Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization.

BACKGROUND:Poly(A) polymerase is a key enzyme in the machinery that mediates mRNA 3' end formation in eukaryotes. In plants, poly(A) polymerases are encoded by modest gene families. To better understand this multiplicity of genes, poly(A) polymerase-encoding genes from several other plants, as...

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Main Authors: Lisa R Meeks, Balasubrahmanyam Addepalli, Arthur G Hunt
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-11-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC2778134?pdf=render
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spelling doaj-47d6677bb1fe47b8bda2cb8c791082d72020-11-24T21:47:46ZengPublic Library of Science (PLoS)PLoS ONE1932-62032009-11-01411e808210.1371/journal.pone.0008082Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization.Lisa R MeeksBalasubrahmanyam AddepalliArthur G HuntBACKGROUND:Poly(A) polymerase is a key enzyme in the machinery that mediates mRNA 3' end formation in eukaryotes. In plants, poly(A) polymerases are encoded by modest gene families. To better understand this multiplicity of genes, poly(A) polymerase-encoding genes from several other plants, as well as from Selaginella, Physcomitrella, and Chlamydomonas, were studied. METHODOLOGY/PRINCIPAL FINDINGS:Using bioinformatics tools, poly(A) polymerase-encoding genes were identified in the genomes of eight species in the plant lineage. Whereas Chlamydomonas reinhardtii was found to possess a single poly(A) polymerase gene, other species possessed between two and six possible poly(A) polymerase genes. With the exception of four intron-lacking genes, all of the plant poly(A) polymerase genes (but not the C. reinhardtii gene) possessed almost identical intron positions within the poly(A) polymerase coding sequences, suggesting that all plant poly(A) polymerase genes derive from a single ancestral gene. The four Arabidopsis poly(A) polymerase genes were found to be essential, based on genetic analysis of T-DNA insertion mutants. GFP fusion proteins containing three of the four Arabidopsis poly(A) polymerases localized to the nucleus, while one such fusion protein was localized in the cytoplasm. The fact that this latter protein is largely pollen-specific suggests that it has important roles in male gametogenesis. CONCLUSIONS/SIGNIFICANCE:Our results indicate that poly(A) polymerase genes have expanded from a single ancestral gene by a series of duplication events during the evolution of higher plants, and that individual members have undergone sorts of functional specialization so as to render them essential for plant growth and development. Perhaps the most interesting of the plant poly(A) polymerases is a novel cytoplasmic poly(A) polymerase that is expressed in pollen in Arabidopsis; this is reminiscent of spermatocyte-specific cytoplasmic poly(A) polymerases in mammals.http://europepmc.org/articles/PMC2778134?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Lisa R Meeks
Balasubrahmanyam Addepalli
Arthur G Hunt
spellingShingle Lisa R Meeks
Balasubrahmanyam Addepalli
Arthur G Hunt
Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization.
PLoS ONE
author_facet Lisa R Meeks
Balasubrahmanyam Addepalli
Arthur G Hunt
author_sort Lisa R Meeks
title Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization.
title_short Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization.
title_full Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization.
title_fullStr Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization.
title_full_unstemmed Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization.
title_sort characterization of genes encoding poly(a) polymerases in plants: evidence for duplication and functional specialization.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2009-11-01
description BACKGROUND:Poly(A) polymerase is a key enzyme in the machinery that mediates mRNA 3' end formation in eukaryotes. In plants, poly(A) polymerases are encoded by modest gene families. To better understand this multiplicity of genes, poly(A) polymerase-encoding genes from several other plants, as well as from Selaginella, Physcomitrella, and Chlamydomonas, were studied. METHODOLOGY/PRINCIPAL FINDINGS:Using bioinformatics tools, poly(A) polymerase-encoding genes were identified in the genomes of eight species in the plant lineage. Whereas Chlamydomonas reinhardtii was found to possess a single poly(A) polymerase gene, other species possessed between two and six possible poly(A) polymerase genes. With the exception of four intron-lacking genes, all of the plant poly(A) polymerase genes (but not the C. reinhardtii gene) possessed almost identical intron positions within the poly(A) polymerase coding sequences, suggesting that all plant poly(A) polymerase genes derive from a single ancestral gene. The four Arabidopsis poly(A) polymerase genes were found to be essential, based on genetic analysis of T-DNA insertion mutants. GFP fusion proteins containing three of the four Arabidopsis poly(A) polymerases localized to the nucleus, while one such fusion protein was localized in the cytoplasm. The fact that this latter protein is largely pollen-specific suggests that it has important roles in male gametogenesis. CONCLUSIONS/SIGNIFICANCE:Our results indicate that poly(A) polymerase genes have expanded from a single ancestral gene by a series of duplication events during the evolution of higher plants, and that individual members have undergone sorts of functional specialization so as to render them essential for plant growth and development. Perhaps the most interesting of the plant poly(A) polymerases is a novel cytoplasmic poly(A) polymerase that is expressed in pollen in Arabidopsis; this is reminiscent of spermatocyte-specific cytoplasmic poly(A) polymerases in mammals.
url http://europepmc.org/articles/PMC2778134?pdf=render
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