How and why do species break a developmental trade-off? Elucidating the association of trichomes and stomata across species.

PREMISE: Previous studies have suggested a trade-off between trichome density (Dt) and stomatal density (Ds) due to shared cell precursors. We clarified how, when, and why this developmental trade-off may be overcome across species. METHODS: We derived equations to determine the developmental basis for Dt and Ds in trichome and stomatal indices (it and is) and the sizes of epidermal pavement cells (e), trichome bases (t), and stomata (s) and quantified the importance of these determinants of Dt and Ds for 78 California species. We compiled 17 previous studies of Dt-Ds relationships to determine the commonness of Dt-Ds associations. We modeled the consequences of different Dt-Ds associations for plant carbon balance. RESULTS: Our analyses showed that higher Dt was determined by higher it and lower e, and higher Ds by higher is and lower e. Across California species, positive Dt-Ds coordination arose due to it-is coordination and impacts of the variation in e. A Dt-Ds trade-off was found in only 30% of studies. Heuristic modeling showed that species sets would have the highest carbon balance with a positive or negative relationship or decoupling of Dt and Ds, depending on environmental conditions. CONCLUSIONS: Shared precursor cells of trichomes and stomata do not limit higher numbers of both cell types or drive a general Dt-Ds trade-off across species. This developmental flexibility across diverse species enables different Dt-Ds associations according to environmental pressures. Developmental trait analysis can clarify how contrasting trait associations would arise within and across species.

Developmental and biophysical determinants of grass leaf size worldwide.

One of the most notable ecological trends-described more than 2,300  years ago by Theophrastus-is the association of small leaves with dry and cold climates, which has recently been recognized for eudicotyledonous plants at a global scale1-3. For eudicotyledons, this pattern has been attributed to the fact that small leaves have a thinner boundary layer that helps to avoid extreme leaf temperatures4 and their leaf development results in vein traits that improve water transport under cold or dry climates5,6. However, the global distribution of leaf size and its adaptive basis have not been tested in the grasses, which represent a diverse lineage that is distinct in leaf morphology and that contributes 33% of terrestrial primary productivity (including the bulk of crop production)7. Here we demonstrate that grasses have shorter and narrower leaves under colder and drier climates worldwide. We show that small grass leaves have thermal advantages and vein development that contrast with those of eudicotyledons, but that also explain the abundance of small leaves in cold and dry climates. The worldwide distribution of leaf size in grasses exemplifies how biophysical and developmental processes result in convergence across major lineages in adaptation to climate globally, and highlights the importance of leaf size and venation architecture for grass performance in past, present and future ecosystems.

Optimal Community Assembly Related to Leaf Economic- Hydraulic-Anatomical Traits.

Multi-dimensional trait mechanisms underlying community assembly at regional scales are largely unclear. In this study, we measured leaf economic, hydraulic and anatomical traits of 394 tree species from tropical to cold temperate forests, from which we calculated the leaf trait moments (mean, variance, skewness, and kurtosis) using community-weighted methods. Economic and hydraulic traits were decoupled at the species level, but coupled at the community level, and relationships between leaf traits in observed communities were stronger than that in null communities, suggesting that the adaptive mechanisms of plant species may be different. Furthermore, leaf economic traits were distributed more evenly across species occupying communities with lower temperature and precipitation, whereas hydraulic traits were distributed more evenly under lower water availability. This suggests that limiting similarity of specific leaf traits within communities would be enhanced when related-resources are limited, and highlights the independent assembly of leaf economics and hydraulic traits in terms of functional evenness. Importantly, the moments of leaf economic and hydraulic traits of observed communities explained more variation in ecosystem productivity than that of null communities, indicating ecosystem productivity depended on trait-based community assembly. Our results highlight the principles of community assembly regarding multi-dimensionsional traits in natural forests at a regional scale.

Comparative leaf growth strategies in response to low-water and low-light availability: variation in leaf physiology underlies variation in leaf mass per area in Populus tremuloides.

Developmental phenotypic plasticity can allow plants to buffer the effects of abiotic and biotic environmental stressors. Therefore, it is vital to improve our understanding of how phenotypic plasticity in ecological functional traits is coordinated with variation in physiological performance in plants. To identify coordinated leaf responses to low-water (LW) versus low-light (LL) availability, we measured leaf mass per area (LMA), leaf anatomical characteristics and leaf gas exchange of juvenile Populus tremuloides Michx. trees. Spongy mesophyll tissue surface area (Asmes/A) was correlated with intrinsic water-use efficiency (WUEi: photosynthesis, (Aarea)/stomatal conductance (gs)). Under LW availability, these changes occurred at the cost of greater leaf tissue density and reduced expansive growth, as leaves were denser but were only 20% the final area of control leaves, resulting in elevated LMA and elevated WUEi. Low light resulted in reduced palisade mesophyll surface area (Apmes/A) while spongy mesophyll surface area was maintained (Asmes/A), with no changes to WUEi. These leaf morphological changes may be a plastic strategy to increase laminar light capture while maintaining WUEi. With reduced density and thickness, however, leaves were 50% the area of control leaves, ultimately resulting in reduced LMA. Our results illustrate that P. tremuloides saplings partially maintain physiological function in response to water and light limitation by inducing developmental plasticity in LMA with underlying anatomical changes. We discuss additional implications of these results in the context of developmental plasticity, growth trade-offs and the ecological impacts of climate change.