Summary A long‐standing research focus in phytology has been to understand how plants allocate leaf epidermal space to stomata in order to achieve an economic balance between the plant's carbon needs and water use. Here, we present a quantitative theoretical framework to predict allometric relationships between morphological stomatal traits in relation to leaf gas exchange and the required allocation of epidermal area to stomata.Our theoretical framework was derived from first principles of diffusion and geometry based on the hypothesis that selection for higher anatomical maximum stomatal conductance (g smax) involves a trade‐off to minimize the fraction of the epidermis that is allocated to stomata. Predicted allometric relationships between stomatal traits were tested with a comprehensive compilation of published and unpublished data on 1057 species from all major clades.In support of our theoretical framework, stomatal traits of this phylogenetically diverse sample reflect spatially optimal allometry that minimizes investment in the allocation of epidermal area when plants evolve towards higher g smax.Our results specifically highlight that the stomatal morphology of angiosperms evolved along spatially optimal allometric relationships. We propose that the resulting wide range of viable stomatal trait combinations equips angiosperms with developmental and evolutionary flexibility in leaf gas exchange unrivalled by gymnosperms and pteridophytes.
The revolutionary rise of broad-leaved (flowering) angiosperm plant species during the Cretaceous initiated a global ecological transformation towards modern biodiversity. Still, the mechanisms involved in this angiosperm radiation remain enigmatic. Here we show that the period of rapid angiosperm evolution initiated after the leaf interior (post venous) transport path length for water was reduced beyond the leaf interior transport path length for CO2 at a critical leaf vein density of 2.5–5 mm mm−2. Data and our modelling approaches indicate that surpassing this critical vein density was a pivotal moment in leaf evolution that enabled evolving angiosperms to profit from developing leaves with more and smaller stomata in terms of higher carbon returns from equal water loss. Surpassing the critical vein density may therefore have facilitated evolving angiosperms to develop leaves with higher gas exchange capacities required to adapt to the Cretaceous CO2 decline and outcompete previously dominant coniferous species in the upper canopy.
A principle response of C3 plants to increasing concentrations of atmospheric CO 2 (CO 2 ) is to reduce transpirational water loss by decreasing stomatal conductance (g s ) and simultaneously increase assimilation rates. Via this adaptation, vegetation has the ability to alter hydrology and climate. Therefore, it is important to determine the adaptation of vegetation to the expected anthropogenic rise in CO 2 . Short-term stomatal opening-closing responses of vegetation to increasing CO 2 are described by free-air carbon enrichments growth experiments, and evolutionary adaptations are known from the geological record. However, to date the effects of decadal to centennial CO 2 perturbations on stomatal conductance are still largely unknown. Here we reconstruct a 34% (±12%) reduction in maximum stomatal conductance (g smax ) per 100 ppm CO 2 increase as a result of the adaptation in stomatal density (D) and pore size at maximal stomatal opening (a max ) of nine common species from Florida over the past 150 y. The species-specific g smax values are determined by different evolutionary development, whereby the angiosperms sampled generally have numerous small stomata and high g smax , and the conifers and fern have few large stomata and lower g smax . Although angiosperms and conifers use different D and a max adaptation strategies, our data show a coherent response in g smax to CO 2 rise of the past century. Understanding these adaptations of C3 plants to rising CO 2 after decadal to centennial environmental changes is essential for quantification of plant physiological forcing at timescales relevant for global warming, and they are likely to continue until the limits of their phenotypic plasticity are reached. cuticular analysis | subtropical vegetation L and plants play a crucial role in regulating our planet's hydrological and energy balance by transpiring water through the stomatal pores on their leaf surfaces. A fundamental response of C3 plants to increasing atmospheric CO 2 concentration (CO 2 ) is to minimize transpirational water loss by reducing diffusive stomatal conductance (g s ) and simultaneously increasing assimilation rates (1). The resulting increased intrinsic water-use efficiency (iWUE: the ratio of assimilation to g s ) improves the vegetation's drought resistance and reduces the cost associated with the leaf's water transport system like leaf venation (2, 3). On a regional to global scale, decreasing rates of transpiration concurrently affect climate through reduced cloud formation and precipitation (4) and with this exert a physiological feedback on climate and hydrology on top of the radiative forcing of increasing CO 2 (5-7). In the light of continuing anthropogenic climate change, it is therefore imperative to determine how plants adapt to rising atmospheric CO 2 .During their 400 million year history, land plants have been exposed to large variations in environmental conditions that prompted genetic adaptations toward mechanisms that optimize individual fitness. Over this period, plant ad...
Summary Leaves with stomata on both upper and lower surfaces, termed amphistomatous, are relatively rare compared with hypostomatous leaves with stomata only on the lower surface. Amphistomaty occurs predominantly in fast‐growing herbaceous annuals and in slow‐growing perennial shrubs and trees. In this paper, we present the current understanding and hypotheses on the costs and benefits of amphistomaty related to water and CO2 transport in contrasting leaf morphologies. First, there is no evidence that amphistomatous species achieve higher stomatal densities on a projected leaf area basis than hypostomatous species, but two‐sided gas exchange is less limited by boundary layer effects. Second, amphistomaty may provide a specific advantage in thick leaves by shortening the pathway for CO2 transport between the atmosphere and the chloroplasts. In thin leaves of fast‐growing herbaceous annuals, in which both the adaxial and abaxial pathways are already short, amphistomaty enhances leaf–atmosphere gas‐exchange capacity. Third, amphistomaty may help to optimise the leaf‐interior water status for CO2 transport by reducing temperature gradients and so preventing the condensation of water that could limit CO2 diffusion. Fourth, a potential cost of amphistomaty is the need for additional investments in leaf water transport tissue to balance the water loss through the adaxial surface.
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