Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution

Abstract

Summary Understanding the drivers of geological‐scale patterns in plant macroevolution is limited by a hesitancy to use measurable traits of fossils to infer palaeoecophysiological function.Here, scaling relationships between morphological traits including maximum theoretical stomatal conductance (g max) and leaf vein density (D v) and physiological measurements including operational stomatal conductance (g op), saturated (A sat ) and maximum (A max) assimilation rates were investigated for 18 extant taxa in order to improve understanding of angiosperm diversification in the Cretaceous.Our study demonstrated significant relationships between g op, g max and D v that together can be used to estimate gas exchange and the photosynthetic capacities of fossils. We showed that acquisition of high g max in angiosperms conferred a competitive advantage over gymnosperms by increasing the dynamic range (plasticity) of their gas exchange and expanding their ecophysiological niche space. We suggest that species with a high g max (> 1400 mmol m−2 s−1) would have been capable of maintaining a high A max as the atmospheric CO 2 declined through the Cretaceous, whereas gymnosperms with a low g max would experience severe photosynthetic penalty.Expansion of the ecophysiological niche space in angiosperms, afforded by coordinated evolution of high g max , D v and increased plasticity in g op , adds further functional insights into the mechanisms driving angiosperm speciation.

The Developmental Basis of Stomatal Density and Flux

“…The g max estimated this way strongly predicted the operating stomatal conductance measured with leaf gas exchange systems (g op ) across Arabidopsis (Arabidopsis thaliana) genotypes under low CO 2 , high humidity, and high red and blue light (Dow et al, 2014). However, across diverse species, the g max values estimated by Equation 2 tend to be much higher than g op (Feild et al, 2011;McElwain et al, 2016) for several reasons. First, for typical leaves transpiring even under the best conditions, the effective area of the stomatal pore (a') is smaller than the anatomical maximum a max , by an amount that varies across species, particularly as the actual pore geometry usually deviates from simplified cylindrical geometry (Franks and Farquhar, 2007).…”

“…The most recent extensions of this equation incorporated basic assumptions about allometries among guard cell dimensions, which have become standard in the stomatal literature (e.g. Taylor et al, 2012;Dow et al, 2014;McElwain et al, 2016) and enable the estimation of g max as a function of d and s. In its simplest form:…”

“…Clearly, much more research is needed to establish models that include all the factors that determine the anatomical influence of stomata on gas exchange rates and to validate these against a wide diversity of plants, yet the anatomical maximum defined as in Equations 1 and 2 is a strong constraint: g max correlates across diverse species with g op and lightsaturated photosynthetic rate (McElwain et al, 2016), and scales up, in combination with leaf area allocation, to the determination of ecosystem net primary productivity (Wang et al, 2015a). The anatomical g max is therefore a theoretical value estimating the maximum stomatal diffusion capacity, and like other theoretical physiological variables, such as photosynthetic parameters including the maximum carboxylation rate (V cmax ), it cannot be reached in practice, but is useful for generating hypotheses regarding the capacity for stomatal diffusion in various domains, such as comparisons of genotypes or species, functional types, or trends in evolutionary time DohenyAdams et al, 2012;Taylor et al, 2012;McElwain et al, 2016;de Boer et al, 2016).…”

“…where b ¼ D v and m ¼ pc 2 j 0:5 ð4hj þ pcÞ such that b is a biophysical constant and m a morphological constant based on scaling factors representing the proportionality of stomatal length (L) and width (W), and pore length (p) and depth (l), with c = p/L, j = W/L, and h = l/W all treated as constant for the estimation of g max (c, h, and j = 0.5 for nongrasses with kidney bean-shaped guard cells, or c = 0.5, h = 0.5, and j = 0.125 for grasses with their dumbbellshaped guard cells; McElwain et al, 2016), though these ratios can be allowed to vary for individual species or genotypes when more detailed information is available on stomatal dimensions (Franks and Farquhar, 2007;Franks et al, 2014). The g max estimated this way strongly predicted the operating stomatal conductance measured with leaf gas exchange systems (g op ) across Arabidopsis (Arabidopsis thaliana) genotypes under low CO 2 , high humidity, and high red and blue light (Dow et al, 2014).…”

Enhanced Stomatal Conductance by a Spontaneous Arabidopsis Tetraploid, Me-0, Results from Increased Stomatal Size and Greater Stomatal Aperture

“…3). Anatomical g smax is calculated on the assumption that stomatal pore area is maximal ; however, it is rare that stomata are opened maximally in response to actual environmental conditions (Desikan et al, 2004;Dow et al, 2014a;McElwain et al, 2016). The difference in g s between Me-0 and tetraploid Col shows that g s is determined not only by stomatal anatomical traits but also by stomatal aperture; however, we must not forget that stomatal movement may be affected to some extent by anatomical traits, as will be discussed later.…”