Mesophyll porosity is modulated by the presence of functional stomata

Marjorie R Lundgren,Craig J Sturrock,Andrew J Fleming,Julie E Gray,Marc Fradera-Soler,Matthew J Wilson,Alice L Baillie,Colin P Osborne,Radoslaw Pajor,Andrew Mathers,Sacha J Mooney,Jessica Dunn,Stephen Rolfe,Lee Hunt

doi:10.1038/s41467-019-10826-5

Abstract

The formation of stomata and leaf mesophyll airspace must be coordinated to establish an efficient and robust network that facilitates gas exchange for photosynthesis, however the mechanism by which this coordinated development occurs remains unclear. Here, we combine microCT and gas exchange analyses with measures of stomatal size and patterning in a range of wild, domesticated and transgenic lines of wheat and Arabidopsis to show that mesophyll airspace formation is linked to stomatal function in both monocots and eudicots. Our results support the hypothesis that gas flux via stomatal pores influences the degree and spatial patterning of mesophyll airspace formation, and indicate that this relationship has been selected for during the evolution of modern wheat. We propose that the coordination of stomata and mesophyll airspace pattern underpins water use efficiency in crops, providing a target for future improvement.

Highlights

The formation of stomata and leaf mesophyll airspace must be coordinated to establish an efficient and robust network that facilitates gas exchange for photosynthesis, the mechanism by which this coordinated development occurs remains unclear
Since it has been proposed that distinct mechanisms underpin stomatal patterning in monocot and eudicot systems[19], we extend our analysis in wheat to the eudicot Arabidopsis, exploiting a range stomatal development mutants to identify a fundamental mechanism linking stomatal and mesophyll differentiation
That the degree and extent of separation of mesophyll cells to form airspaces is linked to the presence of functional pores, rather than relying on the presence of differentiated guard cells

Summary

Introduction

The formation of stomata and leaf mesophyll airspace must be coordinated to establish an efficient and robust network that facilitates gas exchange for photosynthesis, the mechanism by which this coordinated development occurs remains unclear. That the degree and extent of separation of mesophyll cells to form airspaces is linked to the presence of functional pores (i.e., stomata that allow gas flux), rather than relying on the presence of differentiated guard cells. They suggest a step-wise selection during wheat evolution for leaves with a decreased stomatal density/increased stomatal size that is associated with both a decrease in gs and a decrease in mesophyll porosity, yielding a denser leaf. We clarify the link between stomata and mesophyll airspace development in both monocot and eudicot leaf systems and provide new insights into the process of wheat leaf evolution

Methods

Results

Conclusion