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Expression of cyanobacterial genes enhanced CO(2) assimilation and biomass production in transgenic Arabidopsis thaliana

BACKGROUND: Photosynthesis is a key process in plants that is compromised by the oxygenase activity of Rubisco, which leads to the production of toxic compound phosphoglycolate that is catabolized by photorespiratory pathway. Transformation of plants with photorespiratory bypasses have been shown to...

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Autores principales: Abbasi, Anum Zeb, Bilal, Misbah, Khurshid, Ghazal, Yiotis, Charilaos, Zeb, Iftikhar, Hussain, Jamshaid, Baig, Ayesha, Shah, Mohammad Maroof, Chaudhary, Safee Ullah, Osborne, Bruce, Ahmad, Raza
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8359801/
https://www.ncbi.nlm.nih.gov/pubmed/34434649
http://dx.doi.org/10.7717/peerj.11860
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author Abbasi, Anum Zeb
Bilal, Misbah
Khurshid, Ghazal
Yiotis, Charilaos
Zeb, Iftikhar
Hussain, Jamshaid
Baig, Ayesha
Shah, Mohammad Maroof
Chaudhary, Safee Ullah
Osborne, Bruce
Ahmad, Raza
author_facet Abbasi, Anum Zeb
Bilal, Misbah
Khurshid, Ghazal
Yiotis, Charilaos
Zeb, Iftikhar
Hussain, Jamshaid
Baig, Ayesha
Shah, Mohammad Maroof
Chaudhary, Safee Ullah
Osborne, Bruce
Ahmad, Raza
author_sort Abbasi, Anum Zeb
collection PubMed
description BACKGROUND: Photosynthesis is a key process in plants that is compromised by the oxygenase activity of Rubisco, which leads to the production of toxic compound phosphoglycolate that is catabolized by photorespiratory pathway. Transformation of plants with photorespiratory bypasses have been shown to reduce photorespiration and enhance plant biomass. Interestingly, engineering of a single gene from such photorespiratory bypasses has also improved photosynthesis and plant productivity. Although single gene transformations may not completely reduce photorespiration, increases in plant biomass accumulation have still been observed indicating an alternative role in regulating different metabolic processes. Therefore, the current study was aimed at evaluating the underlying mechanism (s) associated with the effects of introducing a single cyanobacterial glycolate decarboxylation pathway gene on photosynthesis and plant performance. METHODS: Transgenic Arabidopsis thaliana plants (GD, HD, OX) expressing independently cyanobacterial decarboxylation pathway genes i.e., glycolate dehydrogenase, hydroxyacid dehydrogenase, and oxalate decarboxylase, respectively, were utilized. Photosynthetic, fluorescence related, and growth parameters were analyzed. Additionally, transcriptomic analysis of GD transgenic plants was also performed. RESULTS: The GD plants exhibited a significant increase (16%) in net photosynthesis rate while both HD and OX plants showed a non-significant (11%) increase as compared to wild type plants (WT). The stomatal conductance was significantly higher (24%) in GD and HD plants than the WT plants. The quantum efficiencies of photosystem II, carbon dioxide assimilation and the chlorophyll fluorescence-based photosynthetic electron transport rate were also higher than WT plants. The OX plants displayed significant reductions in the rate of photorespiration relative to gross photosynthesis and increase in the ratio of the photosynthetic electron flow attributable to carboxylation reactions over that attributable to oxygenation reactions. GD, HD and OX plants accumulated significantly higher biomass and seed weight. Soluble sugars were significantly increased in GD and HD plants, while the starch levels were higher in all transgenic plants. The transcriptomic analysis of GD plants revealed 650 up-regulated genes mainly related to photosynthesis, photorespiratory pathway, sucrose metabolism, chlorophyll biosynthesis and glutathione metabolism. CONCLUSION: This study revealed the potential of introduced cyanobacterial pathway genes to enhance photosynthetic and growth-related parameters. The upregulation of genes related to different pathways provided evidence of the underlying mechanisms involved particularly in GD plants. However, transcriptomic profiling of HD and OX plants can further help to identify other potential mechanisms involved in improved plant productivity.
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spelling pubmed-83598012021-08-24 Expression of cyanobacterial genes enhanced CO(2) assimilation and biomass production in transgenic Arabidopsis thaliana Abbasi, Anum Zeb Bilal, Misbah Khurshid, Ghazal Yiotis, Charilaos Zeb, Iftikhar Hussain, Jamshaid Baig, Ayesha Shah, Mohammad Maroof Chaudhary, Safee Ullah Osborne, Bruce Ahmad, Raza PeerJ Agricultural Science BACKGROUND: Photosynthesis is a key process in plants that is compromised by the oxygenase activity of Rubisco, which leads to the production of toxic compound phosphoglycolate that is catabolized by photorespiratory pathway. Transformation of plants with photorespiratory bypasses have been shown to reduce photorespiration and enhance plant biomass. Interestingly, engineering of a single gene from such photorespiratory bypasses has also improved photosynthesis and plant productivity. Although single gene transformations may not completely reduce photorespiration, increases in plant biomass accumulation have still been observed indicating an alternative role in regulating different metabolic processes. Therefore, the current study was aimed at evaluating the underlying mechanism (s) associated with the effects of introducing a single cyanobacterial glycolate decarboxylation pathway gene on photosynthesis and plant performance. METHODS: Transgenic Arabidopsis thaliana plants (GD, HD, OX) expressing independently cyanobacterial decarboxylation pathway genes i.e., glycolate dehydrogenase, hydroxyacid dehydrogenase, and oxalate decarboxylase, respectively, were utilized. Photosynthetic, fluorescence related, and growth parameters were analyzed. Additionally, transcriptomic analysis of GD transgenic plants was also performed. RESULTS: The GD plants exhibited a significant increase (16%) in net photosynthesis rate while both HD and OX plants showed a non-significant (11%) increase as compared to wild type plants (WT). The stomatal conductance was significantly higher (24%) in GD and HD plants than the WT plants. The quantum efficiencies of photosystem II, carbon dioxide assimilation and the chlorophyll fluorescence-based photosynthetic electron transport rate were also higher than WT plants. The OX plants displayed significant reductions in the rate of photorespiration relative to gross photosynthesis and increase in the ratio of the photosynthetic electron flow attributable to carboxylation reactions over that attributable to oxygenation reactions. GD, HD and OX plants accumulated significantly higher biomass and seed weight. Soluble sugars were significantly increased in GD and HD plants, while the starch levels were higher in all transgenic plants. The transcriptomic analysis of GD plants revealed 650 up-regulated genes mainly related to photosynthesis, photorespiratory pathway, sucrose metabolism, chlorophyll biosynthesis and glutathione metabolism. CONCLUSION: This study revealed the potential of introduced cyanobacterial pathway genes to enhance photosynthetic and growth-related parameters. The upregulation of genes related to different pathways provided evidence of the underlying mechanisms involved particularly in GD plants. However, transcriptomic profiling of HD and OX plants can further help to identify other potential mechanisms involved in improved plant productivity. PeerJ Inc. 2021-08-09 /pmc/articles/PMC8359801/ /pubmed/34434649 http://dx.doi.org/10.7717/peerj.11860 Text en © 2021 Abbasi et al. https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Agricultural Science
Abbasi, Anum Zeb
Bilal, Misbah
Khurshid, Ghazal
Yiotis, Charilaos
Zeb, Iftikhar
Hussain, Jamshaid
Baig, Ayesha
Shah, Mohammad Maroof
Chaudhary, Safee Ullah
Osborne, Bruce
Ahmad, Raza
Expression of cyanobacterial genes enhanced CO(2) assimilation and biomass production in transgenic Arabidopsis thaliana
title Expression of cyanobacterial genes enhanced CO(2) assimilation and biomass production in transgenic Arabidopsis thaliana
title_full Expression of cyanobacterial genes enhanced CO(2) assimilation and biomass production in transgenic Arabidopsis thaliana
title_fullStr Expression of cyanobacterial genes enhanced CO(2) assimilation and biomass production in transgenic Arabidopsis thaliana
title_full_unstemmed Expression of cyanobacterial genes enhanced CO(2) assimilation and biomass production in transgenic Arabidopsis thaliana
title_short Expression of cyanobacterial genes enhanced CO(2) assimilation and biomass production in transgenic Arabidopsis thaliana
title_sort expression of cyanobacterial genes enhanced co(2) assimilation and biomass production in transgenic arabidopsis thaliana
topic Agricultural Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8359801/
https://www.ncbi.nlm.nih.gov/pubmed/34434649
http://dx.doi.org/10.7717/peerj.11860
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