Hydraulic basis for the evolution of photosynthetic productivity.

Clarifying the evolution and mechanisms for photosynthetic productivity is a key to both improving crops and understanding plant evolution and habitat distributions. Current theory recognizes a role for the hydraulics of water transport as a potential determinant of photosynthetic productivity based on comparative data across disparate species. However, there has never been rigorous support for the maintenance of this relationship during an evolutionary radiation. We tested this theory for 30 species of Viburnum, diverse in leaf shape and photosynthetic anatomy, grown in a common garden. We found strong support for a fundamental requirement for leaf hydraulic capacity (Kleaf) in determining photosynthetic capacity (Amax), as these traits diversified across this lineage in tight coordination, with their proportionality modulated by the climate experienced in the species' range. Variation in Kleaf arose from differences in venation architecture that influenced xylem and especially outside-xylem flow pathways. These findings substantiate an evolutionary basis for the coordination of hydraulic and photosynthetic physiology across species, and their co-dependence on climate, establishing a fundamental role for water transport in the evolution of the photosynthetic rate.

Leaf vein length per unit area is not intrinsically dependent on image magnification: avoiding measurement artifacts for accuracy and precision.

Leaf vein length per unit leaf area (VLA; also known as vein density) is an important determinant of water and sugar transport, photosynthetic function, and biomechanical support. A range of software methods are in use to visualize and measure vein systems in cleared leaf images; typically, users locate veins by digital tracing, but recent articles introduced software by which users can locate veins using thresholding (i.e. based on the contrasting of veins in the image). Based on the use of this method, a recent study argued against the existence of a fixed VLA value for a given leaf, proposing instead that VLA increases with the magnification of the image due to intrinsic properties of the vein system, and recommended that future measurements use a common, low image magnification for measurements. We tested these claims with new measurements using the software LEAFGUI in comparison with digital tracing using ImageJ software. We found that the apparent increase of VLA with magnification was an artifact of (1) using low-quality and low-magnification images and (2) errors in the algorithms of LEAFGUI. Given the use of images of sufficient magnification and quality, and analysis with error-free software, the VLA can be measured precisely and accurately. These findings point to important principles for improving the quantity and quality of important information gathered from leaf vein systems.

Developmentally based scaling of leaf venation architecture explains global ecological patterns.

Leaf size and venation show remarkable diversity across dicotyledons, and are key determinants of plant adaptation in ecosystems past and present. Here we present global scaling relationships of venation traits with leaf size. Across a new database for 485 globally distributed species, larger leaves had major veins of larger diameter, but lower length per leaf area, whereas minor vein traits were independent of leaf size. These scaling relationships allow estimation of intact leaf size from fragments, to improve hindcasting of past climate and biodiversity from fossil remains. The vein scaling relationships can be explained by a uniquely synthetic model for leaf anatomy and development derived from published data for numerous species. Vein scaling relationships can explain the global biogeographical trend for smaller leaves in drier areas, the greater construction cost of larger leaves and the ability of angiosperms to develop larger and more densely vascularised lamina to outcompete earlier-evolved plant lineages.

Dynamics of leaf hydraulic conductance with water status: quantification and analysis of species differences under steady state.

Leaf hydraulic conductance (K(leaf)) is a major determinant of photosynthetic rate in well-watered and drought-stressed plants. Previous work assessed the decline of K(leaf) with decreasing leaf water potential (Ψ(leaf)), most typically using rehydration kinetics methods, and found that species varied in the shape of their vulnerability curve, and that hydraulic vulnerability correlated with other leaf functional traits and with drought sensitivity. These findings were tested and extended, using a new steady-state evaporative flux method under high irradiance, and the function for the vulnerability curve of each species was determined individually using maximum likelihood for 10 species varying strongly in drought tolerance. Additionally, the ability of excised leaves to recover in K(leaf) with rehydration was assessed, and a new theoretical framework was developed to estimate how rehydration of measured leaves may affect estimation of hydraulic parameters. As hypothesized, species differed in their vulnerability function. Drought-tolerant species showed shallow linear declines and more negative Ψ(leaf) at 80% loss of K(leaf) (P(80)), whereas drought-sensitive species showed steeper, non-linear declines, and less negative P(80). Across species, the maximum K(leaf) was independent of hydraulic vulnerability. Recovery of K(leaf) after 1 h rehydration of leaves dehydrated below their turgor loss point occurred only for four of 10 species. Across species without recovery, a more negative P(80) correlated with the ability to maintain K(leaf) through both dehydration and rehydration. These findings indicate that resistance to K(leaf) decline is important not only in maintaining open stomata during the onset of drought, but also in enabling sustained function during drought recovery.

Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture.

Across plant species, leaves vary enormously in their size and their venation architecture, of which one major function is to replace water lost to transpiration. The leaf hydraulic conductance (K(leaf)) represents the capacity of the transport system to deliver water, allowing stomata to remain open for photosynthesis. Previous studies showed that K(leaf) relates to vein density (vein length per area). Additionally, venation architecture determines the sensitivity of K(leaf) to damage; severing the midrib caused K(leaf) and gas exchange to decline, with lesser impacts in leaves with higher major vein density that provided more numerous water flow pathways around the damaged vein. Because xylem embolism during dehydration also reduces K(leaf), we hypothesized that higher major vein density would also reduce hydraulic vulnerability. Smaller leaves, which generally have higher major vein density, would thus have lower hydraulic vulnerability. Tests using simulations with a spatially explicit model confirmed that smaller leaves with higher major vein density were more tolerant of major vein embolism. Additionally, for 10 species ranging strongly in drought tolerance, hydraulic vulnerability, determined as the leaf water potential at 50% and 80% loss of K(leaf), was lower with greater major vein density and smaller leaf size (|r| = 0.85-0.90; P < 0.01). These relationships were independent of other aspects of physiological and morphological drought tolerance. These findings point to a new functional role of venation architecture and small leaf size in drought tolerance, potentially contributing to well-known biogeographic trends in leaf size.