Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression

Background: Interspecific hybridizations and admixtures were key in Citrus domestication, but very little is known about their impact at the transcriptomic level. To determine the effects of genome introgressions on gene expression, the transcriptomes of the pulp and flavedo of three pure species (c...

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Autores principales: Borredá, Carles, Pérez-Román, Estela, Talón, Manuel, Terol, Javier
Formato: article
Lenguaje:Inglés
Publicado: Springer Nature 2022
Materias:
Acceso en línea:http://hdl.handle.net/20.500.11939/8049
https://doi.org/10.1186/s12870-022-03509-9
https://link.springer.com/article/10.1186/s12870-022-03509-9
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author Borredá, Carles
Pérez-Román, Estela
Talón, Manuel
Terol, Javier
author_browse Borredá, Carles
Pérez-Román, Estela
Talón, Manuel
Terol, Javier
author_facet Borredá, Carles
Pérez-Román, Estela
Talón, Manuel
Terol, Javier
author_sort Borredá, Carles
collection ReDivia
description Background: Interspecific hybridizations and admixtures were key in Citrus domestication, but very little is known about their impact at the transcriptomic level. To determine the effects of genome introgressions on gene expression, the transcriptomes of the pulp and flavedo of three pure species (citron, pure mandarin and pummelo) and four derived domesticated genetic admixtures (sour orange, sweet orange, lemon and domesticated mandarin) have been analyzed at color break. Results: Many genes involved in relevant physiological processes for domestication, such sugar/acid metabolism and carotenoid/flavonoid synthesis, were differentially expressed among samples. In the low-sugar, highly acidic species lemon and citron, many genes involved in sugar metabolism, the TCA cycle and GABA shunt displayed a reduced expression, while the P-type ATPase CitPH5 and most subunits of the vacuolar ATPase were overexpressed. The redcolored species and admixtures were generally characterized by the overexpression in the flavedo of specific pivotal genes involved in the carotenoid biosynthesis, including phytoene synthase, ζ-carotene desaturase, β-lycopene cyclase and CCD4b, a carotenoid cleavage dioxygenase. The expression patterns of many genes involved in flavonoid modifications, especially the flavonoid and phenylpropanoid O-methyltransferases showed extreme diversity. However, the most noticeable differential expression was shown by a chalcone synthase gene, which catalyzes a key step in the biosynthesis of flavonoids. This chalcone synthase was exclusively expressed in mandarins and their admixed species, which only expressed the mandarin allele. In addition, comparisons between wild and domesticated mandarins revealed that the major differences between their transcriptomes concentrate in the admixed regions. Conclusion: In this work we present a first study providing broad evidence that the genome introgressions that took place during citrus domestication largely shaped gene expression in their fruits.
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spelling ReDivia80492025-04-25T14:48:39Z Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression Borredá, Carles Pérez-Román, Estela Talón, Manuel Terol, Javier Allele specific expression Fruit ripening F30 Plant genetics and breeding U30 Research methods A50 Agricultural research Citrus Domestication RNA sequence Background: Interspecific hybridizations and admixtures were key in Citrus domestication, but very little is known about their impact at the transcriptomic level. To determine the effects of genome introgressions on gene expression, the transcriptomes of the pulp and flavedo of three pure species (citron, pure mandarin and pummelo) and four derived domesticated genetic admixtures (sour orange, sweet orange, lemon and domesticated mandarin) have been analyzed at color break. Results: Many genes involved in relevant physiological processes for domestication, such sugar/acid metabolism and carotenoid/flavonoid synthesis, were differentially expressed among samples. In the low-sugar, highly acidic species lemon and citron, many genes involved in sugar metabolism, the TCA cycle and GABA shunt displayed a reduced expression, while the P-type ATPase CitPH5 and most subunits of the vacuolar ATPase were overexpressed. The redcolored species and admixtures were generally characterized by the overexpression in the flavedo of specific pivotal genes involved in the carotenoid biosynthesis, including phytoene synthase, ζ-carotene desaturase, β-lycopene cyclase and CCD4b, a carotenoid cleavage dioxygenase. The expression patterns of many genes involved in flavonoid modifications, especially the flavonoid and phenylpropanoid O-methyltransferases showed extreme diversity. However, the most noticeable differential expression was shown by a chalcone synthase gene, which catalyzes a key step in the biosynthesis of flavonoids. This chalcone synthase was exclusively expressed in mandarins and their admixed species, which only expressed the mandarin allele. In addition, comparisons between wild and domesticated mandarins revealed that the major differences between their transcriptomes concentrate in the admixed regions. Conclusion: In this work we present a first study providing broad evidence that the genome introgressions that took place during citrus domestication largely shaped gene expression in their fruits. 2022-04-28T07:49:23Z 2022-04-28T07:49:23Z 2022 article publishedVersion Borredá, C., Pérez-Román, E., Talón, M. & Terol, J. (2022). Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression. BMC plant biology, 22(1), 123. 1471-2229 http://hdl.handle.net/20.500.11939/8049 https://doi.org/10.1186/s12870-022-03509-9 https://link.springer.com/article/10.1186/s12870-022-03509-9 en Info:eu-repo/grantAgreement/MINECO/Programa Estatal de I+D+I Orientada a los Retos de la Sociedad/RTI2018-097790-R-100 Financial support was provided by the Ministerio de Ciencia, Innovación y Universidades (Spain) trough grant # RTI2018–097790-R-100 and #PROMETEO/ 2020/027. Funds were used for the design of the study and collection, analysis, and interpretation of data and in writing the manuscript, as well as in the open access payment. Atribución-NoComercial-SinDerivadas 3.0 España http://creativecommons.org/licenses/by-nc-nd/3.0/es/ openAccess Springer Nature electronico
spellingShingle Allele specific expression
Fruit ripening
F30 Plant genetics and breeding
U30 Research methods
A50 Agricultural research
Citrus
Domestication
RNA sequence
Borredá, Carles
Pérez-Román, Estela
Talón, Manuel
Terol, Javier
Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression
title Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression
title_full Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression
title_fullStr Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression
title_full_unstemmed Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression
title_short Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression
title_sort comparative transcriptomics of wild and commercial citrus during early ripening reveals how domestication shaped fruit gene expression
topic Allele specific expression
Fruit ripening
F30 Plant genetics and breeding
U30 Research methods
A50 Agricultural research
Citrus
Domestication
RNA sequence
url http://hdl.handle.net/20.500.11939/8049
https://doi.org/10.1186/s12870-022-03509-9
https://link.springer.com/article/10.1186/s12870-022-03509-9
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AT talonmanuel comparativetranscriptomicsofwildandcommercialcitrusduringearlyripeningrevealshowdomesticationshapedfruitgeneexpression
AT teroljavier comparativetranscriptomicsofwildandcommercialcitrusduringearlyripeningrevealshowdomesticationshapedfruitgeneexpression