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

Darren Chern Jan Wong,Simone D Castellarin,Isabelle Merlin,Gregory A Gambetta,Li Zhang

doi:10.1186/s12864-018-4638-5

Darren Chern Jan Wong, Simone D Castellarin + Show 3 more

Open Access

https://doi.org/10.1186/s12864-018-4638-5

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Abstract

BackgroundThe 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.ResultsA 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.ConclusionsCombining 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.

Highlights

The major intrinsic protein (MIP) family is a family of proteins, including aquaporins, which facilitate water and small molecule transport across plasma membranes
We examined the nature of duplication events contributing to the size of the grapevine MIP gene family (Fig. 2; Additional file 1: Table S1)
When paired with the Gene co-expression network (GCN) analyses conducted here we identified those MIP family members that have undergone duplication and sub-functionalization through characterizing the tissue and developmental specific expression patterns across the family

Summary

Introduction

The major intrinsic protein (MIP) family is a family of proteins, including aquaporins, which facilitate water and small molecule transport across plasma membranes. The plasma membrane intrinsic proteins (PIPs), the tonoplast intrinsic proteins (TIPs), and the nodulin26-like intrinsic proteins (NIPs), comprise the major subfamilies [6, 8, 13] These three groups of aquaporins have been intensively studied and well-documented. The small basic intrinsic proteins (SIPs) include only a few isoforms localized in the ER (e.g., 3 homologs in Arabidopsis) [9, 14] In addition to these four well-conserved subfamilies present in all plant species, several additional novel types of aquaporins have been distinguished but with a less ubiquitous presence among plant species. The GlpF-like intrinsic proteins and the hybrid intrinsic proteins were discovered in moss and algae, but are absent in vascular plants [9, 13]

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