Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field

Abstract

Limited mesophyll diffusion conductance to CO(2) (g(m)) can significantly constrain plant photosynthesis, but the extent of g(m)-limitation is still imperfectly known. As g(m) scales positively with foliage photosynthetic capacity (A), the CO(2) drawdown from substomatal cavities (C(i)) to chloroplasts (C(C), C(i)-C(C)=A/g(m)) rather than g(m) alone characterizes the mesophyll diffusion limitations of photosynthesis. The dependencies of g(m) on A, foliage structure (leaf dry mass per unit area, M(A)), and the resulting drawdowns across a dataset of 81 species of contrasting foliage structure and photosynthetic potentials measured under non-stressed conditions were analysed to describe the structure-driven potential photosynthetic limitations due to g(m). Further the effects of key environmental stress factors and leaf and plant developmental alterations on g(m) and CO(2) drawdown were evaluated and the implications of varying g(m) on foliage photosynthesis in the field were simulated. The meta-analysis demonstrated that g(m) of non-stressed leaves was negatively correlated with M(A), and despite the positive relationship between g(m) and A, the CO(2) drawdown was larger in leaves with more robust structure. The correlations were stronger with mass-based g(m) and A, probably reflecting the circumstance that mesophyll diffusion is a complex three-dimensional process that scales better with mesophyll volume-weighted than with leaf area-weighted traits. The analysis of key environmental stress effects on g(m) and CO(2) drawdowns demonstrated that the effect of individual stresses on CO(2) drawdowns varies depending on the stress effects on foliage structure and assimilation rates. Leaf diffusion limitations are larger in non-senescent older leaves and also in senescent leaves, again reflecting more robust leaf structure and/or non-co-ordinated alterations in leaf photosynthesis and g(m). According to simulation analyses, in plants with a larger part of the overall diffusion conductance from the ambient atmosphere to the chloroplasts in the mesophyll, photosynthesis is less sensitive to changes in stomatal conductance. Accordingly, in harsher environments that support vegetation with tougher long-living stress-tolerant leaves with lower g(m), reductions in stomatal conductance that are common during stress periods are expected to alter photosynthesis less than in species where a larger part of the total diffusion limitation is determined by stomata. While structural robustness improves plant performance under environmental stress, low g(m) and inherently large CO(2) drawdown in robust leaves limits the photosynthesis of these plants more severely under favourable conditions when stomatal conductance is high. The differences in overall responsiveness to environmental modifications of plants with varying g(m) need consideration in current large-scale ecosystem productivity models.

Long-term acclimation of mesophyll conductance, carbon isotope discrimination and growth in two contrasting Picea asperata populations exposed to drought and enhanced UV-B radiation for three years

“…Thus, our results suggest a profound effect of g m on ı 13 C, as proposed by Barbour et al (2010). The inclusion of g m in process-based models of terrestrial vegetation may therefore improve the modeling of regional carbon and water fluxes under projected climate change (Niinemets et al, 2009).…”

Impact of mesophyll diffusion on estimated global land CO 2 fertilization

“…The drawdown of CO 2 from substomatal cavities to chloroplasts may reduce photosynthesis by 25-75%, depending on species (32). Differences in g m may even have the potential to alter the balance in species competitiveness as plant communities respond to rising atmospheric CO 2 because an atmosphere enriched in CO 2 may favor species with lower g m such as needleleaf evergreen trees and others (2,6). Thus, mesophyll diffusion can play a crucial role in our understanding and predicting photosynthetic responses to the increase in atmospheric CO 2 concentration from leaf to global scales.…”

“…However, diffusion of CO 2 through liquids is several orders of magnitude slower than it is through gases; diffusion through lipids in membranes is even slower than it is through liquid water (3), although it may be facilitated by aquaporin-like channels (4). Consequently, mesophyll layers constitute a major barrier for CO 2 movement inside leaves (5)(6)(7)(8)(9).…”

Gas exchange characteristics of the hybrid Azadirachta indica × Melia azedarach

“…In conifers, the age-and size-dependent increase in LMA (LMA = leaf density × thickness) is primarily associated with enhanced leaf density, whereas both the thickness and density are increased in broadleaved species (England & Attiwill 2006, Juárez-López et al 2008, Niinemets et al 2009). Many studies have reported that agedependent (or size) increases in the LMA were possibly caused by greater water stress in the leaves of large trees (Ambrose et al 2009, Niinemets et al 2009). The photosynthetic capacity is also influenced by the increased LMA, and this effect has been related to changes in the ratios of internal air space and mesophyll area to the total area.…”