Key changes in gene expression identified for different stages of C-4 evolution in Alloteropsis semialata

C4 photosynthesis is a complex trait that boosts productivity in tropical conditions. Compared with C3 species, the C4 state seems to require numerous novelties, but species comparisons can be confounded by long divergence times. Here, we exploit the photosynthetic diversity that exists within a sin...

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Autores principales: Dunning, Luke T., Moreno-Villena, Jose J., Lundgren, Marjorie R., Dionora, Jacqueline, Salazar, Paolo, Adams, Claire, Nyirenda, Florence, Olofsson, Jill K., Mapaura, Anthony, Grundy, Isla M., Kayombo, Canisius J., Dunning, Lucy A., Kentatchime, Fabrice, Ariyarathne, Menaka, Yakandawala, Deepthi, Besnard, Guillaume, Quick, W. Paul, Bräutigam, Andrea, Osborne, Colin P., Christin, Pascal-Antoine
Formato: Journal Article
Lenguaje:Inglés
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://hdl.handle.net/10568/164699
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author Dunning, Luke T.
Moreno-Villena, Jose J.
Lundgren, Marjorie R.
Dionora, Jacqueline
Salazar, Paolo
Adams, Claire
Nyirenda, Florence
Olofsson, Jill K.
Mapaura, Anthony
Grundy, Isla M.
Kayombo, Canisius J.
Dunning, Lucy A.
Kentatchime, Fabrice
Ariyarathne, Menaka
Yakandawala, Deepthi
Besnard, Guillaume
Quick, W. Paul
Bräutigam, Andrea
Osborne, Colin P.
Christin, Pascal-Antoine
author_browse Adams, Claire
Ariyarathne, Menaka
Besnard, Guillaume
Bräutigam, Andrea
Christin, Pascal-Antoine
Dionora, Jacqueline
Dunning, Lucy A.
Dunning, Luke T.
Grundy, Isla M.
Kayombo, Canisius J.
Kentatchime, Fabrice
Lundgren, Marjorie R.
Mapaura, Anthony
Moreno-Villena, Jose J.
Nyirenda, Florence
Olofsson, Jill K.
Osborne, Colin P.
Quick, W. Paul
Salazar, Paolo
Yakandawala, Deepthi
author_facet Dunning, Luke T.
Moreno-Villena, Jose J.
Lundgren, Marjorie R.
Dionora, Jacqueline
Salazar, Paolo
Adams, Claire
Nyirenda, Florence
Olofsson, Jill K.
Mapaura, Anthony
Grundy, Isla M.
Kayombo, Canisius J.
Dunning, Lucy A.
Kentatchime, Fabrice
Ariyarathne, Menaka
Yakandawala, Deepthi
Besnard, Guillaume
Quick, W. Paul
Bräutigam, Andrea
Osborne, Colin P.
Christin, Pascal-Antoine
author_sort Dunning, Luke T.
collection Repository of Agricultural Research Outputs (CGSpace)
description C4 photosynthesis is a complex trait that boosts productivity in tropical conditions. Compared with C3 species, the C4 state seems to require numerous novelties, but species comparisons can be confounded by long divergence times. Here, we exploit the photosynthetic diversity that exists within a single species, the grass Alloteropsis semialata, to detect changes in gene expression associated with different photosynthetic phenotypes. Phylogenetically informed comparative transcriptomics show that intermediates with a weak C4 cycle are separated from the C3 phenotype by increases in the expression of 58 genes (0.22% of genes expressed in the leaves), including those encoding just three core C4 enzymes: aspartate aminotransferase, phosphoenolpyruvate carboxykinase, and phosphoenolpyruvate carboxylase. The subsequent transition to full C4 physiology was accompanied by increases in another 15 genes (0.06%), including only the core C4 enzyme pyruvate orthophosphate dikinase. These changes probably created a rudimentary C4 physiology, and isolated populations subsequently improved this emerging C4 physiology, resulting in a patchwork of expression for some C4 accessory genes. Our work shows how C4 assembly in A. semialata happened in incremental steps, each requiring few alterations over the previous step. These create short bridges across adaptive landscapes that probably facilitated the recurrent origins of C4 photosynthesis through a gradual process of evolution.
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spelling CGSpace1646992025-12-08T09:54:28Z Key changes in gene expression identified for different stages of C-4 evolution in Alloteropsis semialata Dunning, Luke T. Moreno-Villena, Jose J. Lundgren, Marjorie R. Dionora, Jacqueline Salazar, Paolo Adams, Claire Nyirenda, Florence Olofsson, Jill K. Mapaura, Anthony Grundy, Isla M. Kayombo, Canisius J. Dunning, Lucy A. Kentatchime, Fabrice Ariyarathne, Menaka Yakandawala, Deepthi Besnard, Guillaume Quick, W. Paul Bräutigam, Andrea Osborne, Colin P. Christin, Pascal-Antoine plant physiology plant science C4 photosynthesis is a complex trait that boosts productivity in tropical conditions. Compared with C3 species, the C4 state seems to require numerous novelties, but species comparisons can be confounded by long divergence times. Here, we exploit the photosynthetic diversity that exists within a single species, the grass Alloteropsis semialata, to detect changes in gene expression associated with different photosynthetic phenotypes. Phylogenetically informed comparative transcriptomics show that intermediates with a weak C4 cycle are separated from the C3 phenotype by increases in the expression of 58 genes (0.22% of genes expressed in the leaves), including those encoding just three core C4 enzymes: aspartate aminotransferase, phosphoenolpyruvate carboxykinase, and phosphoenolpyruvate carboxylase. The subsequent transition to full C4 physiology was accompanied by increases in another 15 genes (0.06%), including only the core C4 enzyme pyruvate orthophosphate dikinase. These changes probably created a rudimentary C4 physiology, and isolated populations subsequently improved this emerging C4 physiology, resulting in a patchwork of expression for some C4 accessory genes. Our work shows how C4 assembly in A. semialata happened in incremental steps, each requiring few alterations over the previous step. These create short bridges across adaptive landscapes that probably facilitated the recurrent origins of C4 photosynthesis through a gradual process of evolution. 2019-06-28 2024-12-19T12:54:12Z 2024-12-19T12:54:12Z Journal Article https://hdl.handle.net/10568/164699 en Open Access Oxford University Press Dunning, Luke T; Moreno-Villena, Jose J; Lundgren, Marjorie R; Dionora, Jacqueline; Salazar, Paolo; Adams, Claire; Nyirenda, Florence; Olofsson, Jill K; Mapaura, Anthony; Grundy, Isla M; Kayombo, Canisius J; Dunning, Lucy A; Kentatchime, Fabrice; Ariyarathne, Menaka; Yakandawala, Deepthi; Besnard, Guillaume; Quick, W Paul; Bräutigam, Andrea; Osborne, Colin P and Christin, Pascal-Antoine. 2019. Key changes in gene expression identified for different stages of C-4 evolution in Alloteropsis semialata. Journal of Experimental Botany, Volume 70 no. 12 p. 3255-3268
spellingShingle plant physiology
plant science
Dunning, Luke T.
Moreno-Villena, Jose J.
Lundgren, Marjorie R.
Dionora, Jacqueline
Salazar, Paolo
Adams, Claire
Nyirenda, Florence
Olofsson, Jill K.
Mapaura, Anthony
Grundy, Isla M.
Kayombo, Canisius J.
Dunning, Lucy A.
Kentatchime, Fabrice
Ariyarathne, Menaka
Yakandawala, Deepthi
Besnard, Guillaume
Quick, W. Paul
Bräutigam, Andrea
Osborne, Colin P.
Christin, Pascal-Antoine
Key changes in gene expression identified for different stages of C-4 evolution in Alloteropsis semialata
title Key changes in gene expression identified for different stages of C-4 evolution in Alloteropsis semialata
title_full Key changes in gene expression identified for different stages of C-4 evolution in Alloteropsis semialata
title_fullStr Key changes in gene expression identified for different stages of C-4 evolution in Alloteropsis semialata
title_full_unstemmed Key changes in gene expression identified for different stages of C-4 evolution in Alloteropsis semialata
title_short Key changes in gene expression identified for different stages of C-4 evolution in Alloteropsis semialata
title_sort key changes in gene expression identified for different stages of c 4 evolution in alloteropsis semialata
topic plant physiology
plant science
url https://hdl.handle.net/10568/164699
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