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The evolution of the Puf superfamily of proteins across the tree of eukaryotes

Najdrová, Vladimíra ; Stairs, Courtney W. LU orcid ; Vinopalová, Martina ; Voleman, Luboš and Doležal, Pavel (2020) In BMC Biology 18.
Abstract

Background: Eukaryotic gene expression is controlled by a number of RNA-binding proteins (RBP), such as the proteins from the Puf (Pumilio and FBF) superfamily (PufSF). These proteins bind to RNA via multiple Puf repeat domains, each of which specifically recognizes a single RNA base. Recently, three diversified PufSF proteins have been described in model organisms, each of which is responsible for the maturation of ribosomal RNA or the translational regulation of mRNAs; however, less is known about the role of these proteins across eukaryotic diversity. Results: Here, we investigated the distribution and function of PufSF RBPs in the tree of eukaryotes. We determined that the following PufSF proteins are universally conserved across... (More)

Background: Eukaryotic gene expression is controlled by a number of RNA-binding proteins (RBP), such as the proteins from the Puf (Pumilio and FBF) superfamily (PufSF). These proteins bind to RNA via multiple Puf repeat domains, each of which specifically recognizes a single RNA base. Recently, three diversified PufSF proteins have been described in model organisms, each of which is responsible for the maturation of ribosomal RNA or the translational regulation of mRNAs; however, less is known about the role of these proteins across eukaryotic diversity. Results: Here, we investigated the distribution and function of PufSF RBPs in the tree of eukaryotes. We determined that the following PufSF proteins are universally conserved across eukaryotes and can be broadly classified into three groups: (i) Nop9 orthologues, which participate in the nucleolar processing of immature 18S rRNA; (ii) 'classical' Pufs, which control the translation of mRNA; and (iii) PUM3 orthologues, which are involved in the maturation of 7S rRNA. In nearly all eukaryotes, the rRNA maturation proteins, Nop9 and PUM3, are retained as a single copy, while mRNA effectors ('classical' Pufs) underwent multiple lineage-specific expansions. We propose that the variation in number of 'classical' Pufs relates to the size of the transcriptome and thus the potential mRNA targets. We further distinguished full set of PufSF proteins in divergent metamonad Giardia intestinalis and initiated their cellular and biochemical characterization. Conclusions: Our data suggest that the last eukaryotic common ancestor (LECA) already contained all three types of PufSF proteins and that 'classical' Pufs then underwent lineage-specific expansions.

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author
; ; ; and
publishing date
type
Contribution to journal
publication status
published
keywords
Giardia intestinalis, LECA, Puf superfamily proteins, RNA processing, RNA-binding protein
in
BMC Biology
volume
18
article number
77
pages
18 pages
publisher
BioMed Central (BMC)
external identifiers
  • scopus:85087409692
  • pmid:32605621
ISSN
1741-7007
DOI
10.1186/s12915-020-00814-3
language
English
LU publication?
no
id
21cc1d4b-a640-4953-8edb-27b40f7aa081
date added to LUP
2020-10-23 10:45:52
date last changed
2024-05-29 21:02:34
@article{21cc1d4b-a640-4953-8edb-27b40f7aa081,
  abstract     = {{<p>Background: Eukaryotic gene expression is controlled by a number of RNA-binding proteins (RBP), such as the proteins from the Puf (Pumilio and FBF) superfamily (PufSF). These proteins bind to RNA via multiple Puf repeat domains, each of which specifically recognizes a single RNA base. Recently, three diversified PufSF proteins have been described in model organisms, each of which is responsible for the maturation of ribosomal RNA or the translational regulation of mRNAs; however, less is known about the role of these proteins across eukaryotic diversity. Results: Here, we investigated the distribution and function of PufSF RBPs in the tree of eukaryotes. We determined that the following PufSF proteins are universally conserved across eukaryotes and can be broadly classified into three groups: (i) Nop9 orthologues, which participate in the nucleolar processing of immature 18S rRNA; (ii) 'classical' Pufs, which control the translation of mRNA; and (iii) PUM3 orthologues, which are involved in the maturation of 7S rRNA. In nearly all eukaryotes, the rRNA maturation proteins, Nop9 and PUM3, are retained as a single copy, while mRNA effectors ('classical' Pufs) underwent multiple lineage-specific expansions. We propose that the variation in number of 'classical' Pufs relates to the size of the transcriptome and thus the potential mRNA targets. We further distinguished full set of PufSF proteins in divergent metamonad Giardia intestinalis and initiated their cellular and biochemical characterization. Conclusions: Our data suggest that the last eukaryotic common ancestor (LECA) already contained all three types of PufSF proteins and that 'classical' Pufs then underwent lineage-specific expansions.</p>}},
  author       = {{Najdrová, Vladimíra and Stairs, Courtney W. and Vinopalová, Martina and Voleman, Luboš and Doležal, Pavel}},
  issn         = {{1741-7007}},
  keywords     = {{Giardia intestinalis; LECA; Puf superfamily proteins; RNA processing; RNA-binding protein}},
  language     = {{eng}},
  month        = {{06}},
  publisher    = {{BioMed Central (BMC)}},
  series       = {{BMC Biology}},
  title        = {{The evolution of the Puf superfamily of proteins across the tree of eukaryotes}},
  url          = {{http://dx.doi.org/10.1186/s12915-020-00814-3}},
  doi          = {{10.1186/s12915-020-00814-3}},
  volume       = {{18}},
  year         = {{2020}},
}