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The common transcriptional subnetworks of the grape berry skin in the late stages of ripening

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 pro...

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Autores principales: Ghan, Ryan, Petereit, Juli, Tillett, Richard L., Schlauch, Karen A., Toubiana, David, Fait, Aaron, Cramer, Grant R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5450095/
https://www.ncbi.nlm.nih.gov/pubmed/28558655
http://dx.doi.org/10.1186/s12870-017-1043-1
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author Ghan, Ryan
Petereit, Juli
Tillett, Richard L.
Schlauch, Karen A.
Toubiana, David
Fait, Aaron
Cramer, Grant R.
author_facet Ghan, Ryan
Petereit, Juli
Tillett, Richard L.
Schlauch, Karen A.
Toubiana, David
Fait, Aaron
Cramer, Grant R.
author_sort Ghan, Ryan
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-017-1043-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-54500952017-06-01 The common transcriptional subnetworks of the grape berry skin in the late stages of ripening Ghan, Ryan Petereit, Juli Tillett, Richard L. Schlauch, Karen A. Toubiana, David Fait, Aaron Cramer, Grant R. BMC Plant Biol Research Article 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-017-1043-1) contains supplementary material, which is available to authorized users. BioMed Central 2017-05-30 /pmc/articles/PMC5450095/ /pubmed/28558655 http://dx.doi.org/10.1186/s12870-017-1043-1 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Ghan, Ryan
Petereit, Juli
Tillett, Richard L.
Schlauch, Karen A.
Toubiana, David
Fait, Aaron
Cramer, Grant R.
The common transcriptional subnetworks of the grape berry skin in the late stages of ripening
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 Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5450095/
https://www.ncbi.nlm.nih.gov/pubmed/28558655
http://dx.doi.org/10.1186/s12870-017-1043-1
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