Light and growth form interact to shape stomatal ratio among British angiosperms

Abstract

In most plants, stomata are located only on the abaxial leaf surface (hypostomy), but many plants have stomata on both surfaces (amphistomy). High light and herbaceous growth form have been hypothesized to favor amphistomy, but these hypotheses have not been rigorously tested together using phylogenetic comparative methods. I leveraged a large dataset including stomatal ratio, Ellenberg light indicator value, growth form and phylogenetic relationships for 372 species of British angiosperms. I used phylogenetic comparative methods to test how light and/or growth form influence stomatal ratio and density. High light and herbaceous growth form are correlated with amphistomy, as predicted, but they also interact; the effect of light is pronounced in therophytes (annuals) and perennial herbs, but muted in phanerophytes (shrubs and trees). Furthermore, amphistomy and stomatal density evolve together in response to light. Comparative analyses of British angiosperms reveal two major insights. First, light and growth form interact to shape stomatal ratio; amphistomy is common under high light, but mostly for herbs. Second, coordinated evolution of adaxial stomatal density and light tolerance indicates that amphistomy helps to optimally balance light acquisition with gas exchange. Stomatal ratio may have potential as a functional trait for paleoecology and crop improvement.

Increased adaxial stomatal density is associated with greater mesophyll surface area exposed to intercellular air spaces and mesophyll conductance in diverse C4 grasses

“…These traits could be the potential targets for modifying g m , and therefore TE i (Flexas et al ., ). However, traits like stomatal distribution and density have not received much attention in terms of their relationship with g m , although previous studies have proposed them to be important determinants of CO 2 diffusion into leaves (Mott & O'Leary, ; Muir, ; Drake et al ., ) and hence leaf photosynthetic capacity (Tanaka et al ., ).…”

“…Stomatal distribution on a leaf can either be hypostomatous or amphistomatous (Parkhurst, ; Mott & O'Leary, ). Hypostomaty or presence of stomata only on the lower (abaxial) surface of leaves is the most common trait and is present in trees and shrubs adapted to mesic and shaded conditions (Muir, ; de Boer et al ., ), whereas amphistomaty or presence of stomata on both leaf surfaces is a less common trait and is present primarily in herbaceous species adapted to open habitats with high light and warm, arid conditions (Mott & O'Leary, ; Muir, , ). Theory and experimental evidence suggest that, compared with having stomata only on the abaxial leaf surface (hypostomaty), distributing stomata on both surfaces (amphistomaty) can provide an adaptive advantage in terms of carbon uptake for plants growing in open habitats where CO 2 diffusion strongly limits A net under high light (Parkhurst, ; Muir, ; Drake et al ., ).…”

“…Hypostomaty or presence of stomata only on the lower (abaxial) surface of leaves is the most common trait and is present in trees and shrubs adapted to mesic and shaded conditions (Muir, ; de Boer et al ., ), whereas amphistomaty or presence of stomata on both leaf surfaces is a less common trait and is present primarily in herbaceous species adapted to open habitats with high light and warm, arid conditions (Mott & O'Leary, ; Muir, , ). Theory and experimental evidence suggest that, compared with having stomata only on the abaxial leaf surface (hypostomaty), distributing stomata on both surfaces (amphistomaty) can provide an adaptive advantage in terms of carbon uptake for plants growing in open habitats where CO 2 diffusion strongly limits A net under high light (Parkhurst, ; Muir, ; Drake et al ., ). This is because, in hypostomatous species, CO 2 must diffuse through the bulk of the leaf to reach the upper (adaxial) or main light‐absorbing surface, thus increasing the CO 2 diffusion path length (Evans & von Caemmerer, ; Muir, ), whereas having stomata on both sides of the leaf reduces the average CO 2 diffusion path length compared with hypostomatous species.…”

“…Theory and experimental evidence suggest that, compared with having stomata only on the abaxial leaf surface (hypostomaty), distributing stomata on both surfaces (amphistomaty) can provide an adaptive advantage in terms of carbon uptake for plants growing in open habitats where CO 2 diffusion strongly limits A net under high light (Parkhurst, ; Muir, ; Drake et al ., ). This is because, in hypostomatous species, CO 2 must diffuse through the bulk of the leaf to reach the upper (adaxial) or main light‐absorbing surface, thus increasing the CO 2 diffusion path length (Evans & von Caemmerer, ; Muir, ), whereas having stomata on both sides of the leaf reduces the average CO 2 diffusion path length compared with hypostomatous species. Furthermore, an increase in adaxial stomatal density (SD ada ) was coordinated with an increase in total stomatal densities, whilst maintaining a constant abaxial stomatal density (SD aba ) will create additional parallel pathways for CO 2 diffusion by increasing intercellular air spaces, and hence S mes (Parkhurst, ; Mott & O'Leary, ; Muir, ).…”

Two sides to every leaf: water and CO2 transport in hypostomatous and amphistomatous leaves

“…One such cost pertains to the greater susceptibility for entry of foliar pathogens through stomata in the upper epidermis (McKown et al ., ). Recent phylogenetic insight further suggests that the occurrence of amphistomaty relates to an interaction between light environment and growth form (Muir, ). For many families, amphistomaty appears to be the derived leaf morphology (Mott et al ., ), but a comprehensive phylogenetic analysis on the evolution of amphistomaty, including representatives from arid environments, has yet to be undertaken.…”