Unraveling the drivers of optimal stomatal behavior in global C3 plants: A carbon isotope perspective.

Abstract

Understanding the drivers of stomatal behavior is critical for modeling terrestrial carbon cycle and water balance. The unified stomatal optimization (USO) model provides a mechanistic linkage between stomatal conductance (g_s) and photosynthesis (A), with its slope parameter (g₁) inversely related to intrinsic water use efficiency (iWUE), providing a key proxy to characterize the differences in iWUE and stomatal behavior. While many studies have identified multiple environmental factors influencing g₁, the potential role of evolutionary history in shaping g₁ remains incompletely understood. Leaf organic matter ¹³C discriminations (Δ¹³C) can be applied to estimate g₁ over timescales from days to whole growing season. However, most applications assume that mesophyll conductance (g_m)-a critical parameter in the Δ¹³C model-is infinite, due to limited information. Here, we incorporated new insight of g_m to allow for more realistic parameterization of this variable, and subsequently to enable improved estimation of g₁ based on a global bulk leaf Δ¹³C dataset comprising 2215 observations of 1521 species that span major biomes. Our analysis revealed a significant phylogenetic signal in g₁ values, which differed among phylogenetic groups. Through a Bayesian phylogenetic linear mixed model, we found that species and phylogeny together explained 36.63 % of g₁ variance, a contribution comparable to that of the environmental factors (44.59 %). Our findings uncovered for the first time that environmental factors, species-level and phylogenetic effects jointly shape g₁ variability, thereby contributing to a more comprehensive understanding of optimal stomatal behavior in the context of global environmental change.