A Novel Hypothesis for the Role of Photosynthetic Physiology in Shaping Macroevolutionary Patterns

Abstract

ORCID IDs: 0000-0003-0317-9563 (C.Y.); 0000-0002-7893-1142 (J.C.M.).The fossil record and models of atmospheric concentrations of O 2 and CO 2 suggest that past shifts in plant ecological dominance often coincided with dramatic changes in Earth's atmospheric composition. This study tested the effects of past changes in atmospheric composition on the photosynthetic physiology of a limited range of early-diverging angiosperms (eight), gymnosperms (three), and ferns (two). We performed physiological measurements on all species and used the results to parameterize simulations of their photosynthetic paleophysiology using three independent modeling approaches. Unique physiological attributes were identified for the three evolutionary groups: angiosperm taxa displayed significantly higher mesophyll conductance (g m ), yet their stomatal conductance (g s ) was lower than that of ferns. Gymnosperm taxa displayed low g s and g m , but they partially offset their significant diffusional limitations on photosynthesis through their higher maximum Rubisco carboxylation rate. Despite their high total conductance to CO 2 , fern taxa lacked an optimized control of g s , which was reflected in their low intrinsic water use efficiency. Simulations of the photosynthetic physiology of ferns, angiosperms, and gymnosperms through Earth's history demonstrated that past fluctuations in O 2 and CO 2 concentrations may have resulted in significant shifts in the relative competitiveness of the three evolutionary groups. Although preliminary because of limited species sampling, these findings hint at a potential mechanistic basis for the observed broad temporal correlation between atmospheric change and shifts in plant evolutionary group-level richness observed in the fossil record and are presented as a framework to be tested with paleophotosynthetic proxies and through increased species sampling.

Photosynthesis and photosynthetic efficiencies along the terrestrial plant’s phylogeny: lessons for improving crop photosynthesis

“…Again here, gymnosperms behave somewhat as outliers as, being the group with the largest WUE – although not differing statistically from pteridophytes and angiosperms (Figure a) – present the lowest g m / g s compared with pteridophytes and angiosperms (Figure a) but the highest ETR/ g s , although similar to those in pteridophytes (Figure b). These observations for gymnosperms are fully in agreement with a recent independent study by Yiotis and McElwain () and suggest that the ratio ETR/ g s (or V c,max / g s ) is a much more ‘powerful means’ to improve WUE than g m / g s . However, for not yet fully understood reasons with the exception of gymnosperms, the g m / g s ratio seems to have had a predominant role in establishing the phylogenetic differences for WUE.…”

“…angiosperms (Figure 5a) but the highest ETR/g s , although similar to those in pteridophytes (Figure 5b). These observations for gymnosperms are fully in agreement with a recent independent study by Yiotis and McElwain (2019) and suggest that the ratio ETR/g s (or V c,max /g s ) is a much more 'powerful means' to improve WUE than g m /g s . However, for not yet fully understood reasons with the exception of gymnosperms, the g m /g s ratio seems to have had a predominant role in establishing the phylogenetic differences for WUE.…”

“…Gymnosperms present lower A mass and PNUE and higher WUE than would be expected from the observed phylogenetic trend. This observation has sometimes been attributed to a partial compensation of their low g s and g m by a high carboxylation capacity (V c,max ), but nevertheless may deserve better attention in future studies (Veromann-J€ urgenson et al, 2017;Yiotis and McElwain, 2019). Increasing LMA (Figure 1), A mass and PNUE levels along the phylogeny were expected because the typical leaf economics spectrum (LES) relationshipssuch as those between A mass and LMA on the one hand, and between A mass and leaf N content on the other handpresent identical slopes but very different intercepts among phylogenetic groups, so that the more basal the group the less A mass achieved per either LMA or N Carriqu ı et al, 2019b).…”

Rising CO 2 drives divergence in water use efficiency of evergreen and deciduous plants

“…High LMA generally occurs in woody evergreens because of their robust leaf structure, which can incur resistance to CO 2 diffusion and, hence, lower mesophyll conductance ( g m ) ( 7 , 15 , 16 ). Therefore, evergreen leaves, in general, are likely to operate at lower g m values than deciduous leaves ( 16 , 17 ).…”

Impacts of soil water stress on the acclimated stomatal limitation of photosynthesis: Insights from stable carbon isotope data

“…Unfortunately, there are still large uncertainties in the values for g m (von Caemmerer & Evans, 2015) and the ratio of g m to g s . Many studies have assumed constant value for g m / g s across plant species (Flanagan & Farquhar, 2014; Wang et al., 2017; Warren, 2008; Warren & Dreyer, 2006), while others have reported variations in g m values between the two major groups of seed plants, with higher g m / g s in angiosperms than in gymnosperms (Flexas & Carriqui, 2020; Yiotis & McElwain, 2019). The magnitude of the offset in g m / g s values between plant groups is, however, still unclear, but very likely is in the range of 25%–50%.…”