No evidence of general CO₂ insensitivity in ferns: one stomatal control mechanism for all land plants?

Abstract

SummaryStomatal regulation of plant carbon uptake and water loss under changing environmental conditions was a crucial evolutionary step in the colonization of land by plants. There are currently two conflicting models describing the nature of stomatal regulation across terrestrial vascular plants: the first is characterized by a fundamental mechanistic similarity across all lineages, and the second is characterized by the evolution of major differences in angiosperms compared with more ancient lineages. Specifically, the second model posits that stomata of ferns lack a response to elevated atmospheric CO 2 concentration (c a ) and therefore cannot regulate leaf intercellular CO 2 concentration (c i ).We compared stomatal sensitivity to changes in c a in three distantly related fern species and a representative angiosperm species.Fern and angiosperm stomata responded strongly and similarly to changes in c a . As a result, c i /c a was maintained within narrow limits during c a changes.Our results challenge the model in which stomata of ferns generally lack a response to elevated c a and that angiosperms evolved new dynamic mechanisms for regulating leaf gas exchange that differ fundamentally from ferns. Instead, the results are consistent with a universal stomatal control mechanism that is fundamentally conserved across ferns and angiosperms, and therefore likely all vascular plant divisions.

Fern Stomatal Responses to ABA and CO2 Depend on Species and Growth Conditions

“…2, A and C). A similar difference in the kinetics of high CO 2 -induced stomatal closure in ferns and Arabidopsis has been found before (Franks and Britton-Harper, 2016). These differences in the kinetics of CO 2 responses between ferns and angiosperms may result from their different stomatal morphology and related mechanical properties.…”

“…However, stomata of the lycophyte S. uncinata responded to both subambient and above-ambient CO 2 concentrations (Ruszala et al, 2011), as did the stomata of the fern Phyllitis scolopendrium (Mansfield and Willmer, 1969). Recently, several fern species were shown to close their stomata in response to CO 2 elevation from the ambient 400 to 800 ppm, similar to the angiosperm Arabidopsis (Franks and Britton-Harper, 2016). It was hypothesized that different growth conditions and species-specific behaviors may account for the varied results obtained in the analysis of stomatal responses of mosses, ferns, and lycophytes (Roelfsema and Hedrich, 2016).…”

Evolution of the Stomatal Regulation of Plant Water Content

“…Stomatal evolution has become a focus of some debate in recent years Brodribb and McAdam, 2011;Chater et al, 2011;Ruszala et al, 2011;Franks and Britton-Harper, 2016), largely initiated by evidence that although the stomata of ancient lineages of vascular plants open similarly to angiosperms in response to light and CO 2 , they close differently. In particular, the observation that stomatal conductance and transpiration of ferns and lycophytes does not significantly decline in response to abscisic acid (ABA; Brodribb and McAdam, 2011) led to the theory that stomatal closure during water stress originated in early vascular plants as a passive response of guard cells to dehydration, and that the "active" closure mechanism, mediated by ABA, evolved much later in the earliest seed plants.…”

“…There remains much debate in the literature on the evolution of the stomatal response to CO 2 Franks and BrittonHarper, 2016). A common feature of all studies in this area is a conserved tendency to respond to CO 2 , particularly low CO 2 , which likely reflects a common photosynthetic signaling in all stomata Franks and Britton-Harper, 2016). However, major differences across lineages in the way stomata instantaneously respond to CO 2 in the dark (Doi and Shimazaki, 2008; as well as the influence of ABA on the sensitivity of stomata to CO 2 reflect as yet undescribed and potentially important mechanistic differences in the way stomata respond to more natural endogenous and environmental signals.…”

Stomatal Function across Temporal and Spatial Scales: Deep-Time Trends, Land-Atmosphere Coupling and Global Models

“…Understanding and predicting larger scale carbon, water, and energy cycles requires accurate estimates of the leaf diffusive (stomatal) conductances to water vapor and CO 2 (g w and g c , respectively [definitions for these and other terms are given in Table I]) using stomatal conductance models. Despite considerable progress in the development and application of these models, theoretical questions remain about some of the most basic stomatal sensitivities to environmental variables, such as the response to CO 2 and water deficit (Brodribb and McAdam, 2011;Chater et al, 2011;Ruszala et al, 2011;Franks, 2013;Lind et al, 2015;Franks and Britton-Harper, 2016).…”