Contrasting adaptation and optimization of stomatal traits across communities at continental-scale

The maximum stomatal conductance (g), a major anatomical constraint on plant productivity, is a function of the stomatal area fraction (f) and stomatal space-use efficiency (e). However, f and g have been considered as equivalents, with e rarely considered, and their adaptation to the environment and their regulation of ecosystem productivity are unclear. Here, we analyzed the community-weighted mean, variance, skewness, and kurtosis of stomatal traits from tropical to cold-temperature forests. The variance of g and f was higher for arid sites, indicating greater functional niche differentiation, whereas that for e was lower, indicating convergence in efficiency. Besides, when other stomatal trait distributions remained unchanged, increasing kurtosis but decreasing skewness of g would improve ecosystem productivity, and f showed the opposite patterns. These findings highlight how the relative importance and equivalence of inter-related traits can differ at community scale.

Developmental integration cannot explain major features of stomatal anatomical evolution in seed plants

Developmental integration can cause traits to covary over macroevolutionary time and in some cases prevent populations from reaching their adaptive optima. Developmental integration between stomatal size and density may contribute to two major features of stomatal anatomical evolution: inverse size-density scaling and bimodal stomatal ratio. If these patterns result from developmental integration, we predicted that in amphistomatous leaves 1) stomatal size and density should covary similarly on both abaxial and adaxial surfaces and 2) stomatal traits (size and density) on each surface should covary isometrically. We synthesized data on stomatal density and length from amphistomatous leaves of 711 terrestrial seed plant taxa mostly from the literature. We estimated the covariance in divergence between stomatal traits from 327 phylogenetically independent contrasts using a robust Bayesian model. Adaxial stomatal density, but not length, is evolutionarily labile and not strongly integrated with stomatal length or abaxial stomatal density. Hence, developmental integration alone cannot explain inverse size-density scaling nor bimodal stomatal ratio. Quasi-independent evolution of stomatal anatomical traits facilitates largely unfettered access to fitness optima. If stomatal anatomical traits are near their current fitness optimum, this implies that limits on trait (co)variance result from selective rather than developmental constraints. However, we cannot rule out that developmental integration is important in some lineages. Future research should identify the mechanistic basis of(dis)integration in stomatal development.

Loading regulation prevents phloem failure during drought and widens the range of phloem and stomatal traits

Plant carbon transport is controlled by a multitude of parameters both internal and external to the sugar transporting phloem tissue. Sucrose transporter kinetics, conduit hydraulic resistance, and xylem water stress are all hypothesized to impact the amount of carbon delivered to sink tissues. However, the most important traits determining carbon export under drought are not well understood, especially for species with active molecular regulation of sucrose transport. This in turn limits our ability to assess species’ resistances to phloem dysfunction under drought. Here, we use an integrated xylem-phloem-stomatal model to calculate leaf water potential from soil dryness, which is then used to determine gas exchange and phloem pressure gradients. We quantitatively compare the impacts of phloem loading kinetics, including feedbacks between loading and phloem pressure, phloem conduit resistances, and stomatal responses to water stress, on the total carbon export to sinks during drought. Regulating sucrose transporter kinetics which downregulates loading at high phloem pressures prevented runaway viscosity in the phloem sap and was the most important determinant of export rates under drought. In contrast to previous models, we found this feedback mechanism decoupled stomatal traits from phloem export efficiency during drought and increased the operational range of phloem hydraulic resistances.

Variation in climatic tolerance, but not stomatal traits, partially explains Pooideae grass species distributions

Background and Aims Grasses in subfamily Pooideae live in some of the world’s harshest terrestrial environments, from frigid boreal zones to the arid wind-swept steppe. It is hypothesized that the climate distribution of species within this group is driven by differences in climatic tolerance, and that tolerance can be partially explained by variation in stomatal traits. Methods We determined aridity index (AI) and minimum temperature of the coldest month (MTCM) for 22 diverse Pooideae accessions and one outgroup, and used comparative methods to assess predicted relationships for climate traits versus fitness traits, stomatal diffusive conductance to water (gw), and speed of stomatal closure following drought and/or cold. Key Results Results demonstrate that AI and MTCM predict variation in survival/regreening following drought/cold, and gw under drought/cold is positively correlated with ẟ 13C-measured water use efficiency (WUE). However, the relationship between climate traits and fitness under drought/cold was not explained by gw or speed of stomatal closure. Conclusions These findings suggest that Pooideae distributions are at least partly determined by tolerance to aridity and above freezing cold, but that variation in tolerance is not uniformly explained by variation in stomatal traits.