Two Arabidopsis Loci Encode Novel Eukaryotic Initiation Factor 4E Isoforms That Are Functionally Distinct from the Conserved Plant Eukaryotic Initiation Factor 4E

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 assembl...

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Veröffentlicht in:Plant physiology (Bethesda) 2014-04, Vol.164 (4), p.1820-1830
Hauptverfasser: Patrick, Ryan M., Mayberry, Laura K., Choy, Grace, Woodard, Lauren E., Liu, Joceline S., White, Allyson, Mullen, Rebecca A., Tanavin, Toug M., Latz, Christopher A., Browning, Karen S.
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container_issue 4
container_start_page 1820
container_title Plant physiology (Bethesda)
container_volume 164
creator Patrick, Ryan M.
Mayberry, Laura K.
Choy, Grace
Woodard, Lauren E.
Liu, Joceline S.
White, Allyson
Mullen, Rebecca A.
Tanavin, Toug M.
Latz, Christopher A.
Browning, Karen S.
description 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 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 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.
doi_str_mv 10.1104/pp.113.227785
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derivatives</subject><subject>Guanosine - metabolism</subject><subject>loci</subject><subject>Messenger RNA</subject><subject>Molecular Sequence Data</subject><subject>Peptide initiation factors</subject><subject>Phylogeny</subject><subject>Plants</subject><subject>Protein Binding</subject><subject>Protein Biosynthesis</subject><subject>Protein isoforms</subject><subject>Protein Isoforms - chemistry</subject><subject>Protein Isoforms - metabolism</subject><subject>Proteins</subject><subject>RNA</subject><subject>Saccharomyces cerevisiae - metabolism</subject><subject>Self-Fertilization</subject><subject>translation (genetics)</subject><subject>Yeasts</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk1v0zAYxy0EYt3gyBHkI5cMv8bJBWnq2lGpAg7lbDmOQz2SPMF2ivZ1-KS46qjgtNNj6__T_3lF6A0l15QS8WGacuTXjClVyWdoQSVnBZOieo4WhOQ3qar6Al3GeE8IoZyKl-iCCUloVhfo9-4X4JtgGt_CFH3EW7Aer0YLrcOf4eB6vJp_mPAAyVu8GX3yJnkY8drYBAGLFd5E6CAMEe_2JmUvh9fzaI-Q6fsHfOtj8vmPuwADTnuHlzBGFw6uxV97M6anErxCLzrTR_f6MV6hb-vVbvmp2H652yxvtoUVgqWirUpLZE0YIy2vbcdV2SlLGlqTrrHMqYa5upOyaYRsJStrUtJWWVoZYfIoFL9CH0--09wMrrVuTMH0egp-yOVpMF7_r4x-r7_DQfO6YkrIbPD-0SDAz9nFpAcfretzkw7mqNlxAVQpxp9EqaRCcKFqmtHihNoAMQbXnSuiRB9PQE9TjlyfTiDz7_5t40z_3XkG3p6A-5gHfNYFpzlbyfkfiBa4Nw</recordid><startdate>20140401</startdate><enddate>20140401</enddate><creator>Patrick, Ryan M.</creator><creator>Mayberry, Laura K.</creator><creator>Choy, Grace</creator><creator>Woodard, Lauren E.</creator><creator>Liu, Joceline S.</creator><creator>White, Allyson</creator><creator>Mullen, Rebecca A.</creator><creator>Tanavin, Toug M.</creator><creator>Latz, Christopher A.</creator><creator>Browning, Karen S.</creator><general>American Society of Plant Biologists</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20140401</creationdate><title>Two Arabidopsis Loci Encode Novel Eukaryotic Initiation Factor 4E Isoforms That Are Functionally Distinct from the Conserved Plant Eukaryotic Initiation Factor 4E</title><author>Patrick, Ryan M. ; Mayberry, Laura K. ; Choy, Grace ; Woodard, Lauren E. ; Liu, Joceline S. ; White, Allyson ; Mullen, Rebecca A. ; Tanavin, Toug M. ; Latz, Christopher A. ; Browning, Karen S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-d86c0590220d39cf376f7c0b190fbc2e7b2e9f55bb45d5269061d7c18a4a00373</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Amino Acid Sequence</topic><topic>Arabidopsis</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - chemistry</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>BIOCHEMISTRY AND METABOLISM</topic><topic>Biological Assay</topic><topic>Computer Simulation</topic><topic>Conserved Sequence</topic><topic>Electrophoresis, Polyacrylamide Gel</topic><topic>Eukaryotic Initiation Factor-4E - metabolism</topic><topic>Eukaryotic Initiation Factor-4G - metabolism</topic><topic>Eukaryotic initiation factors</topic><topic>Genes</topic><topic>Genetic Complementation Test</topic><topic>Genetic Loci</topic><topic>Genetic screening</topic><topic>Genomes</topic><topic>Guanosine - analogs &amp; derivatives</topic><topic>Guanosine - metabolism</topic><topic>loci</topic><topic>Messenger RNA</topic><topic>Molecular Sequence Data</topic><topic>Peptide initiation factors</topic><topic>Phylogeny</topic><topic>Plants</topic><topic>Protein Binding</topic><topic>Protein Biosynthesis</topic><topic>Protein isoforms</topic><topic>Protein Isoforms - chemistry</topic><topic>Protein Isoforms - metabolism</topic><topic>Proteins</topic><topic>RNA</topic><topic>Saccharomyces cerevisiae - metabolism</topic><topic>Self-Fertilization</topic><topic>translation (genetics)</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Patrick, Ryan M.</creatorcontrib><creatorcontrib>Mayberry, Laura K.</creatorcontrib><creatorcontrib>Choy, Grace</creatorcontrib><creatorcontrib>Woodard, Lauren E.</creatorcontrib><creatorcontrib>Liu, Joceline S.</creatorcontrib><creatorcontrib>White, Allyson</creatorcontrib><creatorcontrib>Mullen, Rebecca A.</creatorcontrib><creatorcontrib>Tanavin, Toug M.</creatorcontrib><creatorcontrib>Latz, Christopher A.</creatorcontrib><creatorcontrib>Browning, Karen S.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Patrick, Ryan M.</au><au>Mayberry, Laura K.</au><au>Choy, Grace</au><au>Woodard, Lauren E.</au><au>Liu, Joceline S.</au><au>White, Allyson</au><au>Mullen, Rebecca A.</au><au>Tanavin, Toug M.</au><au>Latz, Christopher A.</au><au>Browning, Karen S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Two Arabidopsis Loci Encode Novel Eukaryotic Initiation Factor 4E Isoforms That Are Functionally Distinct from the Conserved Plant Eukaryotic Initiation Factor 4E</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2014-04-01</date><risdate>2014</risdate><volume>164</volume><issue>4</issue><spage>1820</spage><epage>1830</epage><pages>1820-1830</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><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 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 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.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>24501003</pmid><doi>10.1104/pp.113.227785</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record>
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source Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals
subjects Amino Acid Sequence
Arabidopsis
Arabidopsis - metabolism
Arabidopsis Proteins - chemistry
Arabidopsis Proteins - metabolism
BIOCHEMISTRY AND METABOLISM
Biological Assay
Computer Simulation
Conserved Sequence
Electrophoresis, Polyacrylamide Gel
Eukaryotic Initiation Factor-4E - metabolism
Eukaryotic Initiation Factor-4G - metabolism
Eukaryotic initiation factors
Genes
Genetic Complementation Test
Genetic Loci
Genetic screening
Genomes
Guanosine - analogs & derivatives
Guanosine - metabolism
loci
Messenger RNA
Molecular Sequence Data
Peptide initiation factors
Phylogeny
Plants
Protein Binding
Protein Biosynthesis
Protein isoforms
Protein Isoforms - chemistry
Protein Isoforms - metabolism
Proteins
RNA
Saccharomyces cerevisiae - metabolism
Self-Fertilization
translation (genetics)
Yeasts
title Two Arabidopsis Loci Encode Novel Eukaryotic Initiation Factor 4E Isoforms That Are Functionally Distinct from the Conserved Plant Eukaryotic Initiation Factor 4E
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