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 radiation 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 efficiency 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 photorespiration, enhancing light use efficiency, harnessing natural variation in photosynthetic parameters for breeding purposes, and adopting new-to-nature approaches that show promise for achieving unprecedented gains in photosynthetic efficiency.

Cell wall thickness has phylogenetically consistent effects on the photosynthetic nitrogen-use efficiency of terrestrial plants.

Leaf photosynthetic nitrogen-use efficiency (PNUE) diversified significantly among C3 species. To date, the morpho-physiological mechanisms and interrelationships shaping PNUE on an evolutionary time scale remain unclear. In this study, we assembled a comprehensive matrix of leaf morpho-anatomical and physiological traits for 679 C3 species, ranging from bryophytes to angiosperms, to comprehend the complexity of interrelationships underpinning PNUE variations. We discovered that leaf mass per area (LMA), mesophyll cell wall thickness (Tcwm ), Rubisco N allocation fraction (PR ), and mesophyll conductance (gm ) together explained 83% of PNUE variations, with PR and gm accounting for 65% of those variations. However, the PR effects were species-dependent on gm , meaning the contribution of PR on PNUE was substantially significant in high-gm species compared to low-gm species. Standard major axis (SMA) and path analyses revealed a weak correlation between PNUE and LMA (r2 = 0.1), while the SMA correlation for PNUE-Tcwm was robust (r2 = 0.61). PR was inversely related to Tcwm , paralleling the relationship between gm and Tcwm , resulting in the internal CO2 drawdown being only weakly proportional to Tcwm . The coordination of PR and gm in relation to Tcwm constrains PNUE during the course of evolution.

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.

Acute methyl jasmonate exposure results in major bursts of stress volatiles, but in surprisingly low impact on specialized volatile emissions in the fragrant grass Cymbopogon flexuosus.

Methyl jasmonate (MeJA) is an airborne hormonal elicitor that induces a fast rise of emissions of characteristic stress marker compounds methanol and green leaf volatiles (GLV), and a longer-term release of volatile terpenoids, but there is limited information of how terpene emissions respond to MeJA in terpene-storing species. East-Indian lemongrass (Cymbopogon flexuosus), an aromatic herb with a large terpenoid storage pool in idioblasts, was used to investigate the short- (0-1 h) and long-term (1-16 h) responses of leaf net assimilation rate (A), stomatal conductance (Gs) and volatile emissions to MeJA concentrations ranging from moderate to lethal. Both A and Gs were increasingly inhibited with increasing MeJA concentration in both short and long term. MeJA exposure resulted in a rapid elicitation, within 1 h after exposure, of methanol and GLV emissions. Subsequently, a secondary rise of GLV emissions was observed, peaking at 2 h after MeJA exposure for the highest and at 8 h for the lowest application concentration. The total amount and maximum emission rate of methanol and the first and second GLV emission bursts were positively correlated with MeJA concentration. Unexpectedly, no de novo elicitation of terpene emissions was observed through the experiment. Although high MeJA application concentrations led to visible lesions and desiccation in extensive leaf regions, this did not result in breakage of terpene-storing idioblasts. The study highlights an overall insensitivity of lemongrass to MeJA and indicates that differently from mechanical wounding, MeJA-driven cellular death does not break terpene-storing cells. Further studies are needed to characterize the sensitivity of induced defense responses in species with strongly developed constitutive defenses.

A meta-analysis of mesophyll conductance to CO2 in 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.

Variability in the chloroplast area lining the intercellular airspace and cell walls drives mesophyll conductance in gymnosperms.

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.

Are stomata in ferns and allies sluggish? Stomatal responses to CO2 , humidity and light and their scaling with size and density.

Fast stomatal reactions enable plants to successfully cope with a constantly changing environment yet there is an ongoing debate on the stomatal regulation mechanisms in basal plant groups. We measured stomatal morphological parameters in 29 fern and allied species from temperate to tropical biomes and two outgroup angiosperm species. Stomatal dynamic responses to environmental drivers were measured in 16 ferns and the two angiosperms using a gas-exchange system. Principal components analyses were used to further reveal the structure-function relationships in stomata. We show a > 10-fold variation for stomatal opening delays and 20-fold variation for stomatal closing delays in ferns. Across species, stomatal responses to vapor pressure deficit (VPD) were the fastest, while light and [CO2 ] responses were slower. In most cases the outgroup species' reaction speeds to changes in environmental variables were similar to those of ferns. Correlations between stomatal response rate and size were apparent for stomatal opening in light and low [CO2 ] while not evident for closing reactions and changes in VPD. No correlations between stomatal density and response speed were observed. Together, this study demonstrates different mechanisms controlling stomatal reactions in ferns at different environmental stimuli, which should be considered in future studies relating stomatal morphology and function.

Anatomical constraints to nonstomatal diffusion conductance and photosynthesis in lycophytes and bryophytes.

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 gnsd 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 gnsd . 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.

Glandular trichomes as a barrier against atmospheric oxidative stress: Relationships with ozone uptake, leaf damage, and emission of LOX products across a diverse set of species.

There is a spectacular variability in trichome types and densities and trichome metabolites across species, but the functional implications of this variability in protecting from atmospheric oxidative stresses remain poorly understood. The aim of this study was to evaluate the possible protective role of glandular and non-glandular trichomes against ozone stress. We investigated the interspecific variation in types and density of trichomes and how these traits were associated with elevated ozone impacts on visible leaf damage, net assimilation rate, stomatal conductance, chlorophyll fluorescence, and emissions of lipoxygenase pathway products in 24 species with widely varying trichome characteristics and taxonomy. Both peltate and capitate glandular trichomes played a critical role in reducing leaf ozone uptake, but no impact of non-glandular trichomes was observed. Across species, the visible ozone damage varied 10.1-fold, reduction in net assimilation rate 3.3-fold, and release of lipoxygenase compounds 14.4-fold, and species with lower glandular trichome density were more sensitive to ozone stress and more vulnerable to ozone damage compared to species with high glandular trichome density. These results demonstrate that leaf surface glandular trichomes constitute a major factor in reducing ozone toxicity and function as a chemical barrier that neutralizes the ozone before it enters the leaf.

Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living!

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.

Physiological and structural tradeoffs underlying the leaf economics spectrum.

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.

The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait.

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.

Emission Timetable and Quantitative Patterns of Wound-Induced Volatiles Across Different Leaf Damage Treatments in Aspen (Populus Tremula).

Plant-feeding herbivores can generate complex patterns of foliar wounding, but it is unclear how wounding-elicited volatile emissions scale with the severity of different wounding types, and there is no common protocol for wounding experiments. We investigated the rapid initial response to wounding damage generated by different numbers of straight cuts and punctures through leaf lamina as well as varying area of lamina squeezing in the temperate deciduous tree Populus tremula. Wounding-induced volatile emission time-courses were continuously recorded by a proton-transfer-reaction time-of-flight mass-spectrometer. After the mechanical wounding, an emission cascade was rapidly elicited resulting in sequential emissions of key stress volatiles methanol, acetaldehyde, and volatiles of the lipoxygenase pathway, collectively constituting more than 97% of the total emission. The maximum emission rates, reached after one to three minutes after wounding, and integrated emissions during the burst were strongly correlated with the severity in all damage treatments. For straight cuts and punch hole treatments, the emissions per cut edge length were constant, indicating a direct proportionality. Our results are useful for screening wounding-dependent emission capacities.

Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models.

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.

Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path.

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 of r(m) in leaves with varying structure, the full CO(2) 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(m) was estimated based on combined measurements of gas exchange and chlorophyll fluorescence. In addition, r(m) was modelled on the basis of detailed anatomical measurements to separate the importance of different serial resistances affecting CO(2) diffusion into chloroplasts. The strongest sources of variation in r(m) were S(c)/S, the exposed surface area of chloroplasts per unit leaf area, and mesophyll cell wall thickness, t(cw). The strong correlation of r(m) with t(cw) could not be explained by cell wall thickness alone, and most likely arose from a further effect of cell wall porosity. The CO(2) drawdown from intercellular spaces to chloroplasts was positively correlated with t(cw), suggesting enhanced diffusional limitations in leaves with thicker cell walls. Leaf thickness and density were poorly correlated with S(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 predict r(m) for any given species.

Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis.

Mesophyll diffusion conductance to CO(2) 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 g(m), 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.

Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: how structure constrains function.

Finite mesophyll diffusion conductance (g(m) ) significantly constrains net assimilation rate (A(n) ), but g(m) variations and variation sources in response to environmental stresses during leaf development are imperfectly known. The combined effects of light and water limitations on g(m) 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 g(m) . Leaf development was associated with increases in dry mass per unit area, thickness, density, exposed mesophyll (S(mes) /S) and chloroplast (S(c) /S) to leaf area ratio, internal air space (f(ias) ), cell wall thickness and chloroplast dimensions. Development of S(mes) /S and S(c) /S was delayed under low light. Reduction in light availability was associated with lower S(c) /S, but with larger f(ias) and chloroplast thickness. Water stress reduced S(c) /S and increased cell wall thickness under high light. In all treatments, g(m) and A(n) increased and CO(2) drawdown because of g(m) , C(i) -C(c) , decreased with increasing leaf age. Low light and drought resulted in reduced g(m) and A(n) and increased C(i) -C(c) . These results emphasize the importance of g(m) and its components in determining A(n) variations during leaf development and in response to stress.

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 (Q(int)G), current light (Q(int)C) 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 Q(int)C and Q(int)G for four leaf age classes. Leaf aging resulted in increases in leaf dry mass per unit area (M(A)), and leaf dry to fresh mass ratio (D(F)) and decreases in N content per dry mass (N(M)). N content per area (N(A)) was independent of age, indicating that decreases in N(M) reflected dilution of leaf N because of accumulation of dry mass (NA = N(M) M(A)). M(A), D(F) and N(A) 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 (V(cmax)A), capacity for photosynthetic electron transport (J(max)A) and the rate of non-photorespiratory respiration in light (R(d)A) 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 rate-limiting 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 (g(m)) per unit area (g(m)A) increased curvilinearly with increasing irradiance for two youngest leaf age classes and was independent of light for older leaves. In contrast, g(m) per dry mass (g(m)M) 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 mass-based g(m) 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 (delta(c)) 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 D(F). 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.