Cell wall thickness has phylogenetically consistent effects on photosynthetic N-use efficiency of land species

Abstract

Leaf photosynthetic nitrogen-use efficiency (PNUE) diversified significantly among C3 species. However, morpho-physiological mechanisms and interrelationships forming PNUE remain unclear on the evolutionary time scale. In this study, we compiled a novel extensive matrix of morpho-anatomical and physiological traits of leaf in 679 C3 species ranging from bryophytes to angiosperms to understand the intricacy of interrelationships underlying the variations in PNUE. We found that LMA, mesophyll cell wall thickness (Tcwm), Rubisco N allocation fraction (PR), and mesophyll conductance (gm) together interpreted 83% of variations in PNUE, with PR and gm accounting for 65% of those variations. However, the PR effects were species-dependent on gm; that is, the contribution of PR on PNUE was extensively significant in high-gm species in comparison to low-gm species. Standard major analysis (SMA) and path analysis suggested a weak correlation between PNUE and LMA, whereas the SMA correlation for PNUE-Tcwm was strong. The PR was inversely proportional to Tcwm, which was similar to the relationship between gm and Tcwm (p-value < 0.01), so that the internal CO2 drawdown from intercellular airspace to carboxylaton sites was relatively conservative over a wide range of Tcwm. Collectively, the coordination of changes in PR and gm connecting Tcwm suggested the complex physiological mechanisms mediated by Tcwm modulating PNUE across contrasting plant groups.