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 scale. For eudicotyledons, this pattern has been attributed to the fact that small leaves have a thinner boundary layer that helps to avoid extreme leaf temperatures and their leaf development results in vein traits that improve water transport under cold or dry climates. 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). 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

Turning over a new ‘leaf’: multiple functional significances of leaves versus phyllodes in Hawaiian Acacia koa

Hawaiian endemic tree Acacia koa is a model for heteroblasty with bipinnately compound leaves and phyllodes. Previous studies suggested three hypotheses for their functional differentiation: an advantage of leaves for early growth or shade tolerance, and an advantage of phyllodes for drought tolerance. We tested the ability of these hypotheses to explain differences between leaf types for potted plants in 104 physiological and morphological traits, including gas exchange, structure and composition, hydraulic conductance, and responses to varying light, intercellular CO2, vapour pressure deficit (VPD) and drought. Leaf types were similar in numerous traits including stomatal pore area per leaf area, leaf area-based gas exchange rates and cuticular conductance. Each hypothesis was directly supported by key differences in function. Leaves had higher mass-based gas exchange rates, while the water storage tissue in phyllodes contributed to greater capacitance per area; phyllodes also showed stronger stomatal closure at high VPD, and higher maximum hydraulic conductance per area, with stronger decline during desiccation and recovery with rehydration. While no single hypothesis completely explained the differences between leaf types, together the three hypotheses explained 91% of differences. These findings indicate that the heteroblasty confers multiple benefits, realized across different developmental stages and environmental contexts

Xylem traits mediate a trade-off between resistance to freeze-thaw-induced embolism and photosynthetic capacity in overwintering evergreens

Hydraulic traits were studied in temperate, woody evergreens in a high-elevation heath community to test for trade-offs between the delivery of water to canopies at rates sufficient to sustain photosynthesis and protection against disruption to vascular transport caused by freeze-thaw-induced embolism. Freeze-thaw-induced loss in hydraulic conductivity was studied in relation to xylem anatomy, leaf- and sapwood-specific hydraulic conductivity and gas exchange characteristics of leaves. We found evidence that a trade-off between xylem transport capacity and safety from freeze-thaw-induced embolism affects photosynthetic activity in overwintering evergreens. The mean hydraulically weighted xylem vessel diameter and sapwood-specific conductivity correlated with susceptibility to freeze-thaw-induced embolism. There was also a strong correlation of hydraulic supply and demand across species; interspecific differences in stomatal conductance and CO2 assimilation rates were correlated linearly with sapwood- and leaf-specific hydraulic conductivity. Xylem vessel anatomy mediated an apparent trade-off between resistance to freeze-thaw-induced embolism and hydraulic and photosynthetic capacity during the winter. These results point to a new role for xylem functional traits in determining the degree to which species can maintain photosynthetic carbon gain despite freezing events and cold winter temperatures

Xylem traits mediate a trade-off between resistance to freeze-thaw-induced embolism and photosynthetic capacity in overwintering evergreens

• Hydraulic traits were studied in temperate, woody evergreens in a high-elevation heath community to test for trade-offs between the delivery of water to canopies at rates sufficient to sustain photosynthesis and protection against disruption to vascular transport caused by freeze–thaw-induced embolism. • Freeze–thaw-induced loss in hydraulic conductivity was studied in relation to xylem anatomy, leaf- and sapwood-specific hydraulic conductivity and gas exchange characteristics of leaves. • We found evidence that a trade-off between xylem transport capacity and safety from freeze–thaw-induced embolism affects photosynthetic activity in overwintering evergreens. The mean hydraulically weighted xylem vessel diameter and sapwood-specific conductivity correlated with susceptibility to freeze–thaw-induced embolism. There was also a strong correlation of hydraulic supply and demand across species; interspecific differences in stomatal conductance and CO2 assimilation rates were correlated linearly with sapwood- and leaf-specific hydraulic conductivity. • Xylem vessel anatomy mediated an apparent trade-off between resistance to freeze–thaw-induced embolism and hydraulic and photosynthetic capacity during the winter. These results point to a new role for xylem functional traits in determining the degree to which species can maintain photosynthetic carbon gain despite freezing events and cold winter temperatures

Author response

Nutrients shape the growth, maturation, and aging of plants and animals. In plants, the juvenile to adult transition (vegetative phase change) is initiated by a decrease in miR156. In Arabidopsis, we found that exogenous sugar decreased the abundance of miR156, whereas reduced photosynthesis increased the level of this miRNA. This effect was correlated with a change in the timing of vegetative phase change, and was primarily attributable to a change in the expression of two genes, MIR156A and MIR156C, which were found to play dominant roles in this transition. The glucose-induced repression of miR156 was dependent on the signaling activity of HEXOKINASE1. We also show that the defoliation-induced increase in miR156 levels can be suppressed by exogenous glucose. These results provide a molecular link between nutrient availability and developmental timing in plants, and suggest that sugar is a component of the leaf signal that mediates vegetative phase change. DOI: http://dx.doi.org/10.7554/eLife.00260.00