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

Abstract

Stomata are the primary gatekeepers for CO 2 uptake for photosynthesis and water loss via transpiration and therefore play a central role in crop performance. Although stomatal conductance ( g s ) and assimilation rate ( A ) are often highly correlated, studies have demonstrated an uncoupling between A and g s 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 g s respond. However, stomatal responses are generally an order of magnitude slower than photosynthetic responses, leading to non-synchronized A and g s responses that impact CO 2 uptake and water use efficiency ( i WUE ). 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 [CO 2 ] on stomatal kinetics was also examined in a selected cultivar. Significant genotypic variation was reported for the time constant for stomatal opening ( K i , P = 0.038) and the time to reach 95% steady state A ( P = 0.045). Slow g s opening responses limited A by ∼10% and slow closure reduced i WUE , 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 [CO 2 ] 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.

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

“…This gains support from the observation that in wheat and soybean, intercellular [CO 2 ] is higher during induction than at steady state (Soleh et al , ; Taylor and Long, ), whereas the converse would be expected if stomatal opening was the dominant factor. In other species the speed of stomatal opening appears to be the dominant limitation limiting the speed of induction (McAusland et al , ; De Souza et al , ), and this may be accentuated under stress conditions (Faralli et al , ). In the current study, only the activation of Rubisco by Rca was considered, so the losses resulting from slow induction must be considered a minimum, where slow increases in stomatal and mesophyll conductance could exacerbate these losses.…”

“…Sufficient accumulation of ribulose 1,5-bisphoshate is assumed to require approximately 60 sec, whereas the activation of Rubisco may require more than 10 min (Mott and Woodrow, 2000;Taylor and Long, 2017). At the leaf level, induction can be limited by slow stomatal opening, where full opening can require many minutes (McAusland et al, 2016;De Souza et al, 2019;Faralli et al, 2019;Acevedo-Siaca et al, 2020), and by mesophyll conductance, which generally increases with incident light. The rate of increase in mesophyll conductance upon induction is generally considered faster than both stomatal opening and Rubisco activation (Deans et al, 2019), but the variability between species and environmental conditions is not well defined.…”

Natural genetic variation in photosynthesis: an untapped resource to increase crop yield potential?

“…However, restrictions on growing genetically modified crops in many countries especially in Europe means that alternative methods to achieve increases in photosynthesis must be realized. An undervalued and currently unexploited opportunity to increase yield, not mutually exclusive of genetic engineering approaches, is the extensive natural variation in photosynthetic capacity in different C 3 crops (Rawson et al , ; Blum, ; Watanabe et al , ; Fischer et al , ; Hervé et al , ; Pettigrew, ; Flood et al , ; Gu et al , ; Lawson et al , ; Driever et al , ; Gaju et al , ; Carmo‐Silva et al , ; Qu et al , ; Pater et al , ; Faralli et al , ). A number of studies have explored natural variation in photosynthesis in commercial wheat varieties (often relative to the year of release) (Fischer et al , , ; Blum, ; Watanabe et al , ; Reynolds et al , ; Xue et al , ; Chytyk et al , ; Sadras et al , ), and demonstrated a correlation between photosynthesis and yield (e.g.…”

“…Variation in photosynthesis has been attributed to differences in radiation use efficiency (Sadras et al , ), biochemical differences in RuBisCO activation properties (Carmo‐Silva and Salvucci, ), carboxylation efficiency (Driever et al , ) and electron transport capacity (Carmo‐Silva et al , ). In addition, variations in traits limiting the diffusion of CO 2 to the site of carboxylation including mesophyll conductance ( g m ) (Jahan et al , ) and stomatal conductance ( g s ) (Fischer et al , ), which also includes the rapidity of g s responses to changing environmental conditions (Lawson et al , , ; Faralli et al , ) have been reported in several crops.…”

Photosynthesis in non‐foliar tissues: implications for yield

“…Several studies have demonstrated that the stomatal density in the flag leaf of wheat varies between 40 and 90 mm À2 (e.g. Faralli et al, 2019a), and that in ear organs the stomatal density can be either higher (Kong et al, 2015) or drastically lower (Tambussi et al, 2005) than in the leaf. Furthermore, different stomatal densities and distributions have been reported on both the ventral and the dorsal sides of the glume and the lemma (Figure 3), with the lemma showing variable density depending on the shading area of the neighbouring glume (Tambussi et al, 2005).…”