A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C-4 photosynthesis
In C4 species, β-carbonic anhydrase (CA), localized to the cytosol of the mesophyll cells, accelerates the interconversion of CO2 to HCO3–, the substrate used by phosphoenolpyruvate carboxylase (PEPC) in the first step of C4 photosynthesis. Here we describe the identification and characterization of...
| Autores principales: | , , , , , , , , , , , , , , , , |
|---|---|
| Formato: | Journal Article |
| Lenguaje: | Inglés |
| Publicado: |
Oxford University Press
2021
|
| Materias: | |
| Acceso en línea: | https://hdl.handle.net/10568/164350 |
| _version_ | 1855513802486841344 |
|---|---|
| author | Chatterjee, Jolly Coe, Robert A. Acebron, Kelvin Thakur, Vivek Yennamalli, Ragothaman M. Danila, Florence Lin, Hsiang-Chun Balahadia, Christian Paolo Bagunu, Efren Padhma, Preiya P O.S. Bala, Soumi Yin, Xiaojia Rizal, Govinda Dionora, Jacqueline Furbank, Robert T. von Caemmerer, Susanne Quick, William Paul |
| author_browse | Acebron, Kelvin Bagunu, Efren Bala, Soumi Balahadia, Christian Paolo Chatterjee, Jolly Coe, Robert A. Danila, Florence Dionora, Jacqueline Furbank, Robert T. Lin, Hsiang-Chun Padhma, Preiya P O.S. Quick, William Paul Rizal, Govinda Thakur, Vivek Yennamalli, Ragothaman M. Yin, Xiaojia von Caemmerer, Susanne |
| author_facet | Chatterjee, Jolly Coe, Robert A. Acebron, Kelvin Thakur, Vivek Yennamalli, Ragothaman M. Danila, Florence Lin, Hsiang-Chun Balahadia, Christian Paolo Bagunu, Efren Padhma, Preiya P O.S. Bala, Soumi Yin, Xiaojia Rizal, Govinda Dionora, Jacqueline Furbank, Robert T. von Caemmerer, Susanne Quick, William Paul |
| author_sort | Chatterjee, Jolly |
| collection | Repository of Agricultural Research Outputs (CGSpace) |
| description | In C4 species, β-carbonic anhydrase (CA), localized to the cytosol of the mesophyll cells, accelerates the interconversion of CO2 to HCO3–, the substrate used by phosphoenolpyruvate carboxylase (PEPC) in the first step of C4 photosynthesis. Here we describe the identification and characterization of low CO2-responsive mutant 1 (lcr1) isolated from an N-nitroso-N-methylurea- (NMU) treated Setaria viridis mutant population. Forward genetic investigation revealed that the mutated gene Sevir.5G247800 of lcr1 possessed a single nucleotide transition from cytosine to thymine in a β-CA gene causing an amino acid change from leucine to phenylalanine. This resulted in severe reduction in growth and photosynthesis in the mutant. Both the CO2 compensation point and carbon isotope discrimination values of the mutant were significantly increased. Growth of the mutants was stunted when grown under ambient pCO2 but recovered at elevated pCO2. Further bioinformatics analyses revealed that the mutation has led to functional changes in one of the conserved residues of the protein, situated near the catalytic site. CA transcript accumulation in the mutant was 80% lower, CA protein accumulation 30% lower, and CA activity ~98% lower compared with the wild type. Changes in the abundance of other primary C4 pathway enzymes were observed; accumulation of PEPC protein was significantly increased and accumulation of malate dehydrogenase and malic enzyme decreased. The reduction of CA protein activity and abundance in lcr1 restricts the supply of bicarbonate to PEPC, limiting C4 photosynthesis and growth. This study establishes Sevir.5G247800 as the major CA allele in Setaria for C4 photosynthesis and provides important insights into the function of CA in C4 photosynthesis that would be required to generate a rice plant with a functional C4 biochemical pathway. |
| format | Journal Article |
| id | CGSpace164350 |
| institution | CGIAR Consortium |
| language | Inglés |
| publishDate | 2021 |
| publishDateRange | 2021 |
| publishDateSort | 2021 |
| publisher | Oxford University Press |
| publisherStr | Oxford University Press |
| record_format | dspace |
| spelling | CGSpace1643502025-12-08T09:54:28Z A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C-4 photosynthesis Chatterjee, Jolly Coe, Robert A. Acebron, Kelvin Thakur, Vivek Yennamalli, Ragothaman M. Danila, Florence Lin, Hsiang-Chun Balahadia, Christian Paolo Bagunu, Efren Padhma, Preiya P O.S. Bala, Soumi Yin, Xiaojia Rizal, Govinda Dionora, Jacqueline Furbank, Robert T. von Caemmerer, Susanne Quick, William Paul plant science physiology In C4 species, β-carbonic anhydrase (CA), localized to the cytosol of the mesophyll cells, accelerates the interconversion of CO2 to HCO3–, the substrate used by phosphoenolpyruvate carboxylase (PEPC) in the first step of C4 photosynthesis. Here we describe the identification and characterization of low CO2-responsive mutant 1 (lcr1) isolated from an N-nitroso-N-methylurea- (NMU) treated Setaria viridis mutant population. Forward genetic investigation revealed that the mutated gene Sevir.5G247800 of lcr1 possessed a single nucleotide transition from cytosine to thymine in a β-CA gene causing an amino acid change from leucine to phenylalanine. This resulted in severe reduction in growth and photosynthesis in the mutant. Both the CO2 compensation point and carbon isotope discrimination values of the mutant were significantly increased. Growth of the mutants was stunted when grown under ambient pCO2 but recovered at elevated pCO2. Further bioinformatics analyses revealed that the mutation has led to functional changes in one of the conserved residues of the protein, situated near the catalytic site. CA transcript accumulation in the mutant was 80% lower, CA protein accumulation 30% lower, and CA activity ~98% lower compared with the wild type. Changes in the abundance of other primary C4 pathway enzymes were observed; accumulation of PEPC protein was significantly increased and accumulation of malate dehydrogenase and malic enzyme decreased. The reduction of CA protein activity and abundance in lcr1 restricts the supply of bicarbonate to PEPC, limiting C4 photosynthesis and growth. This study establishes Sevir.5G247800 as the major CA allele in Setaria for C4 photosynthesis and provides important insights into the function of CA in C4 photosynthesis that would be required to generate a rice plant with a functional C4 biochemical pathway. 2021-04-02 2024-12-19T12:53:45Z 2024-12-19T12:53:45Z Journal Article https://hdl.handle.net/10568/164350 en Open Access Oxford University Press Chatterjee, Jolly; Coe, Robert A; Acebron, Kelvin; Thakur, Vivek; Yennamalli, Ragothaman M; Danila, Florence; Lin, Hsiang-Chun; Balahadia, Christian Paolo; Bagunu, Efren; Padhma, Preiya P O S; Bala, Soumi; Yin, Xiaojia; Rizal, Govinda; Dionora, Jacqueline; Furbank, Robert T; von Caemmerer, Susanne and Quick, William Paul. 2021. A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C-4 photosynthesis. Journal of Experimental Botany, Volume 72, no. 8 p. 3122-3136 |
| spellingShingle | plant science physiology Chatterjee, Jolly Coe, Robert A. Acebron, Kelvin Thakur, Vivek Yennamalli, Ragothaman M. Danila, Florence Lin, Hsiang-Chun Balahadia, Christian Paolo Bagunu, Efren Padhma, Preiya P O.S. Bala, Soumi Yin, Xiaojia Rizal, Govinda Dionora, Jacqueline Furbank, Robert T. von Caemmerer, Susanne Quick, William Paul A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C-4 photosynthesis |
| title | A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C-4 photosynthesis |
| title_full | A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C-4 photosynthesis |
| title_fullStr | A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C-4 photosynthesis |
| title_full_unstemmed | A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C-4 photosynthesis |
| title_short | A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C-4 photosynthesis |
| title_sort | low co2 responsive mutant of setaria viridis reveals that reduced carbonic anhydrase limits c 4 photosynthesis |
| topic | plant science physiology |
| url | https://hdl.handle.net/10568/164350 |
| work_keys_str_mv | AT chatterjeejolly alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT coeroberta alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT acebronkelvin alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT thakurvivek alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT yennamalliragothamanm alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT danilaflorence alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT linhsiangchun alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT balahadiachristianpaolo alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT bagunuefren alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT padhmapreiyapos alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT balasoumi alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT yinxiaojia alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT rizalgovinda alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT dionorajacqueline alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT furbankrobertt alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT voncaemmerersusanne alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT quickwilliampaul alowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT chatterjeejolly lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT coeroberta lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT acebronkelvin lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT thakurvivek lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT yennamalliragothamanm lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT danilaflorence lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT linhsiangchun lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT balahadiachristianpaolo lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT bagunuefren lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT padhmapreiyapos lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT balasoumi lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT yinxiaojia lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT rizalgovinda lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT dionorajacqueline lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT furbankrobertt lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT voncaemmerersusanne lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis AT quickwilliampaul lowco2responsivemutantofsetariaviridisrevealsthatreducedcarbonicanhydraselimitsc4photosynthesis |