with photosynthesis and anatomical parameters in bryophyte and lycophyte species in Antarctica, Australia, Estonia, Hawaii and Spain.
On average, lycophytes and, specially, bryophytes had the lowest photosynthetic rates and nonstomatal diffusion conductance reported for terrestrial plants. These low values are related to their very thick cell walls and their low exposure of chloroplasts to cell perimeter.
We conclude that the reason why bryophytes lie at the lower end of the leaf economics spectrum is their strong nonstomatal diffusion conductance limitation to photosynthesis, which is driven by their specific anatomical characteristics.
Leaf age-dependent changes in structure, nitrogen content, internal mesophyll diffusion conductance (g(m)), the capacity for photosynthetic electron transport (J(max)) and the maximum carboxylase ...activity of Rubisco (V(cmax)) were investigated in mature non-senescent leaves of Laurus nobilis L., Olea europea L. and Quercus ilex L. to test the hypothesis that the relative significance of biochemical and diffusion limitations of photosynthesis changes with leaf age. The leaf life-span was up to 3 years in L. nobilis and O. europea and 6 years in Q. ilex. Increases in leaf age resulted in enhanced leaf dry mass per unit area (M(A)), larger leaf dry to fresh mass ratio, and lower nitrogen contents per dry mass (N(M)) in all species, and lower nitrogen contents per area (N(A)) in L. nobilis and Q. ilex. Older leaves had lower g(m), J(max) and V(cmax). Due to the age-dependent increase in M(A), mass-based g(m), J(max) and V(cmax) declined more strongly (7- to 10-fold) with age than area-based (5- to 7-fold) characteristics. Diffusion conductance was positively associated with foliage photosynthetic potentials. However, this correlation was curvilinear, leading to lower ratio of chloroplastic to internal CO2 concentration (C(c)/C(i)) and-larger drawdown of CO2 from leaf internal air space to chloroplasts (delta(C)) in older leaves with lower g(m). Overall the age-dependent decreases in photosynthetic potentials were associated with decreases in N(M) and in the fraction of N in photosynthetic proteins, whereas decreases in g(m) were associated with increases in M(A) and the fraction of cell walls. These age-dependent modifications altered the functional scaling of foliage photosynthetic potentials with M(A), N(M), and N(A). The species primarily differed in the rate of age-dependent modifications in foliage structural and functional characteristics, but also in the degree of age-dependent changes in various variables. Stomatal openness was weakly associated with leaf age, but due to species differences in stomatal openness, the distribution of total diffusion limitation between stomata and mesophyll varied among species. These data collectively demonstrate that in Mediterranean evergreens, structural limitations of photosynthesis strongly interact with biochemical limitations. Age-dependent changes in g(m) and photosynthetic capacities do not occur in a co-ordinated manner in these species such that mesophyll diffusion constraints curb photosynthesis more in older than in younger leaves.
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