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.
We review current knowledge on the effect of cell wall properties, particularly thickness and composition, on mesophyll conductance to CO2 diffusion and photosynthesis in land plants.
Abstract
The ...key role of cell walls in setting mesophyll conductance to CO2 (gm) and, consequently, photosynthesis is reviewed. First, the theoretical properties of cell walls that can affect gm are presented. Then, we focus on cell wall thickness (Tcw) reviewing empirical evidence showing that Tcw varies strongly among species and phylogenetic groups in a way that correlates with gm and photosynthesis; that is, the thicker the mesophyll cell walls, the lower the gm and photosynthesis. Potential interplays of gm, Tcw, dehydration tolerance, and hydraulic properties of leaves are also discussed. Dynamic variations of Tcw in response to the environment and their implications in the regulation of photosynthesis are discussed, and recent evidence suggesting an influence of cell wall composition on gm is presented. We then propose a hypothetical mechanism for the influence of cell walls on photosynthesis, combining the effects of thickness and composition, particularly pectins. Finally, we discuss the prospects for using biotechnology for enhancing photosynthesis by altering cell wall-related genes.
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 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.
Summary
Cell wall thickness is widely recognized as one of the main determinants of mesophyll conductance to CO2 (gm). However, little is known about the components that regulate effective CO2 ...diffusivity in the cell wall (i.e. the ratio between actual porosity and tortuosity, the other two biophysical diffusion properties of cell walls). The aim of this study was to assess, at the interspecific level, potential relationships between cell wall composition, cell wall thickness (Tcw) and gm. Gymnosperms constitute an ideal group to deepen these relationships, as they present, on average, the thickest cell walls within spermatophytes. We characterized the foliar gas exchange, the morphoanatomical traits related with gm, the leaf fraction constituted by cell walls and three main components of primary cell walls (hemicelluloses, cellulose and pectins) in seven gymnosperm species. We found that, although the relatively low gm of gymnosperms was mainly determined by their elevated Tcw, gm was also strongly correlated with cell wall composition, which presumably sets the final effective CO2 diffusivity. The data presented here suggest that (i) differences in gm are strongly correlated to the pectins to hemicelluloses and cellulose ratio in gymnosperms, and (ii) variations in cell wall composition may modify effective CO2 diffusivity in the cell wall to compensate the negative impact of thickened walls. We speculate that higher relative pectin content allows higher gm because pectins increase cell wall hydrophilicity and CO2 molecules cross the wall dissolved in water.
Significance Statement
Cell walls impose a substantial CO2 diffusion resistance, generally increasing their constraint to photosynthesis with increasing wall thickness. However, the effect of cell wall composition on mesophyll conductance is largely unknown, and no interspecific comparison has been made yet. This study reveals the strong effect of the relative cell wall content in cellulose, hemicelluloses and pectins on mesophyll conductance in gymnosperms, thus expanding the knowledge of the mechanistic basics of internal CO2 diffusion resistance.
Summary
Mesophyll conductance (gm), the diffusion of CO2 from substomatal cavities to the carboxylation sites in the chloroplasts, is a highly complex trait driving photosynthesis (net CO2 ...assimilation, AN). However, little is known concerning the mechanisms by which it is dynamically regulated. The apoplast is considered as a ‘key information bridge’ between the environment and cells. Interestingly, most of the environmental constraints affecting gm also cause apoplastic responses, cell wall (CW) alterations and metabolic rearrangements. Since CW thickness is a key determinant of gm, we hypothesize that other changes in this cellular compartiment should also influence gm. We study the relationship between the antioxidant apoplastic system and CW metabolism and the gm responses in tobacco plants (Nicotiana sylvestris L.) under two abiotic stresses (drought and salinity), combining in vivo gas‐exchange measurements with analyses of antioxidant activities, CW composition and primary metabolism. Stress treatments imposed substantial reductions in AN (58–54%) and gm (59%), accompanied by a strong antioxidant enzymatic response at the apoplastic and symplastic levels. Interestingly, apoplastic but not symplastic peroxidases were positively related to gm. Leaf anatomy remained mostly stable; however, the stress treatments significantly affected the CW composition, specifically pectins, which showed significant relationships with AN and gm. The treatments additionally promoted a differential primary metabolic response, and specific CW‐related metabolites including galactose, glucosamine and hydroxycinnamate showed exclusive relationships with gm independent of the stress. These results suggest that gm responses can be attributed to specific changes in the apoplastic antioxidant system and CW metabolism, opening up more possibilities for improving photosynthesis using breeding/biotechnological strategies.
Significance Statement
Mesophyll conductance is a complex trait which imposes considerable limitations on photosynthesis. However, beyond the current knowledge from gas‐exchange measurements and anatomical characterization, the mechanisms driving its dynamic response to the environment are still poorly understood. Here, we relate changes in apoplastic antioxidant metabolism, cell wall composition and primary metabolism with responses of mesophyll conductance to different abiotic stresses. This information improves our understanding about mesophyll conductance responses and opens up more possibilities to improve photosynthetic performance.
Born to revive Fernández-Marín, Beatriz; Nadal, Miquel; Gago, Jorge ...
New phytologist,
20/May , Letnik:
226, Številka:
3
Journal Article
Recenzirano
Odprti dostop
• Resurrection plants recover physiological functions after complete desiccation. Almost all of them are native to tropical warm environments. However, the Gesneriaceae include four genera, remnant ...of the past palaeotropical flora, which inhabit temperate mountains. One of these species is additionally freezing-tolerant: Ramonda myconi. We hypothesise that this species has been able to persist in a colder climate thanks to some resurrection-linked traits.
• To disentangle the physiological mechanisms underpinning multistress tolerance to desiccation and freezing, we conducted an exhaustive seasonal assessment of photosynthesis (gas exchange, limitations to partitioning, photochemistry and galactolipids) and primary metabolism (through metabolomics) in two natural populations at different elevations.
• R. myconi displayed low rates of photosynthesis, largely due to mesophyll limitation. However, plants were photosynthetically active throughout the year, excluding a reversible desiccation period. Common responses to desiccation and low temperature involved chloroplast protection: enhanced thermal energy dissipation, higher carotenoid to Chl ratio and de-epoxidation of the xanthophyll cycle. As specific responses, antioxidants and secondary metabolic routes rose upon desiccation, while putrescine, proline and a variety of sugars rose in winter.
• The data suggest conserved mechanisms to cope with photo-oxidation during desiccation and cold events, while additional metabolic mechanisms may have evolved as specific adaptations to cold during recent glaciations
Besides stomata, the photosynthetic CO2 pathway also involves the transport of CO2 from the sub-stomatal air spaces inside to the carboxylation sites in the chloroplast stroma, where Rubisco is ...located. This pathway is far to be a simple and direct way, formed by series of consecutive barriers that the CO2 should cross to be finally assimilated in photosynthesis, known as the mesophyll conductance (gm). Therefore, the gm reflects the pathway through different air, water and biophysical barriers within the leaf tissues and cell structures. Currently, it is known that gm can impose the same level of limitation (or even higher depending of the conditions) to photosynthesis than the wider known stomata or biochemistry. In this mini-review, we are focused on each of the gm determinants to summarize the current knowledge on the mechanisms driving gm from anatomical to metabolic and biochemical perspectives. Special attention deserve the latest studies demonstrating the importance of the molecular mechanisms driving anatomical traits as cell wall and the chloroplast surface exposed to the mesophyll airspaces (Sc/S) that significantly constrain gm. However, even considering these recent discoveries, still is poorly understood the mechanisms about signaling pathways linking the environment a/biotic stressors with gm responses. Thus, considering the main role of gm as a major driver of the CO2 availability at the carboxylation sites, future studies into these aspects will help us to understand photosynthesis responses in a global change framework.
ABSTRACT
In a previous study, important acclimation to water stress was observed in the Ramellet tomato cultivar (TR) from the Balearic Islands, related to an increase in the water‐use efficiency ...through modifications in both stomatal (gs) and mesophyll conductances (gm). In the present work, the comparison of physiological and morphological traits between TR accessions grown with and without water stress confirmed that variability in the photosynthetic capacity was mostly explained by differences in the diffusion of CO2 through stomata and leaf mesophyll. Maximization of gm under both treatments was mainly achieved through adjustments in the mesophyll thickness and porosity and the surface area of chloroplasts exposed to intercellular airspace (Sc). In addition, the lower gm/Sc ratio for a given porosity in drought‐acclimated plants suggests that the decrease in gm was due to an increased cell wall thickness. Stomatal conductance was also affected by drought‐associated changes in the morphological properties of stomata, in an accession and treatment‐dependent manner. The results confirm the presence of advantageous physiological traits in the response to drought stress in Mediterranean accessions of tomato, and relate them to particular changes in the leaf anatomical properties, suggesting specific adaptive processes operating at the leaf anatomical level.
The Balearic ‘Ramellet’ tomato cultivar showed acclimation to drought stress based on increased water use efficiency, resulting from the modification of stomatal and mesophyll (gm) conductances. In this work, we found that reasons behind gm increases are related to modification of mesophyll thickness and porosity, surface area of chloroplasts exposed to intercellular airspace (Sc) and gm/Sc ratio. Since that, leaf anatomical modifications, rather than biochemical factors, underlie physiological acclimation to water stress in ‘Ramellet’.
Summary
In this work, we review the physiological and molecular mechanisms that allow vascular plants to perform photosynthesis in extreme environments, such as deserts, polar and alpine ecosystems. ...Specifically, we discuss the morpho/anatomical, photochemical and metabolic adaptive processes that enable a positive carbon balance in photosynthetic tissues under extreme temperatures and/or severe water‐limiting conditions in C3 species. Nevertheless, only a few studies have described the in situ functioning of photoprotection in plants from extreme environments, given the intrinsic difficulties of fieldwork in remote places. However, they cover a substantial geographical and functional range, which allowed us to describe some general trends. In general, photoprotection relies on the same mechanisms as those operating in the remaining plant species, ranging from enhanced morphological photoprotection to increased scavenging of oxidative products such as reactive oxygen species. Much less information is available about the main physiological and biochemical drivers of photosynthesis: stomatal conductance (gs), mesophyll conductance (gm) and carbon fixation, mostly driven by RuBisCO carboxylation. Extreme environments shape adaptations in structures, such as cell wall and membrane composition, the concentration and activation state of Calvin–Benson cycle enzymes, and RuBisCO evolution, optimizing kinetic traits to ensure functionality. Altogether, these species display a combination of rearrangements, from the whole‐plant level to the molecular scale, to sustain a positive carbon balance in some of the most hostile environments on Earth.
Significance Statement
The molecular and physiological mechanisms that drive photosynthesis in vascular species from extreme environments still remain largely unknown. Here we review the different adaptations (from the whole plant to the molecular level) that enable plants to succeed and sustain an annual positive carbon balance under the typical short and harsh growing seasons in these environments.
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