Examining the mechanisms by which photosynthetic capacity and water use efficiency are regulated in wheat exposed to soil drying

Wheat contributes significantly to human nutrition and livelihoods around the world, but is highly susceptible to drought stress, which is expected to become more prevalent as the climate changes. Therefore, it is increasingly important to assess wheat genotypic variability for tolerance to water deficit and design screening techniques for use in breeding programs. However, genetic variation in whole plant water use efficiency (WUEwp, - biomass per water used) is not always correlated with variation in leaf level water use efficiency (WUEi - assimilation per stomatal conductance), increasing the difficulty of phenotypic prediction. To understand the disconnect, a mix of spring wheat cultivars and landraces from the Watkins collection were examined for variation in the mechanisms regulating biomass gain (BM) and water use (WU) as components of WUEwp. Specifically, the impact of leaf age and soil drying on stomatal conductance (gs) and assimilation (A) were assessed. Significant variation was observed for WUEwp (two-fold), with genotypes Krichauff and G1 (Watkins) consistently displaying high WUEwp and Gatsby low WUEwp. Increased WUEi was correlated with increased WUEwp, even though no significant genetic variation was observed for WUEi. Additionally, sustained A across leaf age was observed in Krichauff but not Gatsby, corresponding with their measures of WUEwp. Further, lower levels of photosynthetic limitation by rubisco (Vcmax) and decreased leaf biomass partitioning (LP) were correlated to higher WUEwp. While WUEi may not always predict variation in WUEwp, other variables (Vcmax, LP, and sustainability of A across leaf age) were strongly associated with the whole plant response. Thus, in vivo measures of photosynthetic limitation and other whole plant proxies, such as area-based estimates of leaf partitioning, serve as useful tools in predicting WUEwp

Photoprotection and optimization of sucrose usage contribute to faster recovery of photosynthesis after water deficit at high temperatures in wheat

Plants are increasingly exposed to events of elevated temperature and water deficit, which threaten crop productivity. Understanding the ability to rapidly recover from abiotic stress, restoring carbon assimilation and biomass production, is important to unravel crop climate resilience. This study compared the photosynthetic performance of two Triticum aestivum L. cultivars, Sokoll and Paragon, adapted to the climate of Mexico and UK, respectively, exposed to one week water deficit and high temperatures, in isolation or combination. Measurements included photosynthetic assimilation rate, stomatal conductance, in vitro activities of Rubisco (EC 4.1.1.39) and invertase (INV, EC 3.2.1.26), antioxidant capacity and chlorophyll a fluorescence. In both genotypes, under elevated temperatures and water deficit (WD38℃), the photosynthetic limitations were mainly due to stomatal restrictions and to a decrease in the electron transport rate. Chlorophyll a fluorescence parameters clearly indicate differences between the two genotypes in the photoprotection when subjected to WD38℃ and showed faster recovery of Paragon after stress relief. The activity of the cytosolic invertase (CytINV) under these stress conditions was strongly related to the fast photosynthesis recovery of Paragon. Taken together, the results suggest that optimal sucrose export/utilization and increased photoprotection of the electron transport machinery are important components to limit yield fluctuations due to water shortage and elevated temperatures

Heat-induced changes in the abundance of wheat Rubisco activase isoforms

The Triticum aestivum (wheat) genome encodes three isoforms of Rubisco activase (Rca) differing in thermostability, which could be exploited to improve the resilience of this crop to global warming. We hypothesized that elevated temperatures would cause an increase in the relative abundance of heat‐stable Rca1β. Wheat plants were grown at 25° C : 18°C (day : night) and exposed to heat stress (38° C : 22°C) for up to 5 d at pre‐anthesis. Carbon (C) assimilation, Rubisco activity, CA1Pase activity, transcripts of Rca1β, Rca2β, and Rca2α, and the quantities of the corresponding protein products were measured during and after heat stress. The transcript of Rca1β increased 40‐fold in 4 h at elevated temperatures and returned to the original level after 4 h upon return of plants to control temperatures. Rca1β comprised up to 2% of the total Rca protein in unstressed leaves but increased three‐fold in leaves exposed to elevated temperatures for 5 d and remained high at 4 h after heat stress. These results show that elevated temperatures cause rapid changes in Rca gene expression and adaptive changes in Rca isoform abundance. The improved understanding of the regulation of C assimilation under heat stress will inform efforts to improve wheat productivity and climate resilience

Acclimation of biochemical and diffusive components of photosynthesis in rice, wheat and maize to heat and water deficit:implications for modeling photosynthesis

The impact of the combined effects of heat stress, increased vapor pressure deficit (VPD) and water deficit on the physiology of major crops needs to be better understood to help identify the expected negative consequences of climate change and heat waves on global agricultural productivity. To address this issue, rice, wheat and maize plants were grown under control temperature (CT, 25°C, VPD 1.8 kPa), and a high temperature (HT, 38°C, VPD 3.5 kPa), both under well-watered (WW) and water deficit (WD) conditions. Gas-exchange measurements showed that, in general, WD conditions affected the leaf conductance to CO2, while growth at HT had a more marked effect on the biochemistry of photosynthesis. When combined, HT and WD had an additive effect in limiting photosynthesis. The negative impacts of the imposed treatments on the processes governing leaf gas-exchange were species-dependent. Wheat presented a higher sensitivity while rice and maize showed a higher acclimation potential to increased temperature. Rubisco and PEPC kinetic constants determined in vitro at 25°C and 38°C were used to estimated Vcmax, Jmax and Vpmax in the modeling of C3 and C4 photosynthesis. The results here obtained reiterate the need to use species-specific and temperature-specific values for Rubisco and PEPC kinetic constants for a precise parameterization of the photosynthetic response to changing environmental conditions in different crop species

Photosynthesis across African cassava germplasm is limited by Rubisco and mesophyll conductance at steady-state, but by stomatal conductance in fluctuating light

Sub‐Saharan Africa is projected to see a 55% increase in food demand by 2035, where cassava (Manihot esculenta) is the most planted crop and a major calorie source. Cassava yield has not increased significantly for 13 years. Improvement of genetic yield potential, the basis of the first Green Revolution, could be increased by improving photosynthetic efficiency. First, the factors limiting photosynthesis and their genetic variability within extant germplasm must be understood. Biochemical and diffusive limitations to leaf photosynthetic CO2 uptake under steady‐state and fluctuating light in thirteen farm‐preferred and high‐yielding African cultivars were analyzed. A cassava leaf metabolic model was developed to quantify the value of overcoming limitations to leaf photosynthesis. At steady‐state, in vivo Rubisco activity and mesophyll conductance accounted for 84% of the limitation whereas under non‐steady‐state conditions of shade to sun transition stomatal conductance was the major limitation contributing resulting in an estimated 13% and 5% losses in CO2 uptake and water use efficiency, across a diurnal period. Triose phosphate utilization, while sufficient to support observed rates, would limit improvement in leaf photosynthesis to 33%, unless improved itself. The variation of carbon assimilation among cultivars were three times greater under non‐steady‐state compared to steady‐state, pinpointing important overlooked breeding targets for improved photosynthetic efficiency in cassava

Dynamics of Rubisco regulation by sugar phosphate derivatives and their phosphatases

Regulating the central CO2-fixing enzyme Rubisco is as complex as its ancient reaction mechanism and involves interaction with a series of co-factors and auxiliary proteins that activate catalytic sites and maintain activity. A key component among the regulatory mechanisms is the binding of sugar phosphate derivatives that inhibit activity. Removal of inhibitors via the action of Rubisco activase is required to restore catalytic competency. In addition, specific phosphatases dephosphorylate newly released inhibitors, rendering them incapable of binding to Rubisco catalytic sites. The best studied inhibitor is 2-carboxy-D-arabinitol 1-phosphate (CA1P), a naturally occurring nocturnal inhibitor that accumulates in most species during darkness and low light, progressively binding to Rubisco. As light increases, Rubisco activase removes CA1P from Rubisco, and the specific phosphatase CA1Pase dephosphorylates CA1P to CA, which cannot bind Rubisco. Misfire products of Rubisco’s complex reaction chemistry can also act as inhibitors. One example is xylulose-1,5-bisphosphate (XuBP), which is dephosphorylated by XuBPase. Here we revisit key findings related to sugar phosphate derivatives and their specific phosphatases, highlighting outstanding questions and how further consideration of these inhibitors and their role is important for better understanding the regulation of carbon assimilation

Rubisco and carbon-concentrating mechanism co-evolution across chlorophyte and streptophyte green algae.

Green algae expressing a carbon-concentrating mechanism (CCM) are usually associated with a Rubisco-containing micro-compartment, the pyrenoid. A link between the small subunit (SSU) of Rubisco and pyrenoid formation in Chlamydomonas reinhardtii has previously suggested that specific RbcS residues could explain pyrenoid occurrence in green algae. A phylogeny of RbcS was used to compare the protein sequence and CCM distribution across the green algae and positive selection in RbcS was estimated. For six streptophyte algae, Rubisco catalytic properties, affinity for CO2 uptake (K0.5 ), carbon isotope discrimination (δ13 C) and pyrenoid morphology were compared. The length of the βA-βB loop in RbcS provided a phylogenetic marker discriminating chlorophyte from streptophyte green algae. Rubisco kinetic properties in streptophyte algae have responded to the extent of inducible CCM activity, as indicated by changes in inorganic carbon uptake affinity, δ13 C and pyrenoid ultrastructure between high and low CO2 conditions for growth. We conclude that the Rubisco catalytic properties found in streptophyte algae have coevolved and reflect the strength of any CCM or degree of pyrenoid leakiness, and limitations to inorganic carbon in the aquatic habitat, whereas Rubisco in extant land plants reflects more recent selective pressures associated with improved diffusive supply of the terrestrial environment.NE/L002507/1, BB/M007693/1, BB/I024518/1 (NERC, BBSRC and NSF). A Cambridge Trust Vice Chancellor’s award and Lucy Cavendish College, Cambridge, for supporting the PhD scholarship of MMMG. DJO and ECS acknowledge support from (BBSRC; grant number BB/I024488/1)

Stability of wheat grain yields over three field seasons in the UK

Ensuring food security in a changing climate is a major contemporary challenge and requires development of climate resilient crops that perform well under variable environments. The hypothesis that yield stability in sub-optimal conditions is linked to yield penalties in optimal conditions was investigated in field-grown wheat in the UK. The phenotypic responses, rate of wheat crop development and final grain yield, to varying sowing date, rainfall, air temperature and radiation patterns were studied for a panel of 61 elite commercial wheat cultivars grown in the UK in 2012, 2013 and 2014. Contrasting climatic patterns, particularly rainfall accumulation and distribution over the season, influenced the relative performance of the cultivars affecting the duration of grain development stage and impacting on productivity. Indices for crop productivity, yield stability and performance under sub-optimal conditions revealed four cultivars with a combination of stable and high relative grain yields over the three seasons: Gladiator, Humber, Mercato and Zebedee. Genetic similarity between cultivars partially explained yield performance in the contrasting seasons. The year of release of the cultivars correlated with grain yield but not with yield stability, supporting the contention that breeding for yield potential does not select for climate resilience and yield stability of crops. Further analysis of the outstanding cultivars may unravel target traits for breeding efforts aimed at increasing wheat yield potential and stability in the changing climate. This article is protected by copyright. All rights reserved