The common transcriptional subnetworks of the grape berry skin in the late stages of ripening
Abstract Background Wine grapes are important economically in many countries around the world. Defining the optimum time for grape harvest is a major challenge to the grower and winemaker. Berry skins are an important source of flavor, color and other quality traits in the ripening stage. Senescent-...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2017-05-01
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| Series: | BMC Plant Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s12870-017-1043-1 |
| _version_ | 1818034577687445504 |
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| author | Ryan Ghan Juli Petereit Richard L. Tillett Karen A. Schlauch David Toubiana Aaron Fait Grant R. Cramer |
| author_facet | Ryan Ghan Juli Petereit Richard L. Tillett Karen A. Schlauch David Toubiana Aaron Fait Grant R. Cramer |
| author_sort | Ryan Ghan |
| collection | DOAJ |
| description | Abstract Background Wine grapes are important economically in many countries around the world. Defining the optimum time for grape harvest is a major challenge to the grower and winemaker. Berry skins are an important source of flavor, color and other quality traits in the ripening stage. Senescent-like processes such as chloroplast disorganization and cell death characterize the late ripening stage. Results To better understand the molecular and physiological processes involved in the late stages of berry ripening, RNA-seq analysis of the skins of seven wine grape cultivars (Cabernet Franc, Cabernet Sauvignon, Merlot, Pinot Noir, Chardonnay, Sauvignon Blanc and Semillon) was performed. RNA-seq analysis identified approximately 2000 common differentially expressed genes for all seven cultivars across four different berry sugar levels (20 to 26 °Brix). Network analyses, both a posteriori (standard) and a priori (gene co-expression network analysis), were used to elucidate transcriptional subnetworks and hub genes associated with traits in the berry skins of the late stages of berry ripening. These independent approaches revealed genes involved in photosynthesis, catabolism, and nucleotide metabolism. The transcript abundance of most photosynthetic genes declined with increasing sugar levels in the berries. The transcript abundance of other processes increased such as nucleic acid metabolism, chromosome organization and lipid catabolism. Weighted gene co-expression network analysis (WGCNA) identified 64 gene modules that were organized into 12 subnetworks of three modules or more and six higher order gene subnetworks. Some gene subnetworks were highly correlated with sugar levels and some subnetworks were highly enriched in the chloroplast and nucleus. The petal R package was utilized independently to construct a true small-world and scale-free complex gene co-expression network model. A subnetwork of 216 genes with the highest connectivity was elucidated, consistent with the module results from WGCNA. Hub genes in these subnetworks were identified including numerous members of the core circadian clock, RNA splicing, proteolysis and chromosome organization. An integrated model was constructed linking light sensing with alternative splicing, chromosome remodeling and the circadian clock. Conclusions A common set of differentially expressed genes and gene subnetworks from seven different cultivars were examined in the skin of the late stages of grapevine berry ripening. A densely connected gene subnetwork was elucidated involving a complex interaction of berry senescent processes (autophagy), catabolism, the circadian clock, RNA splicing, proteolysis and epigenetic regulation. Hypotheses were induced from these data sets involving sugar accumulation, light, autophagy, epigenetic regulation, and fruit development. This work provides a better understanding of berry development and the transcriptional processes involved in the late stages of ripening. |
| first_indexed | 2024-12-10T06:41:23Z |
| format | Article |
| id | doaj.art-715a1423763647ba9efd5a1c31b2c61a |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-12-10T06:41:23Z |
| publishDate | 2017-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-715a1423763647ba9efd5a1c31b2c61a2022-12-22T01:58:47ZengBMCBMC Plant Biology1471-22292017-05-0117112110.1186/s12870-017-1043-1The common transcriptional subnetworks of the grape berry skin in the late stages of ripeningRyan Ghan0Juli Petereit1Richard L. Tillett2Karen A. Schlauch3David Toubiana4Aaron Fait5Grant R. Cramer6Department of Biochemistry and Molecular Biology, University of NevadaNevada INBRE Bioinformatics Core, University of NevadaNevada INBRE Bioinformatics Core, University of NevadaDepartment of Biochemistry and Molecular Biology, University of NevadaTelekom Innovation, Laboratories and Cyber Security Research Center, Department of Information, Systems Engineering, Ben Gurion UniversityBen-Gurion University of the Negev, Jacob Blaustein Institutes for Desert ResearchDepartment of Biochemistry and Molecular Biology, University of NevadaAbstract Background Wine grapes are important economically in many countries around the world. Defining the optimum time for grape harvest is a major challenge to the grower and winemaker. Berry skins are an important source of flavor, color and other quality traits in the ripening stage. Senescent-like processes such as chloroplast disorganization and cell death characterize the late ripening stage. Results To better understand the molecular and physiological processes involved in the late stages of berry ripening, RNA-seq analysis of the skins of seven wine grape cultivars (Cabernet Franc, Cabernet Sauvignon, Merlot, Pinot Noir, Chardonnay, Sauvignon Blanc and Semillon) was performed. RNA-seq analysis identified approximately 2000 common differentially expressed genes for all seven cultivars across four different berry sugar levels (20 to 26 °Brix). Network analyses, both a posteriori (standard) and a priori (gene co-expression network analysis), were used to elucidate transcriptional subnetworks and hub genes associated with traits in the berry skins of the late stages of berry ripening. These independent approaches revealed genes involved in photosynthesis, catabolism, and nucleotide metabolism. The transcript abundance of most photosynthetic genes declined with increasing sugar levels in the berries. The transcript abundance of other processes increased such as nucleic acid metabolism, chromosome organization and lipid catabolism. Weighted gene co-expression network analysis (WGCNA) identified 64 gene modules that were organized into 12 subnetworks of three modules or more and six higher order gene subnetworks. Some gene subnetworks were highly correlated with sugar levels and some subnetworks were highly enriched in the chloroplast and nucleus. The petal R package was utilized independently to construct a true small-world and scale-free complex gene co-expression network model. A subnetwork of 216 genes with the highest connectivity was elucidated, consistent with the module results from WGCNA. Hub genes in these subnetworks were identified including numerous members of the core circadian clock, RNA splicing, proteolysis and chromosome organization. An integrated model was constructed linking light sensing with alternative splicing, chromosome remodeling and the circadian clock. Conclusions A common set of differentially expressed genes and gene subnetworks from seven different cultivars were examined in the skin of the late stages of grapevine berry ripening. A densely connected gene subnetwork was elucidated involving a complex interaction of berry senescent processes (autophagy), catabolism, the circadian clock, RNA splicing, proteolysis and epigenetic regulation. Hypotheses were induced from these data sets involving sugar accumulation, light, autophagy, epigenetic regulation, and fruit development. This work provides a better understanding of berry development and the transcriptional processes involved in the late stages of ripening.http://link.springer.com/article/10.1186/s12870-017-1043-1Circadian clockChromosome organizationEpigenetic modificationFruit developmentGrape berryNetwork analysis |
| spellingShingle | Ryan Ghan Juli Petereit Richard L. Tillett Karen A. Schlauch David Toubiana Aaron Fait Grant R. Cramer The common transcriptional subnetworks of the grape berry skin in the late stages of ripening BMC Plant Biology Circadian clock Chromosome organization Epigenetic modification Fruit development Grape berry Network analysis |
| title | The common transcriptional subnetworks of the grape berry skin in the late stages of ripening |
| title_full | The common transcriptional subnetworks of the grape berry skin in the late stages of ripening |
| title_fullStr | The common transcriptional subnetworks of the grape berry skin in the late stages of ripening |
| title_full_unstemmed | The common transcriptional subnetworks of the grape berry skin in the late stages of ripening |
| title_short | The common transcriptional subnetworks of the grape berry skin in the late stages of ripening |
| title_sort | common transcriptional subnetworks of the grape berry skin in the late stages of ripening |
| topic | Circadian clock Chromosome organization Epigenetic modification Fruit development Grape berry Network analysis |
| url | http://link.springer.com/article/10.1186/s12870-017-1043-1 |
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