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

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...

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Main Authors: Maria Ermakova, Hannah Osborn, Michael Groszmann, Soumi Bala, Andrew Bowerman, Samantha McGaughey, Caitlin Byrt, Hugo Alonso-cantabrana, Steve Tyerman, Robert T Furbank, Robert E Sharwood, Susanne von Caemmerer
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-11-01
Series:eLife
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Online Access:https://elifesciences.org/articles/70095
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author Maria Ermakova
Hannah Osborn
Michael Groszmann
Soumi Bala
Andrew Bowerman
Samantha McGaughey
Caitlin Byrt
Hugo Alonso-cantabrana
Steve Tyerman
Robert T Furbank
Robert E Sharwood
Susanne von Caemmerer
author_facet Maria Ermakova
Hannah Osborn
Michael Groszmann
Soumi Bala
Andrew Bowerman
Samantha McGaughey
Caitlin Byrt
Hugo Alonso-cantabrana
Steve Tyerman
Robert T Furbank
Robert E Sharwood
Susanne von Caemmerer
author_sort Maria Ermakova
collection DOAJ
description 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.
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spelling doaj.art-03d8535519cd4f69b0bfbc6e492119a82022-12-22T02:02:02ZengeLife Sciences Publications LtdeLife2050-084X2021-11-011010.7554/eLife.70095Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridisMaria Ermakova0https://orcid.org/0000-0001-8466-4186Hannah Osborn1Michael Groszmann2https://orcid.org/0000-0002-5015-6156Soumi Bala3Andrew Bowerman4https://orcid.org/0000-0003-1729-7843Samantha McGaughey5https://orcid.org/0000-0001-6133-0415Caitlin Byrt6https://orcid.org/0000-0001-8549-2873Hugo Alonso-cantabrana7https://orcid.org/0000-0002-5462-5861Steve Tyerman8https://orcid.org/0000-0003-2455-1643Robert T Furbank9https://orcid.org/0000-0001-8700-6613Robert E Sharwood10https://orcid.org/0000-0003-4993-3816Susanne von Caemmerer11https://orcid.org/0000-0002-8366-2071Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaARC Centre of Excellence in Plant Energy Biology, School of Agriculture Food and Wine, University of Adelaide, Adelaide, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, Australia; Hawkesbury Institute for the Environment, Western Sydney University, Richmond, AustraliaAustralian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Research School of Biology, Canberra, AustraliaA 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.https://elifesciences.org/articles/70095Setaria viridisSetaria italicaaquaporinmesophyll conductancec4 photosynthesisco2 diffusion
spellingShingle Maria Ermakova
Hannah Osborn
Michael Groszmann
Soumi Bala
Andrew Bowerman
Samantha McGaughey
Caitlin Byrt
Hugo Alonso-cantabrana
Steve Tyerman
Robert T Furbank
Robert E Sharwood
Susanne von Caemmerer
Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis
eLife
Setaria viridis
Setaria italica
aquaporin
mesophyll conductance
c4 photosynthesis
co2 diffusion
title Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis
title_full Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis
title_fullStr Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis
title_full_unstemmed Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis
title_short Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis
title_sort expression of a co2 permeable aquaporin enhances mesophyll conductance in the c4 species setaria viridis
topic Setaria viridis
Setaria italica
aquaporin
mesophyll conductance
c4 photosynthesis
co2 diffusion
url https://elifesciences.org/articles/70095
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