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A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C(3) plants

Plants employ photosynthesis to produce sugars for supporting their growth. During photosynthesis, an enzyme Ribulose 1,5 bisphosphate carboxylase/oxygenase (Rubisco) combines its substrate Ribulose 1,5 bisphosphate (RuBP) with CO(2) to produce phosphoglycerate (PGA). Alongside, Rubisco also takes u...

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Autores principales: Khurshid, Ghazal, Abbassi, Anum Zeb, Khalid, Muhammad Farhan, Gondal, Mahnoor Naseer, Naqvi, Tatheer Alam, Shah, Mohammad Maroof, Chaudhary, Safee Ullah, Ahmad, Raza
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7705653/
https://www.ncbi.nlm.nih.gov/pubmed/33257792
http://dx.doi.org/10.1038/s41598-020-77894-2
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author Khurshid, Ghazal
Abbassi, Anum Zeb
Khalid, Muhammad Farhan
Gondal, Mahnoor Naseer
Naqvi, Tatheer Alam
Shah, Mohammad Maroof
Chaudhary, Safee Ullah
Ahmad, Raza
author_facet Khurshid, Ghazal
Abbassi, Anum Zeb
Khalid, Muhammad Farhan
Gondal, Mahnoor Naseer
Naqvi, Tatheer Alam
Shah, Mohammad Maroof
Chaudhary, Safee Ullah
Ahmad, Raza
author_sort Khurshid, Ghazal
collection PubMed
description Plants employ photosynthesis to produce sugars for supporting their growth. During photosynthesis, an enzyme Ribulose 1,5 bisphosphate carboxylase/oxygenase (Rubisco) combines its substrate Ribulose 1,5 bisphosphate (RuBP) with CO(2) to produce phosphoglycerate (PGA). Alongside, Rubisco also takes up O(2) and produce 2-phosphoglycolate (2-PG), a toxic compound broken down into PGA through photorespiration. Photorespiration is not only a resource-demanding process but also results in CO(2) loss which affects photosynthetic efficiency in C(3) plants. Here, we propose to circumvent photorespiration by adopting the cyanobacterial glycolate decarboxylation pathway into C(3) plants. For that, we have integrated the cyanobacterial glycolate decarboxylation pathway into a kinetic model of C(3) photosynthetic pathway to evaluate its impact on photosynthesis and photorespiration. Our results show that the cyanobacterial glycolate decarboxylation bypass model exhibits a 10% increase in net photosynthetic rate (A) in comparison with C(3) model. Moreover, an increased supply of intercellular CO(2) (C(i)) from the bypass resulted in a 54.8% increase in PGA while reducing photorespiratory intermediates including glycolate (− 49%) and serine (− 32%). The bypass model, at default conditions, also elucidated a decline in phosphate-based metabolites including RuBP (− 61.3%). The C(3) model at elevated level of inorganic phosphate (Pi), exhibited a significant change in RuBP (+ 355%) and PGA (− 98%) which is attributable to the low availability of C(i). Whereas, at elevated Pi, the bypass model exhibited an increase of 73.1% and 33.9% in PGA and RuBP, respectively. Therefore, we deduce a synergistic effect of elevation in CO(2) and Pi pool on photosynthesis. We also evaluated the integrative action of CO(2), Pi, and Rubisco carboxylation activity (V(cmax)) on A and observed that their simultaneous increase raised A by 26%, in the bypass model. Taken together, the study potentiates engineering of cyanobacterial decarboxylation pathway in C(3) plants to bypass photorespiration thereby increasing the overall efficiency of photosynthesis.
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spelling pubmed-77056532020-12-02 A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C(3) plants Khurshid, Ghazal Abbassi, Anum Zeb Khalid, Muhammad Farhan Gondal, Mahnoor Naseer Naqvi, Tatheer Alam Shah, Mohammad Maroof Chaudhary, Safee Ullah Ahmad, Raza Sci Rep Article Plants employ photosynthesis to produce sugars for supporting their growth. During photosynthesis, an enzyme Ribulose 1,5 bisphosphate carboxylase/oxygenase (Rubisco) combines its substrate Ribulose 1,5 bisphosphate (RuBP) with CO(2) to produce phosphoglycerate (PGA). Alongside, Rubisco also takes up O(2) and produce 2-phosphoglycolate (2-PG), a toxic compound broken down into PGA through photorespiration. Photorespiration is not only a resource-demanding process but also results in CO(2) loss which affects photosynthetic efficiency in C(3) plants. Here, we propose to circumvent photorespiration by adopting the cyanobacterial glycolate decarboxylation pathway into C(3) plants. For that, we have integrated the cyanobacterial glycolate decarboxylation pathway into a kinetic model of C(3) photosynthetic pathway to evaluate its impact on photosynthesis and photorespiration. Our results show that the cyanobacterial glycolate decarboxylation bypass model exhibits a 10% increase in net photosynthetic rate (A) in comparison with C(3) model. Moreover, an increased supply of intercellular CO(2) (C(i)) from the bypass resulted in a 54.8% increase in PGA while reducing photorespiratory intermediates including glycolate (− 49%) and serine (− 32%). The bypass model, at default conditions, also elucidated a decline in phosphate-based metabolites including RuBP (− 61.3%). The C(3) model at elevated level of inorganic phosphate (Pi), exhibited a significant change in RuBP (+ 355%) and PGA (− 98%) which is attributable to the low availability of C(i). Whereas, at elevated Pi, the bypass model exhibited an increase of 73.1% and 33.9% in PGA and RuBP, respectively. Therefore, we deduce a synergistic effect of elevation in CO(2) and Pi pool on photosynthesis. We also evaluated the integrative action of CO(2), Pi, and Rubisco carboxylation activity (V(cmax)) on A and observed that their simultaneous increase raised A by 26%, in the bypass model. Taken together, the study potentiates engineering of cyanobacterial decarboxylation pathway in C(3) plants to bypass photorespiration thereby increasing the overall efficiency of photosynthesis. Nature Publishing Group UK 2020-11-30 /pmc/articles/PMC7705653/ /pubmed/33257792 http://dx.doi.org/10.1038/s41598-020-77894-2 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Khurshid, Ghazal
Abbassi, Anum Zeb
Khalid, Muhammad Farhan
Gondal, Mahnoor Naseer
Naqvi, Tatheer Alam
Shah, Mohammad Maroof
Chaudhary, Safee Ullah
Ahmad, Raza
A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C(3) plants
title A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C(3) plants
title_full A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C(3) plants
title_fullStr A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C(3) plants
title_full_unstemmed A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C(3) plants
title_short A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C(3) plants
title_sort cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in c(3) plants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7705653/
https://www.ncbi.nlm.nih.gov/pubmed/33257792
http://dx.doi.org/10.1038/s41598-020-77894-2
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