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Phylogenetic analysis reveals dynamic evolution of the poly(A)-binding protein gene family in plants

BACKGROUND: The poly(A)-binding protein (PABP) binds the poly(A) tail of eukaryotic mRNAs and functions to maintain the integrity of the mRNA while promoting protein synthesis through its interaction with eukaryotic translation initiation factor (eIF) 4G and eIF4B. PABP is encoded by a single gene i...

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Autores principales: Gallie, Daniel R, Liu, Renyi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4252990/
https://www.ncbi.nlm.nih.gov/pubmed/25421536
http://dx.doi.org/10.1186/s12862-014-0238-4
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author Gallie, Daniel R
Liu, Renyi
author_facet Gallie, Daniel R
Liu, Renyi
author_sort Gallie, Daniel R
collection PubMed
description BACKGROUND: The poly(A)-binding protein (PABP) binds the poly(A) tail of eukaryotic mRNAs and functions to maintain the integrity of the mRNA while promoting protein synthesis through its interaction with eukaryotic translation initiation factor (eIF) 4G and eIF4B. PABP is encoded by a single gene in yeast and marine algae but during plant evolution the PABP gene family expanded substantially, underwent sequence divergence into three subclasses, and acquired tissue-specificity in gene family member expression. Although such changes suggest functional specialization, the size of the family and its sequence divergence have complicated an understanding of which gene family members may be foundational and which may represent more recent expansions of the family to meet the specific needs of speciation. Here, we examine the evolution of the plant PABP gene family to provide insight into these aspects of the family that may yield clues into the function of individual family members. RESULTS: The PABP gene family had expanded to two members by the appearance of fresh water algae and four members in non-vascular plants. In lycophytes, the first sequence divergence yielding a specific class member occurs. The earliest members of the gene family share greatest similarity to those modern members whose expression is confined to reproductive tissues, suggesting that supporting reproductive-associated gene expression is the most conserved function of this family. A family member sharing similarity to modern vegetative-associated members first appears in gymnosperms. Further elaboration of the reproductive-associated and vegetative-associated members occurred during the evolution of flowering plants. CONCLUSIONS: Expansion of the plant PABP gene family began prior to the colonization of land. By the evolution of lycophytes, the first class member whose expression is confined to reproductive tissues in higher plants had appeared. A second class member whose expression is vegetative-associated appeared in gymnosperms and all three modern classes had fully evolved by the appearance of the first known basal angiosperm. The size of each PABP class underwent further expansion during subsequent evolution, especially in the Brassicaceae, suggesting that the family is undergoing dynamic evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-014-0238-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-42529902014-12-04 Phylogenetic analysis reveals dynamic evolution of the poly(A)-binding protein gene family in plants Gallie, Daniel R Liu, Renyi BMC Evol Biol Research Article BACKGROUND: The poly(A)-binding protein (PABP) binds the poly(A) tail of eukaryotic mRNAs and functions to maintain the integrity of the mRNA while promoting protein synthesis through its interaction with eukaryotic translation initiation factor (eIF) 4G and eIF4B. PABP is encoded by a single gene in yeast and marine algae but during plant evolution the PABP gene family expanded substantially, underwent sequence divergence into three subclasses, and acquired tissue-specificity in gene family member expression. Although such changes suggest functional specialization, the size of the family and its sequence divergence have complicated an understanding of which gene family members may be foundational and which may represent more recent expansions of the family to meet the specific needs of speciation. Here, we examine the evolution of the plant PABP gene family to provide insight into these aspects of the family that may yield clues into the function of individual family members. RESULTS: The PABP gene family had expanded to two members by the appearance of fresh water algae and four members in non-vascular plants. In lycophytes, the first sequence divergence yielding a specific class member occurs. The earliest members of the gene family share greatest similarity to those modern members whose expression is confined to reproductive tissues, suggesting that supporting reproductive-associated gene expression is the most conserved function of this family. A family member sharing similarity to modern vegetative-associated members first appears in gymnosperms. Further elaboration of the reproductive-associated and vegetative-associated members occurred during the evolution of flowering plants. CONCLUSIONS: Expansion of the plant PABP gene family began prior to the colonization of land. By the evolution of lycophytes, the first class member whose expression is confined to reproductive tissues in higher plants had appeared. A second class member whose expression is vegetative-associated appeared in gymnosperms and all three modern classes had fully evolved by the appearance of the first known basal angiosperm. The size of each PABP class underwent further expansion during subsequent evolution, especially in the Brassicaceae, suggesting that the family is undergoing dynamic evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-014-0238-4) contains supplementary material, which is available to authorized users. BioMed Central 2014-11-25 /pmc/articles/PMC4252990/ /pubmed/25421536 http://dx.doi.org/10.1186/s12862-014-0238-4 Text en © Gallie and Liu; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Gallie, Daniel R
Liu, Renyi
Phylogenetic analysis reveals dynamic evolution of the poly(A)-binding protein gene family in plants
title Phylogenetic analysis reveals dynamic evolution of the poly(A)-binding protein gene family in plants
title_full Phylogenetic analysis reveals dynamic evolution of the poly(A)-binding protein gene family in plants
title_fullStr Phylogenetic analysis reveals dynamic evolution of the poly(A)-binding protein gene family in plants
title_full_unstemmed Phylogenetic analysis reveals dynamic evolution of the poly(A)-binding protein gene family in plants
title_short Phylogenetic analysis reveals dynamic evolution of the poly(A)-binding protein gene family in plants
title_sort phylogenetic analysis reveals dynamic evolution of the poly(a)-binding protein gene family in plants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4252990/
https://www.ncbi.nlm.nih.gov/pubmed/25421536
http://dx.doi.org/10.1186/s12862-014-0238-4
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