Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis.

Maria Ermakova,Susanne Von Caemmerer,Hugo Alonso-Cantabrana,Hannah Osborn,Robert T Furbank,Caitlin Byrt,Samantha Mcgaughey,Michael Groszmann,Andrew Bowerman,Soumi Bala,Robert E Sharwood,Steve Tyerman

doi:10.7554/elife.70095

Maria Ermakova, Susanne Von Caemmerer + Show 10 more

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https://doi.org/10.7554/elife.70095

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Abstract

A fundamental limitation of photosynthetic carbon fixation is the availability of CO2. In C4 plants, primary carboxylation occurs in mesophyll cytosol, and little is known about the role of CO2 diffusion in facilitating C4 photosynthesis. We have examined the expression, localization, and functional role of selected plasma membrane intrinsic aquaporins (PIPs) from Setaria italica (foxtail millet) and discovered that SiPIP2;7 is CO2-permeable. When ectopically expressed in mesophyll cells of Setaria viridis (green foxtail), SiPIP2;7 was localized to the plasma membrane and caused no marked changes in leaf biochemistry. Gas exchange and C18O16O discrimination measurements revealed that targeted expression of SiPIP2;7 enhanced the conductance to CO2 diffusion from the intercellular airspace to the mesophyll cytosol. Our results demonstrate that mesophyll conductance limits C4 photosynthesis at low pCO2 and that SiPIP2;7 is a functional CO2 permeable aquaporin that can improve CO2 diffusion at the airspace/mesophyll interface and enhance C4 photosynthesis.

Highlights

Diffusion of CO2 across biological membranes is a fundamental aspect to photosynthesis
Our results demonstrate that CO2-permeable aquaporins can be used to increase CO2 diffusion from the intercellular airspace to mesophyll cytosol to provide higher carboxylation efficiency in C4 leaves
Four PIP1 and eight PIP2 genes were identified in both S. italica and S. viridis and their protein sequences were 99–100 % identical between the two species (Supplementary File 1)

Summary

Introduction

Diffusion of CO2 across biological membranes is a fundamental aspect to photosynthesis. Aquaporins have key roles in regulating the movement of water and solutes into roots and between tissues, cells and organelles (Tyerman, McGaughey, Qiu, Yool, & Byrt, 2021). These pore-forming integral membrane proteins can be divided into multiple sub-families depending on their amino acid sequence and sub-cellular localization. PIP2s show higher water permeability when expressed in heterologous systems (Chaumont, Barrieu, Jung, & Chrispeels, 2000) and PIP1s seemingly require interaction with a PIP2 to correctly traffic to the plasma membrane (Berny, Gilis, Rooman, & Chaumont, 2016; Zelazny et al, 2007).

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