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Structure and transcriptional regulation of the major intrinsic protein gene family in grapevine

BACKGROUND: The major intrinsic protein (MIP) family is a family of proteins, including aquaporins, which facilitate water and small molecule transport across plasma membranes. In plants, MIPs function in a huge variety of processes including water transport, growth, stress response, and fruit devel...

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Autores principales: Wong, Darren Chern Jan, Zhang, Li, Merlin, Isabelle, Castellarin, Simone D., Gambetta, Gregory A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5896048/
https://www.ncbi.nlm.nih.gov/pubmed/29642857
http://dx.doi.org/10.1186/s12864-018-4638-5
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author Wong, Darren Chern Jan
Zhang, Li
Merlin, Isabelle
Castellarin, Simone D.
Gambetta, Gregory A.
author_facet Wong, Darren Chern Jan
Zhang, Li
Merlin, Isabelle
Castellarin, Simone D.
Gambetta, Gregory A.
author_sort Wong, Darren Chern Jan
collection PubMed
description BACKGROUND: The major intrinsic protein (MIP) family is a family of proteins, including aquaporins, which facilitate water and small molecule transport across plasma membranes. In plants, MIPs function in a huge variety of processes including water transport, growth, stress response, and fruit development. In this study, we characterize the structure and transcriptional regulation of the MIP family in grapevine, describing the putative genome duplication events leading to the family structure and characterizing the family’s tissue and developmental specific expression patterns across numerous preexisting microarray and RNAseq datasets. Gene co-expression network (GCN) analyses were carried out across these datasets and the promoters of each family member were analyzed for cis-regulatory element structure in order to provide insight into their transcriptional regulation. RESULTS: A total of 29 Vitis vinifera MIP family members (excluding putative pseudogenes) were identified of which all but two were mapped onto Vitis vinifera chromosomes. In this study, segmental duplication events were identified for five plasma membrane intrinsic protein (PIP) and four tonoplast intrinsic protein (TIP) genes, contributing to the expansion of PIPs and TIPs in grapevine. Grapevine MIP family members have distinct tissue and developmental expression patterns and hierarchical clustering revealed two primary groups regardless of the datasets analyzed. Composite microarray and RNA-seq gene co-expression networks (GCNs) highlighted the relationships between MIP genes and functional categories involved in cell wall modification and transport, as well as with other MIPs revealing a strong co-regulation within the family itself. Some duplicated MIP family members have undergone sub-functionalization and exhibit distinct expression patterns and GCNs. Cis-regulatory element (CRE) analyses of the MIP promoters and their associated GCN members revealed enrichment for numerous CREs including AP2/ERFs and NACs. CONCLUSIONS: Combining phylogenetic analyses, gene expression profiling, gene co-expression network analyses, and cis-regulatory element enrichment, this study provides a comprehensive overview of the structure and transcriptional regulation of the grapevine MIP family. The study highlights the duplication and sub-functionalization of the family, its strong coordinated expression with genes involved in growth and transport, and the putative classes of TFs responsible for its regulation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4638-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-58960482018-04-12 Structure and transcriptional regulation of the major intrinsic protein gene family in grapevine Wong, Darren Chern Jan Zhang, Li Merlin, Isabelle Castellarin, Simone D. Gambetta, Gregory A. BMC Genomics Research Article BACKGROUND: The major intrinsic protein (MIP) family is a family of proteins, including aquaporins, which facilitate water and small molecule transport across plasma membranes. In plants, MIPs function in a huge variety of processes including water transport, growth, stress response, and fruit development. In this study, we characterize the structure and transcriptional regulation of the MIP family in grapevine, describing the putative genome duplication events leading to the family structure and characterizing the family’s tissue and developmental specific expression patterns across numerous preexisting microarray and RNAseq datasets. Gene co-expression network (GCN) analyses were carried out across these datasets and the promoters of each family member were analyzed for cis-regulatory element structure in order to provide insight into their transcriptional regulation. RESULTS: A total of 29 Vitis vinifera MIP family members (excluding putative pseudogenes) were identified of which all but two were mapped onto Vitis vinifera chromosomes. In this study, segmental duplication events were identified for five plasma membrane intrinsic protein (PIP) and four tonoplast intrinsic protein (TIP) genes, contributing to the expansion of PIPs and TIPs in grapevine. Grapevine MIP family members have distinct tissue and developmental expression patterns and hierarchical clustering revealed two primary groups regardless of the datasets analyzed. Composite microarray and RNA-seq gene co-expression networks (GCNs) highlighted the relationships between MIP genes and functional categories involved in cell wall modification and transport, as well as with other MIPs revealing a strong co-regulation within the family itself. Some duplicated MIP family members have undergone sub-functionalization and exhibit distinct expression patterns and GCNs. Cis-regulatory element (CRE) analyses of the MIP promoters and their associated GCN members revealed enrichment for numerous CREs including AP2/ERFs and NACs. CONCLUSIONS: Combining phylogenetic analyses, gene expression profiling, gene co-expression network analyses, and cis-regulatory element enrichment, this study provides a comprehensive overview of the structure and transcriptional regulation of the grapevine MIP family. The study highlights the duplication and sub-functionalization of the family, its strong coordinated expression with genes involved in growth and transport, and the putative classes of TFs responsible for its regulation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4638-5) contains supplementary material, which is available to authorized users. BioMed Central 2018-04-11 /pmc/articles/PMC5896048/ /pubmed/29642857 http://dx.doi.org/10.1186/s12864-018-4638-5 Text en © The Author(s). 2018 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
Wong, Darren Chern Jan
Zhang, Li
Merlin, Isabelle
Castellarin, Simone D.
Gambetta, Gregory A.
Structure and transcriptional regulation of the major intrinsic protein gene family in grapevine
title Structure and transcriptional regulation of the major intrinsic protein gene family in grapevine
title_full Structure and transcriptional regulation of the major intrinsic protein gene family in grapevine
title_fullStr Structure and transcriptional regulation of the major intrinsic protein gene family in grapevine
title_full_unstemmed Structure and transcriptional regulation of the major intrinsic protein gene family in grapevine
title_short Structure and transcriptional regulation of the major intrinsic protein gene family in grapevine
title_sort structure and transcriptional regulation of the major intrinsic protein gene family in grapevine
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5896048/
https://www.ncbi.nlm.nih.gov/pubmed/29642857
http://dx.doi.org/10.1186/s12864-018-4638-5
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