Maximum leaf conductance driven by CO ₂ effects on stomatal size and density over geologic time

Abstract

Stomatal pores are microscopic structures on the epidermis of leaves formed by 2 specialized guard cells that control the exchange of water vapor and CO 2 between plants and the atmosphere. Stomatal size (S) and density (D) determine maximum leaf diffusive (stomatal) conductance of CO 2 (gc max ) to sites of assimilation. Although large variations in D observed in the fossil record have been correlated with atmospheric CO 2, the crucial significance of similarly large variations in S has been overlooked. Here, we use physical diffusion theory to explain why large changes in S necessarily accompanied the changes in D and atmospheric CO 2 over the last 400 million years. In particular, we show that high densities of small stomata are the only way to attain the highest g cmax values required to counter CO 2''starvation'' at low atmospheric CO2 concentrations. This explains cycles of increasing D and decreasing S evident in the fossil history of stomata under the CO 2 impoverished atmospheres of the Permo-Carboniferous and Cenozoic glaciations. The pattern was reversed under rising atmospheric CO 2 regimes. Selection for small S was crucial for attaining high gcmax under falling atmospheric CO2 and, therefore, may represent a mechanism linking CO 2 and the increasing gas-exchange capacity of land plants over geologic time.Phanerozoic ͉ photosynthesis ͉ plant evolution ͉ transpiration ͉ xylem

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

“…Changes in D appear to be inextricably linked to changes in S, and it is the combination of S and D that determines g c(max) and g w(max) . There is a consistent negative relationship between S and D at all scales, including leaves within a single species (Franks et al, 2009), across species in a population (Hetherington and Woodward, 2003;Russo et al, 2010), through the fossil record (Franks and Beerling, 2009b), and across mutants of a single species where D is induced to vary by genetic manipulation (Doheny-Adams et al, 2012;Dow et al, 2014;Franks et al, 2015). This negative logarithmic relationship (often represented as a negative linear log-log plot) fundamentally constrains the adaptation and evolution of stomata under forcing by any environmental variable affecting leaf gas exchange.…”

“…Note the positive (amplifying) feedback effect of stomata on DTs (top right). Beerling, 2009b). The implications from this, based on the well-established coupling between vegetation and climate (Bonan, 2016) and the influence of stomatal morphology on leaf gas exchange (Franks and Farquhar, 2007), are that these patterns reflect coordinated shifts in global vegetation and climate.…”

“…To be fully functional, stomata need to be separated by at least one epidermal cell, the so-called one-cell-spacing rule (Geisler et al, 2000;Dow et al, 2014), and stomatal guard cells cannot be any smaller than their nucleus. 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.…”

“…To achieve a new g c(max) and g w(max) , plants alter S and D within the confines of a general negative logarithmic relationship that optimizes the allocation of leaf epidermal area to gas exchange (de Boer et al, 2016). Fundamentally, selection for higher stomatal conductance is linked to lower S and higher D (Franks and Beerling, 2009b) The optimization strategy identified by de Boer et al (2016) has its own set of physical constraints, imposed by the biochemical and mechanical requirements of stomata and the size of the genome that is packed into the nucleus of each guard cell. To be fully functional, stomata need to be separated by at least one epidermal cell, the so-called one-cell-spacing rule (Geisler et al, 2000;Dow et al, 2014), and stomatal guard cells cannot be any smaller than their nucleus.…”

Evolution of the Stomatal Regulation of Plant Water Content

“…Right, The epidermis of the angiosperm, canopy tree species (Elaeocarpus kirtonii) is the primary stomata-bearing organ of this and most other angiosperm species. Stomatal density in this leaf is approximately 230 stomata mm 22 , which is quite modest for the leaves of an angiosperm tree (Franks and Beerling, 2009;. Images were taken at the same magnification, scale bar = 100 mm.…”