Rafael E. Coopman

Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants

Water limitation is a major global constraint for plant productivity that is likely to be exacerbated by climate change. Hence, improving plant water use efficiency (WUE) has become a major goal for the near future. At the leaf level, WUE is the ratio between photosynthesis and transpiration. Maintaining high photosynthesis under water stress, while improving WUE requires either increasing mesophyll conductance (gm ) and/or improving the biochemical capacity for CO2 assimilation-in which Rubisco properties play a key role, especially in C3 plants at current atmospheric CO2 . The goals of the present analysis are: (1) to summarize the evidence that improving gm and/or Rubisco can result in increased WUE; (2) to review the degree of success of early attempts to genetically manipulate gm or Rubisco; (3) to analyse how gm , gsw and the Rubiscos maximum velocity (Vcmax ) co-vary across different plant species in well-watered and drought-stressed conditions; (4) to examine how these variations cause differences in WUE and what is the overall extent of variation in individual determinants of WUE; and finally, (5) to use simulation analysis to provide a theoretical framework for the possible control of WUE by gm and Rubisco catalytic constants vis-à-vis gsw under water limitations.

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.

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 (gm ), 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, gm 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.

Stomatal and mesophyll conductances to CO2 in different plant groups: Underrated factors for predicting leaf photosynthesis responses to climate change?

The climate change conditions predicted for the end of the current century are expected to have an impact on the performance of plants under natural conditions. The variables which are foreseen to have a larger effect are increased CO2 concentration and temperature. Although it is generally considered CO2 assimilation rate could be increased by the increasing levels of CO2, it has been reported in previous studies that acclimation to high CO2 results in reductions of physiological parameters involved in photosynthesis, like the maximum carboxylation rate (Vc,max), stomatal conductance (gs) and mesophyll conductance to CO2 (gm). On the one hand, most of the previous modeling efforts have neglected the potential role played by the acclimation of gm to high CO2 and temperature. On the other hand, the effect of climate change on plant clades other than angiosperms, like ferns, has received little attention, and there are no studies evaluating the potential impact of increasing CO2 and temperature on these species. In this study we predicted responses of several representative species among angiosperms, gymnosperms and ferns to increasing CO2 and temperature. Our results show that species with lower photosynthetic capacity - such as some ferns and gymnosperms - would be proportionally more favored under these foreseen environmental conditions. The main reason for this difference is the lower diffusion limitation imposed by gs and gm in plants having high capacity for photosynthesis among the angiosperms, which reduces the positive effect of increasing CO2. However, this apparent advantage of low-diffusion species would be canceled if the two conductances - gs and gm - acclimate and are down regulated to high CO2, which is basically unknown, especially for gymnosperms and ferns. Hence, for a better understanding of different plant responses to future climate, studies are urged in which the actual photosynthetic response/acclimation to increased CO2 and temperature of ferns, gymnosperms and other under-evaluated plant groups is assessed.

Photosynthesis limitations in three fern species

Maximum photosynthesis rates in ferns are generally lower than those of seed plants, but little is known about the limiting factors, which are crucial to understand the evolution of photosynthesis in land plants. To address this issue, a gas exchange/chlorophyll fluorescence analysis was performed in three fern species spanning high phylogenetic range within Polypodiopsida (Osmunda regalis, Blechnum gibbum and Nephrolepis exaltata) to determine their maximum net photosynthesis (AN ), stomatal (gs ) and mesophyll (gm ) conductances to CO2 , and the maximum velocity of carboxylation (Vc,max ). The in vitro Rubisco specificity factor (SC /O ) was also determined. All three species had values for SC /O similar to those typical of seed plants, but values of AN , gs , gm and Vc,max were within the lowest range of those observed in seed plants. In addition, gs was unresponsive to light and CO2 , as already described in other fern species. On the contrary, gm varied with changes CO2 . A quantitative photosynthesis limitation analysis suggested that early land plants (ferns) presented not only stomatal limitations-which were less adjustable to the environment-but also restricted gm and Vc,max , resulting in limited maximum photosynthesis rates.

Differences in light usage among three fern species of genus Blechnum of contrasting ecological breadth in a forest light gradient

In Chilean evergreen temperate forest, fern species of the genus Blechnum occur in diverse microhabitats in a light gradient. We hypothesized that differences in the habitat preferences of three co-occurring Blechnum species would be associated with differences in the magnitude of responses of light capture [chlorophyll (Chl) content] and use (photosynthetic capacity and performance) to light availability. We measured the abundance, chlorophyll content, photosynthetic capacity (A), and photosynthetic performance (chlorophyll fluorescence of photosystems I and II) of juvenile individuals of each species growing in different light levels in the field. While Blechnum magellanicum covers a broad light environments range, B. mochaenum is restricted to shade, and B. penna-marina occupies full sun sites. Despite significant interspecific differences in average total chlorophyll content, this trait did not differ among species along the light gradient. There was significant interspecific variation in both the mean value and the plasticity of Chl a:Chl b ratio and A to light availability. While B. penna-marina showed a flatter reaction norm (lower response) of Chl a:Chl b ratio to light availability than its two congeners, B. mochaenum showed a lower response of A to light availability. B. penna-marina and B. magellanicum individuals from open sites had higher light saturation points of the electron transport rate (ETR) of both photosystems (ETRLSP I and II) and photochemical quenching (qL and NA) than the shade restricted B. mochaenum. Additionally, non-photochemical quenching values for both photosystems (NPQ and ND) were higher in ferns species occurring in shaded sites. The adjustment of the photosynthetic capacity and performance to light availability appears to be an important mechanism of acclimation in these three Blechnum species that differ in their habitat preferences across a light gradient.

Early performance of planted Nothofagus dombeyi and Nothofagus alpina in response to light availability and gap size in a high-graded forest in the south-central Andes of Chile

Resumen en: The Andes of south-central Chile (38 – 41° S) were once dominated by highly productive and valuable forests mainly dominated by Nothofagus dombeyi and N....

Tree size and light availability increase photochemical instead of non-photochemical capacities of Nothofagus nitida trees growing in an evergreen temperate rain forest

Nothofagus nitida (Phil.) Krasser (Nothofagaceae) regenerates under the canopy in microsites protected from high light. Nonetheless, it is common to find older saplings in clear areas and adults as emergent trees of the Chilean evergreen forest. We hypothesized that this shade to sun transition in N. nitida is supported by an increase in photochemical and non-photochemical energy dissipation capacities of both photosystems in parallel with the increase in plant size and light availability. To dissect the relative contribution of light environment and plant developmental stage to these physiological responses, the photosynthetic performance of both photosystems was studied from the morpho-anatomical to the biochemical level in current-year leaves of N. nitida plants of different heights (ranging from 0.1 to 7 m) growing under contrasting light environments (integrated quantum flux (IQF) 5-40 mol m(-2). Tree height (TH) and light environment (IQF) independently increased the saturated electron transport rates of both photosystems, as well as leaf and palisade thickness, but non-photochemical energy flux, photoinhibition susceptibility, state transition capacity, and the contents of D1 and PsbS proteins were not affected by IQF and TH. Spongy mesophyll thickness and palisade cell diameter decreased with IQF and TH. A(max), light compensation and saturation points, Rubisco and nitrogen content (area basis) only increased with light environment (IQF), whereas dark respiration (R(d)) decreased slightly and relative chlorophyll content was higher in taller trees. Overall, the independent effects of more illuminated environment and tree height mainly increased the photochemical instead of the non-photochemical energy flux. Regardless of the photochemical increase with TH, carbon assimilation only significantly improved with higher IQF. Therefore it seems that mainly acclimation to the light environment supports the phenotypic transition of N. nitida from shade to sun.

Acclimation of leaf cohorts expanded under light and water stresses: an adaptive mechanism of Eucryphia cordifolia to face changes in climatic conditions?

Eucryphia cordifolia Cav. is a long-lived evergreen tree species, commonly found as a canopy emergent tree in the Chilean temperate rain forest. This species displays successive leaf cohorts throughout the entire growing season. Thus, full leaf expansion occurs under different environmental conditions during growing such as air temperature, vapor pressure deficit and the progress of moderate water stress (WS). These climate variations can be reflected as differences in anatomical and physiological characteristics among leaf cohorts. Thus, we investigated the potential adaptive role of different co-existing leaf cohorts in seedlings grown under shade, drought stress or a combination of the two. Photosynthetic and anatomical traits were measured in the first displayed leaf cohort and in a subsequent leaf cohort generated during the mid-season. Although most anatomical and photosynthetic pigments did not vary between cohorts, photosynthetic acclimation did occur in the leaf cohort and was mainly driven by biochemical processes such as leaf nitrogen content, Rubisco carboxylation capacity and maximal Photosystem II electron transport rather than CO2 diffusion conductance. Cohort acclimation could be relevant in the context of climate change, as this temperate rainforest will likely face some degree of summer WS even under low light conditions. We suggest that the acclimation of the photosynthetic capacity among current leaf cohorts represents a well-tuned mechanism helping E. cordifolia seedlings to face a single stress like shade or drought stress, but is insufficient to cope with simultaneous stresses.

Photosynthetic responses of trees in high-elevation forests: comparing evergreen species along an elevation gradient in the Central Andes

Polylepis tarapacana forms the worlds highest forest, being able to grow up to 5,200 m a.s.l. At such elevations, low temperatures, high solar radiation and water scarcity severely restrict plant survival. Our study was focused on the photosynthetic responses of Polylepis species and how they are able to cope with such a challenging environment. We performed all measurements and samplings in their natural environment. This strategy allowed us to observe unexpected patterns of daily adjustments in photosynthetic pigments, which reflect major changes in the structure and organization of the photosynthetic apparatus.