Abstract
Canonical translation initiation in eukaryotes begins with the Eukaryotic Initiation Factor 4F (eIF4F) complex, made up of eIF4E, which recognizes the 7-methylguanosine cap of messenger RNA, and eIF4G, which serves as a scaffold to recruit other translation initiation factors that ultimately assemble the 80S ribosome. Many eukaryotes have secondary EIF4E genes with divergent properties. The model plant Arabidopsis (Arabidopsis thaliana) encodes two such genes in tandem loci on chromosome 1, EIF4E1B (At1g29550) and EIF4E1C (At1g29590). This work identifies EIF4E1B/EIF4E1C-type genes as a Brassicaceae-specific diverged form of EIF4E. There is little evidence for EIF4E1C gene expression; however, the EIF4E1B gene appears to be expressed at low levels in most tissues, though microarray and RNA Sequencing data support enrichment in reproductive tissue. Purified recombinant eIF4E1b and eIF4E1c proteins retain cap-binding ability and form functional complexes in vitro with eIF4G. The eIF4E1b/eIF4E1c-type proteins support translation in yeast (Saccharomyces cerevisiae) but promote translation initiation in vitro at a lower rate compared with eIF4E. Findings from surface plasmon resonance studies indicate that eIF4E1b and eIF4E1c are unlikely to bind eIF4G in vivo when in competition with eIF4E. This study concludes that eIF4E1b/eIF4E1c-type proteins, although bona fide cap-binding proteins, have divergent properties and, based on apparent limited tissue distribution in Arabidopsis, should be considered functionally distinct from the canonical plant eIF4E involved in translation initiation.
Highlights
Canonical translation initiation in eukaryotes begins with the Eukaryotic Initiation Factor 4F complex, made up of eIF4E, which recognizes the 7-methylguanosine cap of messenger RNA, and eIF4G, which serves as a scaffold to recruit other translation initiation factors that assemble the 80S ribosome
The eIF4E proteins generally thought to be involved in translation initiation are Class I eIF4E proteins (Joshi et al, 2005), of which two exist in flowering plants: eIF4E, which pairs with eIF4G to form the Eukaryotic Initiation Factor 4F (eIF4F) complex, and the plant-specific isoform eIFiso4E, which pairs with eIFiso4G to form eIFiso4F (Mayberry et al, 2011; Patrick and Browning, 2012)
There is little evidence for EIF4E1C gene expression, and the EIF4E1B gene is expressed at low levels in most tissues, though microarray and RNA Sequencing (RNA-Seq) data support enrichment in reproductive tissue
Summary
Canonical translation initiation in eukaryotes begins with the Eukaryotic Initiation Factor 4F (eIF4F) complex, made up of eIF4E, which recognizes the 7-methylguanosine cap of messenger RNA, and eIF4G, which serves as a scaffold to recruit other translation initiation factors that assemble the 80S ribosome. This study concludes that eIF4E1b/eIF4E1c-type proteins, bona fide cap-binding proteins, have divergent properties and, based on apparent limited tissue distribution in Arabidopsis, should be considered functionally distinct from the canonical plant eIF4E involved in translation initiation. Class I eIF4E family members have conserved Trp residues at positions equivalent to Trp-43 and Trp-56 of Homo sapiens eIF4E (Joshi et al, 2005), and the canonical members of this class, such as plant eIF4E and eIFiso4E, have the ability to promote translation through binding of mRNA cap structure and eIF4G (or eIFiso4G). Schizosaccharomyces pombe has a second eIF4E isoform, eIF4E2, which is nonessential under normal growth conditions, but accumulates in response to high temperatures (Ptushkina et al, 2001) It cannot, complement deletion of EIF4E1, and while it can bind capped mRNA and promote translation in vitro, it has reduced ability to bind an eIF4G-derived peptide. The eIF4E-3 isoform of D. melanogaster was recently described as having a specific role in spermatogenesis (Hernández et al, 2012)
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