Photosynthesis is currently a focus for crop improvement. The majority of this work has taken place and been assessed in leaves, and limited consideration has been given to the contribution that other green tissues make to whole-plant carbon assimilation. The major focus of this review is to evaluate the impact of non-foliar photosynthesis on carbon-use efficiency and total assimilation. Here we appraise and summarize past and current literature on the substantial contribution of different photosynthetically active organs and tissues to productivity in a variety of different plant types, with an emphasis on fruit and cereal crops. Previous studies provide evidence that non-leaf photosynthesis could be an unexploited potential target for crop improvement. We also briefly examine the role of stomata in non-foliar tissues, gas exchange, maintenance of optimal temperatures and thus photosynthesis. In the final section, we discuss possible opportunities to manipulate these processes and provide evidence that Triticum aestivum (wheat) plants genetically manipulated to increase leaf photosynthesis also displayed higher rates of ear assimilation, which translated to increased grain yield. By understanding these processes, we can start to provide insights into manipulating non-foliar photosynthesis and stomatal behaviour to identify novel targets for exploitation in continuing breeding programmes.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.14633

Photosynthesis in non-foliar tissues: implications for yield

A close correlation between stomatal conductance and the steady-state photosynthetic rate has been observed for diverse plant species under various environmental conditions. However, it remains unclear whether stomatal conductance is a major limiting factor for the photosynthetic rate under naturally fluctuating light conditions. We analysed a SLAC1 knockout rice line to examine the role of stomatal conductance in photosynthetic responses to fluctuating light. SLAC1 encodes a stomatal anion channel that regulates stomatal closure. Long exposures to weak light before treatments with strong light increased the photosynthetic induction time required for plants to reach a steady-state photosynthetic rate and also induced stomatal limitation of photosynthesis by restricting the diffusion of CO2 into leaves. The slac1 mutant exhibited a significantly higher rate of stomatal opening after an increase in irradiance than wild-type plants, leading to a higher rate of photosynthetic induction. Under natural conditions, in which irradiance levels are highly variable, the stomata of the slac1 mutant remained open to ensure efficient photosynthetic reaction. These observations reveal that stomatal conductance is important for regulating photosynthesis in rice plants in the natural environment with fluctuating light.

Increased stomatal conductance induces rapid changes to photosynthetic rate in response to naturally fluctuating light conditions in rice

Photosynthesis measurements are traditionally taken under steady-state conditions; however, leaves in crop fields experience frequent fluctuations in light and take time to respond. This slow response reduces the efficiency of carbon assimilation. Transitions from low to high light require photosynthetic induction, including the activation of Rubisco and the opening of stomata, whereas transitions from high to low light require the relaxation of dissipative energy processes, collectively known as non-photochemical quenching (NPQ). Previous attempts to assess the impact of these delays on net carbon assimilation have used simplified models of crop canopies, limiting the accuracy of predictions. Here, we use ray tracing to predict the spatial and temporal dynamics of lighting for a rendered mature Glycine max (soybean) canopy to review the relative importance of these delays on net cumulative assimilation over the course of both a sunny and a cloudy summer day. Combined limitations result in a 13% reduction in crop carbon assimilation on both sunny and cloudy days, with induction being more important on cloudy than on sunny days. Genetic variation in NPQ relaxation rates and photosynthetic induction in parental lines of a soybean nested association mapping (NAM) population was assessed. Short-term NPQ relaxation (<30 min) showed little variation across the NAM lines, but substantial variation was found in the speeds of photosynthetic induction, attributable to Rubisco activation. Over the course of a sunny and an intermittently cloudy day these would translate to substantial differences in total crop carbon assimilation. These findings suggest an unexplored potential for breeding improved photosynthetic potential in our major crops.

https://onlinelibrary.wiley.com/doi/epdf/10.1111/tpj.14663

Photosynthesis in the fleeting shadows: an overlooked opportunity for increasing crop productivity?

Dynamic light conditions require continuous adjustments of stomatal aperture. The kinetics of stomatal conductance (gs) are hypothesized to be key to plant productivity and water use efficiency. Using step-changes in light intensity, we studied the diversity of light-induced gs kinetics in relation to stomatal anatomy in five banana genotypes (Musa spp.) and modelled the impact of both diffusional and biochemical limitations on photosynthesis (A). The dominant photosynthesis limiting factor was the diffusional limitation associated with gs kinetics. All genotypes exhibited a strong limitation of A by gs, indicating a priority for water saving. Moreover, significant genotypic differences in gs kinetics and gslimitations of A were observed. For two contrasting genotypes the impact of differential gs kinetics was further investigated under realistic diurnally fluctuating light conditions and at whole-plant level. Genotype-specific stomatal kinetics observed at the leaf level were corroborated at whole-plant level by transpiration dynamics, validating that genotype-specific responses are still maintained despite differences in gs control at different locations in the leaf and across leaves. However, under diurnally fluctuating light conditions the impact of gs speediness on A and intrinsic water use efficiency (iWUE) depended on time of day. During the afternoon there was a setback in kinetics: absolute gs and gs responses to light were damped, strongly limiting A and impacting diurnal iWUE. We conclude the impact of differential gs kinetics depended on target light intensity, magnitude of change, gs prior to the change in light intensity and particularly time of day.

/pdf/the-impact-of-slow-stomatal-kinetics-on-photosynthesis-and-3in909zhii.pdf

The impact of slow stomatal kinetics on photosynthesis and water use efficiency under fluctuating light.

Crop water use efficiency (WUE) has come into sharp focus as population growth and climate change place increasing strain on the water used in cropping. Rainfed crops are being challenged by an upward trend in evaporative demand as average temperatures rise and, in many regions, there is an increased irregularity and a downward trend in rainfall. In addition, irrigated cropping faces declining water availability and increased competition from other users. Crop WUE would be improved by, first, ensuring that as much water as possible is actually transpired by the crop rather than being wasted. Deeper roots and greater early crop vigour are two traits that should help achieve this. Crop WUE would also be improved by achieving greater biomass per unit water transpired. A host of traits has been proposed to address this outcome. Restricting crop transpiration through lower stomatal conductance is assessed as having limited utility compared with traits that improve carbon gain, such as enhancements to photosynthetic biochemistry and responsiveness, or greater mesophyll conductance. Ultimately, the most useful outcomes for improved crop WUE will probably be achieved by combining traits to achieve synergistic benefit. The potential utility of trait combinations is supported by the results of crop simulation modelling.

/pdf/drying-times-plant-traits-to-improve-crop-water-use-18ap45ga2r.pdf

Drying times: plant traits to improve crop water use efficiency and yield.

Summary Although stomata are typically found in greater numbers on the abaxial surface, wheat flag leaves have greater densities on the adaxial surface. We determine the impact of this less common stomatal patterning on gaseous fluxes using a novel chamber that simultaneously measures both leaf surfaces. Using a combination of differential illuminations and CO2 concentrations at each leaf surface, we found that mesophyll cells associated with the adaxial leaf surface have a higher photosynthetic capacity than those associated with the abaxial leaf surface, which is supported by an increased stomatal conductance (driven by differences in stomatal density). When vertical gas flux at the abaxial leaf surface was blocked, no compensation by adaxial stomata was observed, suggesting each surface operates independently. Similar stomatal kinetics suggested some co‐ordination between the two surfaces, but factors other than light intensity played a role in these responses. Higher photosynthetic capacity on the adaxial surface facilitates greater carbon assimilation, along with higher adaxial stomatal conductance, which would also support greater evaporative leaf cooling to maintain optimal leaf temperatures for photosynthesis. Furthermore, abaxial gas exchange contributed c. 50% to leaf photosynthesis and therefore represents an important contributor to overall leaf gas exchange.

/pdf/stomata-on-the-abaxial-and-adaxial-leaf-surfaces-contribute-jczsoteg.pdf

Stomata on the abaxial and adaxial leaf surfaces contribute differently to leaf gas exchange and photosynthesis in wheat

Stomata are the primary gatekeepers for CO2 uptake for photosynthesis and water loss via transpiration and therefore play a central role in crop performance. Although stomatal conductance (gs ) and assimilation rate (A) are often highly correlated, studies have demonstrated an uncoupling between A and gs that can result in sub-optimal physiological processes in dynamic light environments. Wheat (Triticum aestivum L.) is exposed to changes in irradiance due to leaf self-shading, moving clouds and shifting sun angle to which both A and gs respond. However, stomatal responses are generally an order of magnitude slower than photosynthetic responses, leading to non-synchronized A and gs responses that impact CO2 uptake and water use efficiency ( iWUE). Here we phenotyped a panel of eight wheat cultivars (estimated to capture 80% of the single nucleotide polymorphism variation in North-West European bread wheat) for differences in the speed of stomatal responses (to changes in light intensity) and photosynthetic performance at different stages of development. The impact of water stress and elevated [CO2] on stomatal kinetics was also examined in a selected cultivar. Significant genotypic variation was reported for the time constant for stomatal opening (Ki, P = 0.038) and the time to reach 95% steady state A (P = 0.045). Slow gs opening responses limited A by ∼10% and slow closure reduced iWUE, with these impacts found to be greatest in cultivars Soissons, Alchemy and Xi19. A decrease in stomatal rapidity (and thus an increase in the limitation of photosynthesis) (P < 0.001) was found during the post-anthesis stage compared to the early booting stage. Reduced water availability triggered stomatal closure and asymmetric stomatal opening and closing responses, while elevated atmospheric [CO2] conditions reduced the time for stomatal opening during a low to high light transition, thus suggesting a major environmental effect on dynamic stomatal kinetics. We discuss these findings in terms of exploiting various traits to develop ideotypes for specific environments, and suggest that intraspecific variation in the rapidity of stomatal responses could provide a potential unexploited breeding target to optimize the physiological responses of wheat to dynamic field conditions.

/pdf/genotypic-developmental-and-environmental-effects-on-the-cbtnvb3mp4.pdf

Genotypic, Developmental and Environmental Effects on the Rapidity of gs in Wheat: Impacts on Carbon Gain and Water-Use Efficiency.

There remains an ongoing need to make crops more productive in the face of further increases in atmospheric CO2 concentrations as predicted under climate change, along with higher global surface temperatures and more prolonged, severe and frequent periods of drought. With over 90% of water transpired by plants diffusing through their stomata, studying these small, morphologically varied valves in leaf surfaces remains critical to our understanding the consequences of climate change on stomatal responses, and by extension crop productivity. In the short term, stomata adjust their aperture in response to changes in environmental variables affecting carbon assimilation and water loss. In the longer term, adjustments to stomatal density and size may occur, in conjunction with a range of other responses from the plant. While increasing CO2 concentration under climate change had been shown to raise yields and reduce water use by partial stomatal closure, the extent of the fertilisation effect has not been as strong as expected. Meanwhile, higher temperatures and decreasing water availability are likely to have negative yield consequences, with divergent expectations for stomatal aperture and consequently plant water use. However, changes in environmental factors will not occur in isolation and therefore stomatal and plant responses to a combination of these changes will be hierarchical and involve multiple and possibly unique signalling pathways. Predicting stomatal responses to several simultaneous abiotic stresses such as those outlined above adds a layer of complexity, notably where the stresses produce antagonistic responses in the plant. Targeting steady- state stomatal behaviour has been a successful breeding tactic to date, and continues to generate new insights under interacting stresses. Meanwhile, the emerging field of dynamic stomatal responses to environmental stresses offers new phenotypic targets, and the possibility for enhancing water use efficiency by targeting novel signalling and molecular pathways in stomatal responses.

Stomatal responses to climate change

Carbon fixation

There remains an ongoing need to make crops more productive in the face of further increases in atmospheric CO2 concentrations as predicted under climate change, along with higher global surface temperatures and more prolonged, severe and frequent periods of drought. With over 90 % of water transpired by plants diffusing through stomata, studying these small, morphologically varied valves in leaf surfaces remains critical to our understanding the consequences of climate change on stomatal responses, and by extension crop productivity. In the short term, stomata adjust aperture in response to changes in environmental variables affecting carbon assimilation and water loss. In the longer term, adjustments to stomatal density and size may occur, in conjunction with a range of other responses from the plant.

Chapter 2 Stomatal Responses to Climate Change

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