Cell density and airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity

Abstract

SummaryThe pattern of cell division, growth and separation during leaf development determines the pattern and volume of airspace in a leaf. The resulting balance of cellular material and airspace is expected to significantly influence the primary function of the leaf, photosynthesis, and yet the manner and degree to which cell division patterns affect airspace networks and photosynthesis remains largely unexplored. In this paper we investigate the relationship of cell size and patterning, airspace and photosynthesis by promoting and repressing the expression of cell cycle genes in the leaf mesophyll. Using microCT imaging to quantify leaf cellular architecture and fluorescence/gas exchange analysis to measure leaf function, we show that increased cell density in the mesophyll of Arabidopsis can be used to increase leaf photosynthetic capacity. Our analysis suggests that this occurs both by increasing tissue density (decreasing the relative volume of airspace) and by altering the pattern of airspace distribution within the leaf. Our results indicate that cell division patterns influence the photosynthetic performance of a leaf, and that it is possible to engineer improved photosynthesis via this approach.

Cellular perspectives for improving mesophyll conductance

“…This raises the question of whether the pattern of airspace observed in leaves is at all limiting to CO 2 flux and, if not, whether this parameter can be decreased without any adverse effect on CO 2 flux within the leaf. Experimental data support the case for this to be true, showing that airspace can be essentially be replaced with photosynthetic tissue, leading to a maintained photosynthetic activity on a per tissue volume basis with no decrease in g m (Lehmeier et al , ) . Interestingly, in manipulations in which airspace was filled with small mesophyll cells, there was actually an increase in g m (and increased assimilation rate) which correlated with an increased air channel density and smaller air channels (Lehmeier et al , ).…”

“…Experimental data support the case for this to be true, showing that airspace can be essentially be replaced with photosynthetic tissue, leading to a maintained photosynthetic activity on a per tissue volume basis with no decrease in g m (Lehmeier et al , ) . Interestingly, in manipulations in which airspace was filled with small mesophyll cells, there was actually an increase in g m (and increased assimilation rate) which correlated with an increased air channel density and smaller air channels (Lehmeier et al , ). The mechanistic basis for the link between air channel network parameters (tortuosity, channel diameter) and g m is unclear, but it suggests that we may need to revisit our view of CO 2 flux in the intercellular air space as being something that does not significantly impinge on g m .…”

Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism

“…Furthermore, r m is influenced by anatomical traits such as cell wall thickness (Ellsworth et al , ), chloroplast shape and cover (Busch et al , ; Weise et al , ), cell density, and the relative amount of intercellular air space (Lehmeier et al , ). Mesophyll CO 2 diffusion properties, and consequently the CO 2 concentration inside the chloroplast, therefore are mediated by the 3D anatomy of the mesophyll cells and the leaf as a whole (Earles et al , ).…”

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

“…While g m plays a dominant role in setting maximum photosynthesis in land plants as a whole, g m has been already maximized in angiosperms and especially in crops . Although some promising photosynthetic improvements have been achieved by manipulating several Calvin cycle enzymes (Ort et al, 2015;Simkin et al, 2019), by-passing photorespiration (Kebeish et al, 2007;South et al, 2019) or even indirectly manipulating g m by means of cell re-arrangement during leaf development (Lehmeier et al, 2017;Ren et al, 2019), these successful examples are still scarce and, in general, represent modest improvements of the maximum photosynthetic capacity. This is indeed predicted by the theory because, as in angiosperms, on average, the three limitations (stomata, mesophyll conductance and photo/biochemistry) co-limit photosynthesis in a well balanced proportion ; significant improvement of total photosynthesis would be possible only if the three limitations were simultaneously alleviated.…”