THE ROLE OF DEVELOPMENTAL CONSTRAINTS ON LEAF ARCHITECTURE AND THE EVOLUTION OF UNIQUELY HIGH LEAF VEIN DENSITIES IN ANGIOSPERMS

The capacity of a leaf to transpire water and assimilate CO₂ was previously found to correlate to the density of veins within the leaf. The resistance to water movement of cells between the veins and the stomatal pores is orders of magnitude higher than the hydraulic resistance of the veins. Decreasing the path length through the living tissue by increasing the density of veins (Dv) lowers the resistance of the system as a whole. An important evolutionary pattern rises from the link of Dv and physiology: flowering plants can have a Dv three or four times higher than any other plants. The higher physiological rates associated with high vein density also require higher stomatal conductances, but stomata and veins—and the photosynthetic tissue supported—might end up competing for space on the leaf at high densities. The reason stomata and veins cannot simultaneously occupy the same epidermal area is that all plant lineages can have bundle sheath extensions (BSE)—densely packed cells that link the vein to epidermis and exclude stomata.

We measured the occupation of the leaf surface across Angiosperm canopy trees, supplemented by additional measurements in ferns and gymnosperm seed plants. In rain forest trees, it is typically found that stomata occupy 6%-14% of a leaf and veins 13%-25% (max 60%). However, for a low vein density fern or gymnosperm, if the density of veins and stomata were simply scaled up, the leaf surface would be occupied entirely at vein densities far below those achieved by angiosperms.

The diffuse leaf growth and hierarchical vein orders of flowering plants allows differential deployment of BSE across vein orders, so that high vein density leaves ­reduce occupation by lowering BSE density versus vein density. The marginal leaf growth, common to most non-Angiosperm leaves requires an all or nothing approach, consequently BSE limits the possibility of high vein density because all veins must be equally expressed in the epidermis.