A chloroplast Glycolate catabolic pathway bypassing the endogenous photorespiratory cycle enhances photosynthesis, biomass and yield in rice (Oryza sativa L.)
•Introduction of E. coli glycolate catabolic pathway in rice enhanced photosynthetic efficiency of RuBisCO.•Reduced photorespiration showed superior plant architecture and higher grain yield.•Partial photorespiratory bypass transgenics performed agronomically better than full bypass lines. Photoresp...
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Veröffentlicht in: | Plant science (Limerick) 2022-01, Vol.314, p.111103-111103, Article 111103 |
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creator | Nayak, Lopamudra Panda, Darshan Dash, Goutam Kumar Lal, Milan Kumar Swain, Padmini Baig, M.J. Kumar, Awadhesh |
description | •Introduction of E. coli glycolate catabolic pathway in rice enhanced photosynthetic efficiency of RuBisCO.•Reduced photorespiration showed superior plant architecture and higher grain yield.•Partial photorespiratory bypass transgenics performed agronomically better than full bypass lines.
Photorespiration accounts for 20–50 % reduction in grain yield in C3 crops. The process is essential to remove 2-phosphoglycolate produced due to the oxygenation activity of the ribulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO) enzyme. Attempts were made to improve photosynthesis through enriched CO2 concentration by installing numerous photorespiratory bypass modules in the chloroplast of several crops. In this study, we have introduced Escherichia coli glycolate catabolic pathway (ECGC) into rice chloroplast to bypass photorespiration partially (PB) or completely (FB). Five genes encoding glyoxylate carboligase (GCL), tartronic semialdehyde reductase (TSR), and three subunits of glycolate dehydrogenase (GDH) were introduced to get FB plants, whereas only the three subunits of GDH were introduced to get PB plants. Southern analysis confirmed stable integration of the transgenes and their expression was confirmed by RT-qPCR analysis in the T3 progenies. Both FB and PB transformed lines exhibited increased photosynthetic efficiency, biomass, and grain yield than wild type (WT) with empty vector control. The introduction of ECGC pathway favoured the carboxylase activity of RuBisCO while decreasing its oxygenase activity fostering the functioning of Calvin-Benson cycle and resulting in an increased carbon-assimilation that was manifested in their superior architecture and harvest index. These findings will support rice and related cereal crop breeding programs to increase yield under elevated temperature and arid conditions. |
doi_str_mv | 10.1016/j.plantsci.2021.111103 |
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Photorespiration accounts for 20–50 % reduction in grain yield in C3 crops. The process is essential to remove 2-phosphoglycolate produced due to the oxygenation activity of the ribulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO) enzyme. Attempts were made to improve photosynthesis through enriched CO2 concentration by installing numerous photorespiratory bypass modules in the chloroplast of several crops. In this study, we have introduced Escherichia coli glycolate catabolic pathway (ECGC) into rice chloroplast to bypass photorespiration partially (PB) or completely (FB). Five genes encoding glyoxylate carboligase (GCL), tartronic semialdehyde reductase (TSR), and three subunits of glycolate dehydrogenase (GDH) were introduced to get FB plants, whereas only the three subunits of GDH were introduced to get PB plants. Southern analysis confirmed stable integration of the transgenes and their expression was confirmed by RT-qPCR analysis in the T3 progenies. Both FB and PB transformed lines exhibited increased photosynthetic efficiency, biomass, and grain yield than wild type (WT) with empty vector control. The introduction of ECGC pathway favoured the carboxylase activity of RuBisCO while decreasing its oxygenase activity fostering the functioning of Calvin-Benson cycle and resulting in an increased carbon-assimilation that was manifested in their superior architecture and harvest index. These findings will support rice and related cereal crop breeding programs to increase yield under elevated temperature and arid conditions.</description><identifier>ISSN: 0168-9452</identifier><identifier>EISSN: 1873-2259</identifier><identifier>DOI: 10.1016/j.plantsci.2021.111103</identifier><identifier>PMID: 34895540</identifier><language>eng</language><publisher>Ireland: Elsevier B.V</publisher><subject>Biomass ; Chloroplasts - metabolism ; Crop Production ; Crops, Agricultural - genetics ; Crops, Agricultural - physiology ; Glycolate catabolic pathway ; Glycolates - metabolism ; Metabolic Networks and Pathways - genetics ; Oryza - genetics ; Oryza - growth & development ; Photorespiratory bypass mechanism ; Photosynthesis ; Photosynthesis - physiology ; Rice ; Yield</subject><ispartof>Plant science (Limerick), 2022-01, Vol.314, p.111103-111103, Article 111103</ispartof><rights>2021 Elsevier B.V.</rights><rights>Copyright © 2021 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c368t-35ed73103b25d1da1528cea07a8439b5d92251907441cb075cfc77d0aa59357a3</citedby><cites>FETCH-LOGICAL-c368t-35ed73103b25d1da1528cea07a8439b5d92251907441cb075cfc77d0aa59357a3</cites><orcidid>0000-0003-1803-6821 ; 0000-0002-4428-1030 ; 0000-0002-2442-9640</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.plantsci.2021.111103$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34895540$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nayak, Lopamudra</creatorcontrib><creatorcontrib>Panda, Darshan</creatorcontrib><creatorcontrib>Dash, Goutam Kumar</creatorcontrib><creatorcontrib>Lal, Milan Kumar</creatorcontrib><creatorcontrib>Swain, Padmini</creatorcontrib><creatorcontrib>Baig, M.J.</creatorcontrib><creatorcontrib>Kumar, Awadhesh</creatorcontrib><title>A chloroplast Glycolate catabolic pathway bypassing the endogenous photorespiratory cycle enhances photosynthesis, biomass and yield in rice (Oryza sativa L.)</title><title>Plant science (Limerick)</title><addtitle>Plant Sci</addtitle><description>•Introduction of E. coli glycolate catabolic pathway in rice enhanced photosynthetic efficiency of RuBisCO.•Reduced photorespiration showed superior plant architecture and higher grain yield.•Partial photorespiratory bypass transgenics performed agronomically better than full bypass lines.
Photorespiration accounts for 20–50 % reduction in grain yield in C3 crops. The process is essential to remove 2-phosphoglycolate produced due to the oxygenation activity of the ribulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO) enzyme. Attempts were made to improve photosynthesis through enriched CO2 concentration by installing numerous photorespiratory bypass modules in the chloroplast of several crops. In this study, we have introduced Escherichia coli glycolate catabolic pathway (ECGC) into rice chloroplast to bypass photorespiration partially (PB) or completely (FB). Five genes encoding glyoxylate carboligase (GCL), tartronic semialdehyde reductase (TSR), and three subunits of glycolate dehydrogenase (GDH) were introduced to get FB plants, whereas only the three subunits of GDH were introduced to get PB plants. Southern analysis confirmed stable integration of the transgenes and their expression was confirmed by RT-qPCR analysis in the T3 progenies. Both FB and PB transformed lines exhibited increased photosynthetic efficiency, biomass, and grain yield than wild type (WT) with empty vector control. The introduction of ECGC pathway favoured the carboxylase activity of RuBisCO while decreasing its oxygenase activity fostering the functioning of Calvin-Benson cycle and resulting in an increased carbon-assimilation that was manifested in their superior architecture and harvest index. These findings will support rice and related cereal crop breeding programs to increase yield under elevated temperature and arid conditions.</description><subject>Biomass</subject><subject>Chloroplasts - metabolism</subject><subject>Crop Production</subject><subject>Crops, Agricultural - genetics</subject><subject>Crops, Agricultural - physiology</subject><subject>Glycolate catabolic pathway</subject><subject>Glycolates - metabolism</subject><subject>Metabolic Networks and Pathways - genetics</subject><subject>Oryza - genetics</subject><subject>Oryza - growth & development</subject><subject>Photorespiratory bypass mechanism</subject><subject>Photosynthesis</subject><subject>Photosynthesis - physiology</subject><subject>Rice</subject><subject>Yield</subject><issn>0168-9452</issn><issn>1873-2259</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkcFu3CAURVHUqpmm_YWIZSrFLmBj7F2jKE0rjZRNu0bP8CZm5DEOMKncj8m3htFMui0bkDj3Pr17CbnkrOSMN1-35TzClKJxpWCClzwfVp2RFW9VVQghu3dklcG26GopzsnHGLeMMSGl-kDOq7rtpKzZirzcUDOMPvhsFxO9HxfjR0hIDSTo_egMnSENf2Ch_TJDjG56pGlAipP1jzj5faTz4JMPGGcXID8WahYzHogBJoOn_7hMWRZdvKa987vsRGGydHE4WuomGpxBevUQlr9AIyT3DHRdfvlE3m9gjPj5dF-Q39_vft3-KNYP9z9vb9aFqZo2FZVEq6ocQC-k5Ra4FK1BYArauup6abucCO-Yqmtueqak2RilLAOQXSUVVBfk6ug7B_-0x5j0zkWDY84Y84paNCznKIVsMtocURN8jAE3eg5uB2HRnOlDN3qr37rRh270sZssvDzN2Pc7tP9kb2Vk4NsRwLzps8OgswXmCK0LaJK23v1vxisgU6ag</recordid><startdate>202201</startdate><enddate>202201</enddate><creator>Nayak, Lopamudra</creator><creator>Panda, Darshan</creator><creator>Dash, Goutam Kumar</creator><creator>Lal, Milan Kumar</creator><creator>Swain, Padmini</creator><creator>Baig, M.J.</creator><creator>Kumar, Awadhesh</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-1803-6821</orcidid><orcidid>https://orcid.org/0000-0002-4428-1030</orcidid><orcidid>https://orcid.org/0000-0002-2442-9640</orcidid></search><sort><creationdate>202201</creationdate><title>A chloroplast Glycolate catabolic pathway bypassing the endogenous photorespiratory cycle enhances photosynthesis, biomass and yield in rice (Oryza sativa L.)</title><author>Nayak, Lopamudra ; Panda, Darshan ; Dash, Goutam Kumar ; Lal, Milan Kumar ; Swain, Padmini ; Baig, M.J. ; Kumar, Awadhesh</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c368t-35ed73103b25d1da1528cea07a8439b5d92251907441cb075cfc77d0aa59357a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Biomass</topic><topic>Chloroplasts - metabolism</topic><topic>Crop Production</topic><topic>Crops, Agricultural - genetics</topic><topic>Crops, Agricultural - physiology</topic><topic>Glycolate catabolic pathway</topic><topic>Glycolates - metabolism</topic><topic>Metabolic Networks and Pathways - genetics</topic><topic>Oryza - genetics</topic><topic>Oryza - growth & development</topic><topic>Photorespiratory bypass mechanism</topic><topic>Photosynthesis</topic><topic>Photosynthesis - physiology</topic><topic>Rice</topic><topic>Yield</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nayak, Lopamudra</creatorcontrib><creatorcontrib>Panda, Darshan</creatorcontrib><creatorcontrib>Dash, Goutam Kumar</creatorcontrib><creatorcontrib>Lal, Milan Kumar</creatorcontrib><creatorcontrib>Swain, Padmini</creatorcontrib><creatorcontrib>Baig, M.J.</creatorcontrib><creatorcontrib>Kumar, Awadhesh</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Plant science (Limerick)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nayak, Lopamudra</au><au>Panda, Darshan</au><au>Dash, Goutam Kumar</au><au>Lal, Milan Kumar</au><au>Swain, Padmini</au><au>Baig, M.J.</au><au>Kumar, Awadhesh</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A chloroplast Glycolate catabolic pathway bypassing the endogenous photorespiratory cycle enhances photosynthesis, biomass and yield in rice (Oryza sativa L.)</atitle><jtitle>Plant science (Limerick)</jtitle><addtitle>Plant Sci</addtitle><date>2022-01</date><risdate>2022</risdate><volume>314</volume><spage>111103</spage><epage>111103</epage><pages>111103-111103</pages><artnum>111103</artnum><issn>0168-9452</issn><eissn>1873-2259</eissn><abstract>•Introduction of E. coli glycolate catabolic pathway in rice enhanced photosynthetic efficiency of RuBisCO.•Reduced photorespiration showed superior plant architecture and higher grain yield.•Partial photorespiratory bypass transgenics performed agronomically better than full bypass lines.
Photorespiration accounts for 20–50 % reduction in grain yield in C3 crops. The process is essential to remove 2-phosphoglycolate produced due to the oxygenation activity of the ribulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO) enzyme. Attempts were made to improve photosynthesis through enriched CO2 concentration by installing numerous photorespiratory bypass modules in the chloroplast of several crops. In this study, we have introduced Escherichia coli glycolate catabolic pathway (ECGC) into rice chloroplast to bypass photorespiration partially (PB) or completely (FB). Five genes encoding glyoxylate carboligase (GCL), tartronic semialdehyde reductase (TSR), and three subunits of glycolate dehydrogenase (GDH) were introduced to get FB plants, whereas only the three subunits of GDH were introduced to get PB plants. Southern analysis confirmed stable integration of the transgenes and their expression was confirmed by RT-qPCR analysis in the T3 progenies. Both FB and PB transformed lines exhibited increased photosynthetic efficiency, biomass, and grain yield than wild type (WT) with empty vector control. The introduction of ECGC pathway favoured the carboxylase activity of RuBisCO while decreasing its oxygenase activity fostering the functioning of Calvin-Benson cycle and resulting in an increased carbon-assimilation that was manifested in their superior architecture and harvest index. These findings will support rice and related cereal crop breeding programs to increase yield under elevated temperature and arid conditions.</abstract><cop>Ireland</cop><pub>Elsevier B.V</pub><pmid>34895540</pmid><doi>10.1016/j.plantsci.2021.111103</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0003-1803-6821</orcidid><orcidid>https://orcid.org/0000-0002-4428-1030</orcidid><orcidid>https://orcid.org/0000-0002-2442-9640</orcidid></addata></record> |
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subjects | Biomass Chloroplasts - metabolism Crop Production Crops, Agricultural - genetics Crops, Agricultural - physiology Glycolate catabolic pathway Glycolates - metabolism Metabolic Networks and Pathways - genetics Oryza - genetics Oryza - growth & development Photorespiratory bypass mechanism Photosynthesis Photosynthesis - physiology Rice Yield |
title | A chloroplast Glycolate catabolic pathway bypassing the endogenous photorespiratory cycle enhances photosynthesis, biomass and yield in rice (Oryza sativa L.) |
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