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.

The Causes of Leaf Hydraulic Vulnerability and Its Influence on Gas Exchange in Arabidopsis thaliana.

The influence of the dynamics of leaf hydraulic conductance (K leaf) diurnally and during dehydration on stomatal conductance and photosynthesis remains unclear. Using the model species Arabidopsis (Arabidopsis thaliana ecotype Columbia-0), we applied a multitiered approach including physiological measurements, high-resolution x-ray microcomputed tomography, and modeling at a range of scales to characterize (1) K leaf decline during dehydration; (2) its basis in the hydraulic conductances of leaf xylem and outside-xylem pathways (K ox); (3) the dependence of its dynamics on irradiance; (4) its impact on diurnal patterns of stomatal conductance and photosynthetic rate; and (5) its influence on gas exchange and survival under simulated drought regimes. Arabidopsis leaves showed strong vulnerability to dehydration diurnally in both gas exchange and hydraulic conductance, despite lack of xylem embolism or conduit collapse above the turgor loss point, indicating a pronounced sensitivity of K ox to dehydration. K leaf increased under higher irradiance in well-hydrated leaves across the full range of water potential, but no shift in K leaf vulnerability was observed. Modeling indicated that responses to dehydration and irradiance are likely attributable to changes in membrane permeability and that a dynamic K ox would contribute strongly to stomatal closure, improving performance, survival, and efficient water use during drought. These findings for Columbia-0 provide a baseline for assessing variation across genotypes in hydraulic traits and their influence on gas exchange during dehydration.

Leaf hydraulic conductance varies with vein anatomy across Arabidopsis thaliana wild-type and leaf vein mutants.

Leaf venation is diverse across plant species and has practical applications from paleobotany to modern agriculture. However, the impact of vein traits on plant performance has not yet been tested in a model system such as Arabidopsis thaliana. Previous studies analysed cotyledons of A. thaliana vein mutants and identified visible differences in their vein systems from the wild type (WT). We measured leaf hydraulic conductance (Kleaf ), vein traits, and xylem and mesophyll anatomy for A. thaliana WT (Col-0) and four vein mutants (dot3-111 and dot3-134, and cvp1-3 and cvp2-1). Mutant true leaves did not possess the qualitative venation anomalies previously shown in the cotyledons, but varied quantitatively in vein traits and leaf anatomy across genotypes. The WT had significantly higher mean Kleaf . Across all genotypes, there was a strong correlation of Kleaf with traits related to hydraulic conductance across the bundle sheath, as influenced by the number and radial diameter of bundle sheath cells and vein length per area. These findings support the hypothesis that vein traits influence Kleaf , indicating the usefulness of this mutant system for testing theory that was primarily established comparatively across species, and supports a strong role for the bundle sheath in influencing Kleaf .

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.

Effects of phyllotaxy on biomechanical properties of stems of Cercis occidentalis (Fabaceae).

PREMISE OF THE STUDY: Phyllotaxy, the arrangement of leaves on a stem, may impact the mechanical properties of woody stems several years after the leaves have been shed. We explored mechanical properties of a plant with alternate distichous phyllotaxy, with a row of leaves produced on each side of the stem, to determine whether the nodes behave as spring-like joints. METHODS: Flexural stiffness of 1 cm diameter woody stems was measured in four directions with an Instron mechanical testing system; the xylem of the stems was then cut into node (former leaf junction) and nonnode segments for measurement of xylem density. KEY RESULTS: Stems had 20% greater flexural stiffness in the plane perpendicular to the original leaf placement than in the parallel plane. The xylem in the node region was more flexible, but it had significantly greater tissue density than adjacent regions, contradicting the usual correlation between wood density and stiffness. CONCLUSIONS: Nodes can behave as spring-like joints in woody plants. For plagiotropic shoots, distichous phyllotaxy results in stems that resist up-and-down bending more than lateral back-and-forth movement. Thus, they may more effectively absorb applied loads from fruits, animals, wind, rain, and snow and resist stresses due to gravity without cracking and breaking. Under windy conditions, nodes may improve damping by absorbing vibrational energy and thus reducing oscillation damage. The effect of plant nodes also has biomimetic design implications for architects and material engineers.