Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability
To identify key traits brought about by citrus domestication, we have analyzed the transcriptomes of the pulp of developing fruitlets of inedible wild Ichang papeda (Citrus ichangensis), acidic Sun Chu Sha Kat mandarin (C. reticulata) and three palatable segregants of a cross between commercial Clem...
| Autores principales: | , , , |
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| Formato: | Artículo |
| Lenguaje: | Inglés |
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Frontiers Media
2023
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| Acceso en línea: | https://hdl.handle.net/20.500.11939/8617 https://www.frontiersin.org/articles/10.3389/fpls.2022.982683/full |
| _version_ | 1855492525035356160 |
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| author | Pérez-Román, Estela Borredá, Carles Tadeo, Francisco R. Talón, Manuel |
| author_browse | Borredá, Carles Pérez-Román, Estela Tadeo, Francisco R. Talón, Manuel |
| author_facet | Pérez-Román, Estela Borredá, Carles Tadeo, Francisco R. Talón, Manuel |
| author_sort | Pérez-Román, Estela |
| collection | ReDivia |
| description | To identify key traits brought about by citrus domestication, we have analyzed the transcriptomes of the pulp of developing fruitlets of inedible wild Ichang papeda (Citrus ichangensis), acidic Sun Chu Sha Kat mandarin (C. reticulata) and three palatable segregants of a cross between commercial Clementine (C. x clementina) and W. Murcott (C. x reticulata) mandarins, two pummelo/mandarin admixtures of worldwide distribution. RNA-seq comparison between the wild citrus and the ancestral sour mandarin identified 7267 differentially expressed genes, out of which 2342 were mapped to 117 KEGG pathways. From the remaining genes, a set of 2832 genes was functionally annotated and grouped into 45 user-defined categories. The data suggest that domestication promoted fundamental growth processes to the detriment of the production of chemical defenses, namely, alkaloids, terpenoids, phenylpropanoids, flavonoids, glucosinolates and cyanogenic glucosides. In the papeda, the generation of energy to support a more active secondary metabolism appears to be dependent upon upregulation of glycolysis, fatty acid degradation, Calvin cycle, oxidative phosphorylation, and ATP-citrate lyase and GABA pathways. In the acidic mandarin, downregulation of cytosolic citrate degradation was concomitant with vacuolar citrate accumulation. These changes affected nitrogen and carbon allocation in both species leading to major differences in organoleptic properties since the reduction of unpleasant secondary metabolites increases palatability while acidity reduces acceptability. The comparison between the segregants and the acidic mandarin identified 357 transcripts characterized by the occurrence in the three segregants of additional downregulation of secondary metabolites and basic structural cell wall components. The segregants also showed upregulation of genes involved in the synthesis of methyl anthranilate and furaneol, key substances of pleasant fruity aroma and flavor, and of sugar transporters relevant for sugar accumulation. Transcriptome and qPCR analysis in developing and ripe fruit of a set of genes previously associated with citric acid accumulation, demonstrated that lower acidity is linked to downregulation of these regulatory genes in the segregants. The results suggest that the transition of inedible papeda to sour mandarin implicated drastic gene expression reprograming of pivotal pathways of the primary and secondary metabolism, while palatable mandarins evolved through progressive refining of palatability properties, especially acidity. |
| format | Artículo |
| id | ReDivia8617 |
| institution | Instituto Valenciano de Investigaciones Agrarias (IVIA) |
| language | Inglés |
| publishDate | 2023 |
| publishDateRange | 2023 |
| publishDateSort | 2023 |
| publisher | Frontiers Media |
| publisherStr | Frontiers Media |
| record_format | dspace |
| spelling | ReDivia86172025-04-25T14:49:10Z Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability Pérez-Román, Estela Borredá, Carles Tadeo, Francisco R. Talón, Manuel Edible mandarins Fruit acidity Genetic admixture Secondary metabolism Wild citrus Transcriptome analysis F30 Plant genetics and breeding F60 Plant physiology and biochemistry F62 Plant physiology - Growth and development Q01 Food science and technology S01 Human nutrition - General aspects U30 Research methods Citrus Fruit pulps Plant growth stimulants Palatability Plant domestication RNA sequence Plant defense reactions Aroma (organoleptic property) To identify key traits brought about by citrus domestication, we have analyzed the transcriptomes of the pulp of developing fruitlets of inedible wild Ichang papeda (Citrus ichangensis), acidic Sun Chu Sha Kat mandarin (C. reticulata) and three palatable segregants of a cross between commercial Clementine (C. x clementina) and W. Murcott (C. x reticulata) mandarins, two pummelo/mandarin admixtures of worldwide distribution. RNA-seq comparison between the wild citrus and the ancestral sour mandarin identified 7267 differentially expressed genes, out of which 2342 were mapped to 117 KEGG pathways. From the remaining genes, a set of 2832 genes was functionally annotated and grouped into 45 user-defined categories. The data suggest that domestication promoted fundamental growth processes to the detriment of the production of chemical defenses, namely, alkaloids, terpenoids, phenylpropanoids, flavonoids, glucosinolates and cyanogenic glucosides. In the papeda, the generation of energy to support a more active secondary metabolism appears to be dependent upon upregulation of glycolysis, fatty acid degradation, Calvin cycle, oxidative phosphorylation, and ATP-citrate lyase and GABA pathways. In the acidic mandarin, downregulation of cytosolic citrate degradation was concomitant with vacuolar citrate accumulation. These changes affected nitrogen and carbon allocation in both species leading to major differences in organoleptic properties since the reduction of unpleasant secondary metabolites increases palatability while acidity reduces acceptability. The comparison between the segregants and the acidic mandarin identified 357 transcripts characterized by the occurrence in the three segregants of additional downregulation of secondary metabolites and basic structural cell wall components. The segregants also showed upregulation of genes involved in the synthesis of methyl anthranilate and furaneol, key substances of pleasant fruity aroma and flavor, and of sugar transporters relevant for sugar accumulation. Transcriptome and qPCR analysis in developing and ripe fruit of a set of genes previously associated with citric acid accumulation, demonstrated that lower acidity is linked to downregulation of these regulatory genes in the segregants. The results suggest that the transition of inedible papeda to sour mandarin implicated drastic gene expression reprograming of pivotal pathways of the primary and secondary metabolism, while palatable mandarins evolved through progressive refining of palatability properties, especially acidity. 2023-05-23T09:54:49Z 2023-05-23T09:54:49Z 2022 article publishedVersion Peréz-Román, E., Borredá, C., Tadeo, F. R. & Talon, M. (2022). Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability. Frontiers in Plant Science, 13, 982683. 1664-462X https://hdl.handle.net/20.500.11939/8617 10.3389/fpls.2022.982683 https://www.frontiersin.org/articles/10.3389/fpls.2022.982683/full en This research was co-funded by the Ministerio de Ciencia, Innovación y Universidades (Spain) through grant #RTI2018-097790-R-100 and by the European Union through the European Regional Development Fund (ERDF) of the Generalitat Valenciana 2014–2020, through grants #PROMETEO/2020/027 and #IVIA/52201A. info:eu-repo/grantAgreement/MICINN//RTI2018-097790-R-100 info:eu-repo/grantAgreement/CEGVA/Prometeo 2020/027 info:eu-repo/grantAgreement/ERDF/PCV 2021-2027/52201/ES/Relanzando la agroalimentación valenciana para una producción y consumo sostenibles y seguros/AgroAlimVal Attribution-NonCommercial-NoDerivatives 4.0 Internacional http://creativecommons.org/licenses/by-nc-nd/4.0/ openAccess Frontiers Media electronico |
| spellingShingle | Edible mandarins Fruit acidity Genetic admixture Secondary metabolism Wild citrus Transcriptome analysis F30 Plant genetics and breeding F60 Plant physiology and biochemistry F62 Plant physiology - Growth and development Q01 Food science and technology S01 Human nutrition - General aspects U30 Research methods Citrus Fruit pulps Plant growth stimulants Palatability Plant domestication RNA sequence Plant defense reactions Aroma (organoleptic property) Pérez-Román, Estela Borredá, Carles Tadeo, Francisco R. Talón, Manuel Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability |
| title | Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability |
| title_full | Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability |
| title_fullStr | Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability |
| title_full_unstemmed | Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability |
| title_short | Transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability |
| title_sort | transcriptome analysis of the pulp of citrus fruitlets suggests that domestication enhanced growth processes and reduced chemical defenses increasing palatability |
| topic | Edible mandarins Fruit acidity Genetic admixture Secondary metabolism Wild citrus Transcriptome analysis F30 Plant genetics and breeding F60 Plant physiology and biochemistry F62 Plant physiology - Growth and development Q01 Food science and technology S01 Human nutrition - General aspects U30 Research methods Citrus Fruit pulps Plant growth stimulants Palatability Plant domestication RNA sequence Plant defense reactions Aroma (organoleptic property) |
| url | https://hdl.handle.net/20.500.11939/8617 https://www.frontiersin.org/articles/10.3389/fpls.2022.982683/full |
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