Ectopic Expression of CDF3 Genes in Tomato Enhances Biomass Production and Yield under Salinity Stress Conditions

Cycling Dof Factor (CDF) transcription factors (TFs) are involved in multiple processes related to plant growth and development. A member of this family, CDF3, has recently been linked in Arabidopsis to the regulation of primary metabolism and abiotic stress responses, but its role in crop productio...

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Main Authors: Begoña Renau-Morata, Rosa V. Molina, Laura Carrillo, Jaime Cebolla-Cornejo, Manuel Sánchez-Perales, Stephan Pollmann, José Domínguez-Figueroa, Alba R. Corrales, Jaume Flexas, Jesús Vicente-Carbajosa, Joaquín Medina, Sergio G. Nebauer
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-05-01
Series:Frontiers in Plant Science
Subjects:
CDF
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2017.00660/full
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spelling doaj-b8a214fec8d34fb091fac92edb119f982020-11-24T21:25:51ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2017-05-01810.3389/fpls.2017.00660239333Ectopic Expression of CDF3 Genes in Tomato Enhances Biomass Production and Yield under Salinity Stress ConditionsBegoña Renau-Morata0Rosa V. Molina1Laura Carrillo2Jaime Cebolla-Cornejo3Manuel Sánchez-Perales4Stephan Pollmann5José Domínguez-Figueroa6Alba R. Corrales7Jaume Flexas8Jesús Vicente-Carbajosa9Joaquín Medina10Sergio G. Nebauer11Área de Fisiología Vegetal, Universitat Politècnica de ValènciaValència, SpainÁrea de Fisiología Vegetal, Universitat Politècnica de ValènciaValència, SpainCentro de Biotecnología y Genómica de PlantasMadrid, SpainDepartamento de Biotecnología, Universitat Politècnica de ValènciaValència, SpainÁrea de Fisiología Vegetal, Universitat Politècnica de ValènciaValència, SpainCentro de Biotecnología y Genómica de PlantasMadrid, SpainCentro de Biotecnología y Genómica de PlantasMadrid, SpainCentro de Biotecnología y Genómica de PlantasMadrid, SpainDepartamento de Biología, Universitat de les Illes BalearsPalma, SpainCentro de Biotecnología y Genómica de PlantasMadrid, SpainCentro de Biotecnología y Genómica de PlantasMadrid, SpainÁrea de Fisiología Vegetal, Universitat Politècnica de ValènciaValència, SpainCycling Dof Factor (CDF) transcription factors (TFs) are involved in multiple processes related to plant growth and development. A member of this family, CDF3, has recently been linked in Arabidopsis to the regulation of primary metabolism and abiotic stress responses, but its role in crop production under stress is still unknown. In this study, we characterized tomato plants overexpressing the CDF3 genes from Arabidopsis and tomato and analyzed their effects on growth and yield under salinity, additionally gaining deeper insights into the molecular function of these TFs. Our results provide evidence for higher biomass production and yield in the 35S::AtCDF3 and 35S::SlCDF3 plants, likely due to a higher photosynthetic capacity resulting in increased sucrose availability. Transcriptome analysis revealed that CDF3 genes regulate a set of genes involved in redox homeostasis, photosynthesis performance and primary metabolism that lead to enhanced biomass production. Consistently, metabolomic profiling revealed that CDF3 evokes changes in the primary metabolism triggering enhanced nitrogen assimilation, and disclosed that the amount of some protective metabolites including sucrose, GABA and asparagine were higher in vegetative tissues of CDF3 overexpressing plants. Altogether these changes improved performance of 35S::AtCDF3 and 35S::SlCDF3 plants under salinity conditions. Moreover, the overexpression of CDF3 genes modified organic acid and sugar content in fruits, improving variables related to flavor perception and fruit quality. Overall, our results associate the CDF3 TF with a role in the control of growth and C/N metabolism, and highlight that overexpression of CDF3 genes can substantially improve plant yield.http://journal.frontiersin.org/article/10.3389/fpls.2017.00660/fullCDFtomatophotosynthesisabiotic stresscrop yieldC/N metabolism
collection DOAJ
language English
format Article
sources DOAJ
author Begoña Renau-Morata
Rosa V. Molina
Laura Carrillo
Jaime Cebolla-Cornejo
Manuel Sánchez-Perales
Stephan Pollmann
José Domínguez-Figueroa
Alba R. Corrales
Jaume Flexas
Jesús Vicente-Carbajosa
Joaquín Medina
Sergio G. Nebauer
spellingShingle Begoña Renau-Morata
Rosa V. Molina
Laura Carrillo
Jaime Cebolla-Cornejo
Manuel Sánchez-Perales
Stephan Pollmann
José Domínguez-Figueroa
Alba R. Corrales
Jaume Flexas
Jesús Vicente-Carbajosa
Joaquín Medina
Sergio G. Nebauer
Ectopic Expression of CDF3 Genes in Tomato Enhances Biomass Production and Yield under Salinity Stress Conditions
Frontiers in Plant Science
CDF
tomato
photosynthesis
abiotic stress
crop yield
C/N metabolism
author_facet Begoña Renau-Morata
Rosa V. Molina
Laura Carrillo
Jaime Cebolla-Cornejo
Manuel Sánchez-Perales
Stephan Pollmann
José Domínguez-Figueroa
Alba R. Corrales
Jaume Flexas
Jesús Vicente-Carbajosa
Joaquín Medina
Sergio G. Nebauer
author_sort Begoña Renau-Morata
title Ectopic Expression of CDF3 Genes in Tomato Enhances Biomass Production and Yield under Salinity Stress Conditions
title_short Ectopic Expression of CDF3 Genes in Tomato Enhances Biomass Production and Yield under Salinity Stress Conditions
title_full Ectopic Expression of CDF3 Genes in Tomato Enhances Biomass Production and Yield under Salinity Stress Conditions
title_fullStr Ectopic Expression of CDF3 Genes in Tomato Enhances Biomass Production and Yield under Salinity Stress Conditions
title_full_unstemmed Ectopic Expression of CDF3 Genes in Tomato Enhances Biomass Production and Yield under Salinity Stress Conditions
title_sort ectopic expression of cdf3 genes in tomato enhances biomass production and yield under salinity stress conditions
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2017-05-01
description Cycling Dof Factor (CDF) transcription factors (TFs) are involved in multiple processes related to plant growth and development. A member of this family, CDF3, has recently been linked in Arabidopsis to the regulation of primary metabolism and abiotic stress responses, but its role in crop production under stress is still unknown. In this study, we characterized tomato plants overexpressing the CDF3 genes from Arabidopsis and tomato and analyzed their effects on growth and yield under salinity, additionally gaining deeper insights into the molecular function of these TFs. Our results provide evidence for higher biomass production and yield in the 35S::AtCDF3 and 35S::SlCDF3 plants, likely due to a higher photosynthetic capacity resulting in increased sucrose availability. Transcriptome analysis revealed that CDF3 genes regulate a set of genes involved in redox homeostasis, photosynthesis performance and primary metabolism that lead to enhanced biomass production. Consistently, metabolomic profiling revealed that CDF3 evokes changes in the primary metabolism triggering enhanced nitrogen assimilation, and disclosed that the amount of some protective metabolites including sucrose, GABA and asparagine were higher in vegetative tissues of CDF3 overexpressing plants. Altogether these changes improved performance of 35S::AtCDF3 and 35S::SlCDF3 plants under salinity conditions. Moreover, the overexpression of CDF3 genes modified organic acid and sugar content in fruits, improving variables related to flavor perception and fruit quality. Overall, our results associate the CDF3 TF with a role in the control of growth and C/N metabolism, and highlight that overexpression of CDF3 genes can substantially improve plant yield.
topic CDF
tomato
photosynthesis
abiotic stress
crop yield
C/N metabolism
url http://journal.frontiersin.org/article/10.3389/fpls.2017.00660/full
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