Contrasting anatomical and biochemical controls on mesophyll conductance across plant functional types

Mesophyll conductance (gm) limits photosynthesis by restricting CO2 diffusion between the substomatal cavities and chloroplasts. Although it is known that gm is determined by both leaf anatomical and biochemical traits, their relative contribution across plant functional types (PFTs) is still unclear. We compiled a dataset of gm measurements and concomitant leaf traits in unstressed plants comprising 563 studies and 617 species from all major PFTs. We investigated to what extent gm limits photosynthesis across PFTs, how gm relates to structural, anatomical, biochemical, and physiological leaf properties, and whether these relationships differ among PFTs. We found that gm imposes a significant limitation to photosynthesis in all C3 PFTs, ranging from 10–30% in most herbaceous annuals to 25–50% in woody evergreens. Anatomical leaf traits explained a significant proportion of the variation in gm (R2 > 0.3) in all PFTs except annual herbs, in which gm is more strongly related to biochemical factors associated with leaf nitrogen and potassium content. Our results underline the need to elucidate mechanisms underlying the global variability of gm. We emphasise the underestimated potential of gm for improving photosynthesis in crops and identify modifications in leaf biochemistry as the most promising pathway for increasing gm in these species

Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species

Leaf age-dependent changes in structure, nitrogen content, internal mesophyll diffusion conductance (gm), the capacity for photosynthetic electron transport (Jmax) and the maximum carboxylase activity of Rubisco (Vcmax) 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 (MA), larger leaf dry to fresh mass ratio, and lower nitrogen contents per dry mass (NM) in all species, and lower nitrogen contents per area (NA) in L. nobilis and Q. ilex. Older leaves had lower gm, Jmax and Vcmax. Due to the age-dependent increase in MA, mass-based gm, Jmax and Vcmax 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 ( Cc/Ci) and larger drawdown of CO2 from leaf internal air space to chloroplasts (DC) in older leaves with lower gm. Overall the agedependent decreases in photosynthetic potentials were associated with decreases in NM and in the fraction of N in photosynthetic proteins, whereas decreases in gm were associated with increases in MA and the fraction of cell walls. These age-dependent modifications altered the functional scaling of foliage photosynthetic potentials with MA, NM, and NA. The species primarily differed in the rate of agedependent modifications in foliage structural and functional characteristics, but also in the degree of agedependent 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 gm 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

Complex adjustments of photosynthetic potentials and internal diffusion conductance to current and previous light availabilities and leaf age in Mediterranean evergreen species Quercus ilex

Mature non-senescent leaves of evergreen species become gradually shaded as new foliage develops and canopy expands, but the interactive effects of integrated light during leaf formation (QintG), current light (QintC) and leaf age on foliage photosynthetic competence are poorly understood. In Quercus ilex L., we measured the responses of leaf structural and physiological variables to QintC and QintG for four leaf age classes. Leaf aging resulted in increases in leaf dry mass per unit area (MA), and leaf dry to fresh mass ratio (DF) and decreases in N content per dry mass (NM). N content per area (NA) was independent of age, indicating that decreases in NM reflected dilution of leaf N because of accumulation of dry mass (NA=NMMA). MA, DF and NA scaled positively with irradiance, whereas these age-specific correlations were stronger with leaf growth light than with current leaf light. Area-based maximum ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) carboxylase activity (VcmaxA), capacity for photosynthetic electron transport (JmaxA) and the rate of non-photorespiratory respiration in light (RdA) were also positively associated with irradiance. Differently from leaf structural characteristics, for all data pooled, these relationships were stronger with current light with little differences among leaves of different age. Acclimation to current leaf light environment was achieved by light-dependent partitioning of N in ratelimiting proteins. Mass-based physiological activities decreased with increasing leaf age, reflecting dilution of leaf N and a larger fraction of non-photosynthetic N in older leaves. This resulted in age-dependent modification of leaf photosynthetic potentials versus N relationships. Internal diffusion conductance (gm) per unit area (gmA) increased curvilinearly with increasing irradiance for two youngest leaf age classes and was independent of light for older leaves. In contrast, gmper dry mass (gmM) was negatively associated with light in current-year leaves. Greater photosynthetic potentials and moderate changes in diffusion conductance resulted in greater internal diffusion limitations of photosynthesis in higher light. Both area- and massbased gm decreased with increasing leaf age. The decrease in diffusion conductance was larger than changes in photosynthetic potentials, leading to larger CO2 drawdown from leaf internal air space to chloroplasts (DC) in older leaves. The increases in diffusion limitations in older leaves and at higher light scaled with age- and light-dependent increases in MA and DF. Overall, our study demonstrates a large potential of foliage photosynthetic acclimation to changes in leaf light environment, but also highlights enhanced structural diffusion limitations in older leaves that result from leaf structural acclimation to previous rather than to current light environment and accumulation of structural compounds with leaf age

A meta-analysis of mesophyll conductance to CO2in relation to major abiotic stresses in poplar species

Mesophyll conductance (gm) determines the diffusion of CO2 from the substomatal cavities to the site of carboxylation in the chloroplasts and represents a critical component of the diffusive limitation of photosynthesis. In this study, we evaluated the average effect sizes of different environmental constraints on gm in Populus spp., a forest tree model. We collected raw data of 815 A-Ci response curves from 26 datasets to estimate gm, using a single curve-fitting method to alleviate method-related bias. We performed a meta-analysis to assess the effects of different abiotic stresses on gm. We found a significant increase in gm from the bottom to the top of the canopy that was concomitant with the increase of maximum rate of carboxylation and light-saturated photosynthetic rate (Amax). gm was positively associated with increases in soil moisture and nutrient availability, but was insensitive to increasing soil copper concentration and did not vary with atmospheric CO2 concentration. Our results showed that gm was strongly related to Amax and to a lesser extent to stomatal conductance (gs). Moreover, a negative exponential relationship was obtained between gm and specific leaf area, which may be used to scale-up gm within the canopy

Improving photosynthetic efficiency toward food security: Strategies, advances, and perspectives

Photosynthesis in crops and natural vegetation allows light energy to be converted into chemical energy and thus forms the foundation for almost all terrestrial trophic networks on Earth. The efficiency of photosynthetic energy conversion plays a crucial role in determining the portion of incident solar radia-tion that can be used to generate plant biomass throughout a growth season. Consequently, alongside the factors such as resource availability, crop management, crop selection, maintenance costs, and intrinsic yield potential, photosynthetic energy use efficiency significantly influences crop yield. Photosynthetic ef-ficiency is relevant to sustainability and food security because it affects water use efficiency, nutrient use efficiency, and land use efficiency. This review focuses specifically on the potential for improvements in photosynthetic efficiency to drive a sustainable increase in crop yields. We discuss bypassing photorespi-ration, enhancing light use efficiency, harnessing natural variation in photosynthetic parameters for breeding purposes, and adopting new-to-nature approaches that show promise for achieving unprece-dented gains in photosynthetic efficiency

The leaf economics spectrum and its underlying physiological and anatomical principles

Large variations are found in leaf morphology and physiology across species in nature, reflecting diversity in carbon fixation and growth strategies. These variations in leaf traits are not random; rather, they are tightly coordinated with each other. Leaf traits can be expressed per leaf dry mass or per leaf area. A leaf-mass basis reflects leaf economics, i.e., revenues and expenditures per unit investment of biomass, while a leaf-area basis reflects fluxes in relation to surfaces. Leaf N and P concentrations, and photosynthetic and respiration rates – all considered on a mass basis, are negatively correlated with leaf mass per area (LMA) whilst leaf lifespan is positively correlated with LMA. These correlations are summarized into a single major axis called the “leaf economics spectrum” that runs from “quick-return” to “slow-return” species. On the other hand, correlations among area-based traits are less consistent and less understood in relation to leaf economy. LMA was positively correlated with leaf N content but mostly independent from photosynthetic rates per unit leaf area. Given that N is an essential element in photosynthetic proteins and thus photosynthesis, clarifying the mechanisms why the efficiency of photosynthesis (photosynthesis per unit N) decreases with LMA is a major concern in understanding the correlations among area-based traits in relation to leaf economy. Currently available data suggest that greater amounts of cell wall are required for long-lived leaves, which reduces the efficiency of photosynthesis by lowering (1) the fraction of leaf N invested in photosynthetic proteins and (2) CO2 diffusion rates through thicker and denser mesophyll cell walls. These physiological and structural constraints are a fundamental mechanism underpinning the general correlations among leaf economic traits