Physiological framework for adaptation of stomata to CO ₂ from glacial to future concentrations

Abstract

In response to short-term fluctuations in atmospheric CO 2 concentration, c a , plants adjust leaf diffusive conductance to CO 2 , g c , via feedback regulation of stomatal aperture as part of a mechanism for optimizing CO 2 uptake with respect to water loss. The operational range of this elaborate control mechanism is determined by the maximum diffusive conductance to CO 2 , g c(max) , which is set by the size (S) and density (number per unit area, D) of stomata on the leaf surface. Here, we show that, in response to long-term exposure to elevated or subambient c a , plants alter g c(max) in the direction of the short-term feedback response of g c to c a via adjustment of S and D. This adaptive feedback response to c a , consistent with long-term optimization of leaf gas exchange, was observed in four species spanning a diverse taxonomic range (the lycophyte Selaginella uncinata, the fern Osmunda regalis and the angiosperms Commelina communis and Vicia faba). Furthermore, using direct observation as well as flow cytometry, we observed correlated increases in S, guard cell nucleus size and average apparent 1C DNA amount in epidermal cell nuclei with increasing c a , suggesting that stomatal and leaf adaptation to c a is linked to genome scaling.

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

“…For example, Woodward (1987) found that D decreased by 40% to 67% for both historic and growth chamber-simulated change in c a from 280 to 340 mL L 21 , a rate of 66% to 112% per 100 mL L 21 , assuming an approximately linear response in this relatively narrow range of c a . From the many hundreds of studies that have followed, it appears that the sensitivity is usually much less than this, perhaps as little as 2% to 4% per 100 mL L 21 increase in c a on average (Franks et al, 2012b). This relatively moderate mean sensitivity of D to c a should be considered in the A key insight to emerge in studying the effects of changing c a on stomatal density is its coordination with stomatal size (S) and, ultimately, the anatomical maximum diffusive conductance to CO 2 and water vapor [g c(max) and g w(max) , respectively].…”

“…This adaptation is usually in the direction that would tend to counteract the physiological effects of the change in c a (e.g. higher D with lower c a increases stomatal conductance to counteract the initial drop in CO 2 assimilation rate; Franks et al, 2012bFranks et al, , 2013. What remains unclear about this simple principle is how to characterize this sensitivity quantitatively for the purpose of simulation or prediction.…”

“…Across vascular plants, much of the greater than 40-fold range in stomatal size (length 3 width) and, hence, maximum stomatal conductance (Franks and Beerling, 2009b) is linked to the evolution of plant genome size Knight and Beaulieu, 2008;Franks et al, 2012a), and angiosperms span the broadest range. This widely observed correlation between stomatal size, guard cell nucleus size, and plant genome size has prompted the hypothesis (yet to be tested comprehensively) that selection for higher or lower stomatal conductance involves coselection for correlated changes in S, D, and genome size (Franks et al, 2012a(Franks et al, , 2012b. The role of factors that determine nucleus size and architecture also must be considered, including coiled-coil proteins in the Nuclear Matrix Constituent Protein family (Wang et al, 2013).…”

Evolution of the Stomatal Regulation of Plant Water Content

“…Behavioral differences in the responses of stomata to water stress within plant communities have been recognized as an important axis of variation in ecological strategy (Martínez-Vilalta and Garcia-Forner, 2016;Meinzer et al, 2016), while systematic variation in stomatal size, density, and response characteristics among plant clades have important implications for interpreting plant-atmosphere interactions (Franks et al, 2012;Franks e Buckley, 2017). Understanding how stomatal behavior feeds into processes of plant selection is a fundamental goal in plant science, and much progress over the past three decades has been made toward this goal by applying the tools of genetic manipulation to the model angiosperm, Arabidopsis thaliana (Schroeder et al, 2001;Hetherington and Woodward, 2003;Kim et al, 2010;Hedrich, 2012;Eisenach and De Angeli, 2017;Jezek and Blatt, 2017).…”

Atmospheric carbon dioxide: a driver of photosynthetic eukaryote evolution for over a billion years?

“…In particular, high densities of small stomata appear to be an adaption for allowing high maximum leaf CO 2 diffusive conductances (g cmax ) and countering CO 2 starvation during Permo-Carboniferous and Cenozoic glaciations [24]. Franks et al [25] report new experimental observations for a range of plant taxa, from clubmosses through to late-branching angiosperms, which provide supporting evidence for the causal action of CO 2 on coordinated changes in S and D. These results suggest that S-and D-controlled adaptation of g cmax to atmospheric CO 2 is widespread in vascular plants, possibly with a conserved underlying genetic basis.…”