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Alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment

BACKGROUND: Alternative splicing (AS) produces transcript variants playing potential roles in proteome diversification and gene expression regulation. AS modulation is thus essential to respond to developmental and environmental stimuli. In grapevine, a better understanding of berry development is c...

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Autores principales: Maillot, Pascale, Velt, Amandine, Rustenholz, Camille, Butterlin, Gisèle, Merdinoglu, Didier, Duchêne, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8543832/
https://www.ncbi.nlm.nih.gov/pubmed/34696712
http://dx.doi.org/10.1186/s12870-021-03266-1
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author Maillot, Pascale
Velt, Amandine
Rustenholz, Camille
Butterlin, Gisèle
Merdinoglu, Didier
Duchêne, Eric
author_facet Maillot, Pascale
Velt, Amandine
Rustenholz, Camille
Butterlin, Gisèle
Merdinoglu, Didier
Duchêne, Eric
author_sort Maillot, Pascale
collection PubMed
description BACKGROUND: Alternative splicing (AS) produces transcript variants playing potential roles in proteome diversification and gene expression regulation. AS modulation is thus essential to respond to developmental and environmental stimuli. In grapevine, a better understanding of berry development is crucial for implementing breeding and viticultural strategies allowing adaptation to climate changes. Although profound changes in gene transcription have been shown to occur in the course of berry ripening, no detailed study on splicing modifications during this period has been published so far. We report here on the regulation of gene AS in developing berries of two grapevine (Vitis vinifera L.) varieties, Gewurztraminer (Gw) and Riesling (Ri), showing distinctive phenotypic characteristics. Using the software rMATS, the transcriptomes of berries at four developmental steps, from the green stage to mid-ripening, were analysed in pairwise comparisons between stages and varieties. RESULTS: A total of 305 differential AS (DAS) events, affecting 258 genes, were identified. Interestingly, 22% of these AS events had not been reported before. Among the 80 genes that underwent the most significant variations during ripening, 22 showed a similar splicing profile in Gw and Ri, which suggests their involvement in berry development. Conversely, 23 genes were subjected to splicing regulation in only one variety. In addition, the ratios of alternative isoforms were different in Gw and Ri for 35 other genes, without any change during ripening. This last result indicates substantial AS differences between the two varieties. Remarkably, 8 AS events were specific to one variety, due to the lack of a splice site in the other variety. Furthermore, the transcription rates of the genes affected by stage-dependent splicing regulation were mostly unchanged, identifying AS modulation as an independent way of shaping the transcriptome. CONCLUSIONS: The analysis of AS profiles in grapevine varieties with contrasting phenotypes revealed some similarity in the regulation of several genes with developmental functions, suggesting their involvement in berry ripening. Additionally, many splicing differences were discovered between the two varieties, that could be linked to phenotypic specificities and distinct adaptive capacities. Together, these findings open perspectives for a better understanding of berry development and for the selection of grapevine genotypes adapted to climate change. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03266-1.
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spelling pubmed-85438322021-10-25 Alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment Maillot, Pascale Velt, Amandine Rustenholz, Camille Butterlin, Gisèle Merdinoglu, Didier Duchêne, Eric BMC Plant Biol Research BACKGROUND: Alternative splicing (AS) produces transcript variants playing potential roles in proteome diversification and gene expression regulation. AS modulation is thus essential to respond to developmental and environmental stimuli. In grapevine, a better understanding of berry development is crucial for implementing breeding and viticultural strategies allowing adaptation to climate changes. Although profound changes in gene transcription have been shown to occur in the course of berry ripening, no detailed study on splicing modifications during this period has been published so far. We report here on the regulation of gene AS in developing berries of two grapevine (Vitis vinifera L.) varieties, Gewurztraminer (Gw) and Riesling (Ri), showing distinctive phenotypic characteristics. Using the software rMATS, the transcriptomes of berries at four developmental steps, from the green stage to mid-ripening, were analysed in pairwise comparisons between stages and varieties. RESULTS: A total of 305 differential AS (DAS) events, affecting 258 genes, were identified. Interestingly, 22% of these AS events had not been reported before. Among the 80 genes that underwent the most significant variations during ripening, 22 showed a similar splicing profile in Gw and Ri, which suggests their involvement in berry development. Conversely, 23 genes were subjected to splicing regulation in only one variety. In addition, the ratios of alternative isoforms were different in Gw and Ri for 35 other genes, without any change during ripening. This last result indicates substantial AS differences between the two varieties. Remarkably, 8 AS events were specific to one variety, due to the lack of a splice site in the other variety. Furthermore, the transcription rates of the genes affected by stage-dependent splicing regulation were mostly unchanged, identifying AS modulation as an independent way of shaping the transcriptome. CONCLUSIONS: The analysis of AS profiles in grapevine varieties with contrasting phenotypes revealed some similarity in the regulation of several genes with developmental functions, suggesting their involvement in berry ripening. Additionally, many splicing differences were discovered between the two varieties, that could be linked to phenotypic specificities and distinct adaptive capacities. Together, these findings open perspectives for a better understanding of berry development and for the selection of grapevine genotypes adapted to climate change. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03266-1. BioMed Central 2021-10-25 /pmc/articles/PMC8543832/ /pubmed/34696712 http://dx.doi.org/10.1186/s12870-021-03266-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Maillot, Pascale
Velt, Amandine
Rustenholz, Camille
Butterlin, Gisèle
Merdinoglu, Didier
Duchêne, Eric
Alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment
title Alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment
title_full Alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment
title_fullStr Alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment
title_full_unstemmed Alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment
title_short Alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment
title_sort alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8543832/
https://www.ncbi.nlm.nih.gov/pubmed/34696712
http://dx.doi.org/10.1186/s12870-021-03266-1
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