Stomatal anatomy coordinates leaf size with Rubisco kinetics in the Balearic Limonium

Abstract

Trait integration arises through both selection on functional coordination and shared developmental pathways. Different anatomical components must both work well and develop together to generate individuals with the appropriate physiology to survive and reproduce in their environment. In this study, we used a common garden experiment and Bayesian multilevel models to test whether stomatal anatomy coordinates leaf gas exchange, Rubisco kinetics and leaf size across 10 closely related species of Limonium from the Balearic Islands. The results indicate that the anatomical determinants of maximum stomatal conductance, stomatal density and size, were functionally coordinated with Rubisco kinetics-species whose stomatal anatomy was correlated with low stomatal conductance have evolved Rubisco enzymes better adapted to low operational chloroplastic CO2 concentrations. Lower stomatal density was associated with greater leaf size, which can be explained by a greater proportion of pavement cells in large-leaved species. These results suggest that both selection for functional coordination (stomata and Rubisco kinetics) and shared development pathways (stomatal density and leaf area) likely shape patterns of trait integration between species. The genus Limonium is adapted to stressful environments in the Mediterranean Basin. There are important differences among species in the biochemical properties of the key enzyme fixing CO2, Rubisco and also in leaf size. This study demonstrates that variation in both Rubisco and leaf size across species is coordinated through stomatal traits. Moreover, trait relationships seen within Limonium are in some cases opposite to previous descriptions of very diverse species worldwide, which denotes that trait coordination within particular species groups may be variable.