In Depth Exploration of the Alternative Proteome of Drosophila melanogaster

Recent studies have shown that hundreds of small proteins were occulted when protein-coding genes were annotated. These proteins, called alternative proteins, have failed to be annotated notably due to the short length of their open reading frame (less than 100 codons) or the enforced rule establish...

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Main Authors: Bertrand Fabre, Sebastien A. Choteau, Carine Duboé, Carole Pichereaux, Audrey Montigny, Dagmara Korona, Michael J. Deery, Mylène Camus, Christine Brun, Odile Burlet-Schiltz, Steven Russell, Jean-Philippe Combier, Kathryn S. Lilley, Serge Plaza
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Cell and Developmental Biology
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Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2022.901351/full
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author Bertrand Fabre
Bertrand Fabre
Sebastien A. Choteau
Carine Duboé
Carole Pichereaux
Carole Pichereaux
Carole Pichereaux
Audrey Montigny
Dagmara Korona
Michael J. Deery
Mylène Camus
Mylène Camus
Christine Brun
Christine Brun
Odile Burlet-Schiltz
Odile Burlet-Schiltz
Steven Russell
Jean-Philippe Combier
Kathryn S. Lilley
Serge Plaza
author_facet Bertrand Fabre
Bertrand Fabre
Sebastien A. Choteau
Carine Duboé
Carole Pichereaux
Carole Pichereaux
Carole Pichereaux
Audrey Montigny
Dagmara Korona
Michael J. Deery
Mylène Camus
Mylène Camus
Christine Brun
Christine Brun
Odile Burlet-Schiltz
Odile Burlet-Schiltz
Steven Russell
Jean-Philippe Combier
Kathryn S. Lilley
Serge Plaza
author_sort Bertrand Fabre
collection DOAJ
description Recent studies have shown that hundreds of small proteins were occulted when protein-coding genes were annotated. These proteins, called alternative proteins, have failed to be annotated notably due to the short length of their open reading frame (less than 100 codons) or the enforced rule establishing that messenger RNAs (mRNAs) are monocistronic. Several alternative proteins were shown to be biologically active molecules and seem to be involved in a wide range of biological functions. However, genome-wide exploration of the alternative proteome is still limited to a few species. In the present article, we describe a deep peptidomics workflow which enabled the identification of 401 alternative proteins in Drosophila melanogaster. Subcellular localization, protein domains, and short linear motifs were predicted for 235 of the alternative proteins identified and point toward specific functions of these small proteins. Several alternative proteins had approximated abundances higher than their canonical counterparts, suggesting that these alternative proteins are actually the main products of their corresponding genes. Finally, we observed 14 alternative proteins with developmentally regulated expression patterns and 10 induced upon the heat-shock treatment of embryos, demonstrating stage or stress-specific production of alternative proteins.
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spelling doaj.art-c3280b188e334a1b912ba22d6e1bf5092022-12-22T00:18:26ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2022-05-011010.3389/fcell.2022.901351901351In Depth Exploration of the Alternative Proteome of Drosophila melanogasterBertrand Fabre0Bertrand Fabre1Sebastien A. Choteau2Carine Duboé3Carole Pichereaux4Carole Pichereaux5Carole Pichereaux6Audrey Montigny7Dagmara Korona8Michael J. Deery9Mylène Camus10Mylène Camus11Christine Brun12Christine Brun13Odile Burlet-Schiltz14Odile Burlet-Schiltz15Steven Russell16Jean-Philippe Combier17Kathryn S. Lilley18Serge Plaza19Laboratoire de Recherche en Sciences Végétales, UMR5546, Université de Toulouse, UPS, INP, CNRS, Auzeville-Tolosane, FranceCambridge Centre for Proteomics, Cambridge Systems Biology Centre and Department of Biochemistry, University of Cambridge, Cambridge, United KingdomAix-Marseille Université, INSERM, TAGC, Turing Centre for Living Systems, Marseille, FranceLaboratoire de Recherche en Sciences Végétales, UMR5546, Université de Toulouse, UPS, INP, CNRS, Auzeville-Tolosane, FranceFédération de Recherche (FR3450), Agrobiosciences, Interactions et Biodiversité (AIB), CNRS, Toulouse, FranceInstitut de Pharmacologie et de Biologie Structurale (IPBS), Université de Toulouse, CNRS, UPS, Toulouse, FranceInfrastructure Nationale de Protéomique, ProFI, FR 2048, Toulouse, FranceLaboratoire de Recherche en Sciences Végétales, UMR5546, Université de Toulouse, UPS, INP, CNRS, Auzeville-Tolosane, FranceCambridge Systems Biology Centre and Department of Genetics, University of Cambridge, Cambridge, United KingdomCambridge Centre for Proteomics, Cambridge Systems Biology Centre and Department of Biochemistry, University of Cambridge, Cambridge, United KingdomInstitut de Pharmacologie et de Biologie Structurale (IPBS), Université de Toulouse, CNRS, UPS, Toulouse, FranceInfrastructure Nationale de Protéomique, ProFI, FR 2048, Toulouse, FranceAix-Marseille Université, INSERM, TAGC, Turing Centre for Living Systems, Marseille, FranceCNRS, Marseille, FranceInstitut de Pharmacologie et de Biologie Structurale (IPBS), Université de Toulouse, CNRS, UPS, Toulouse, FranceInfrastructure Nationale de Protéomique, ProFI, FR 2048, Toulouse, FranceCambridge Systems Biology Centre and Department of Genetics, University of Cambridge, Cambridge, United KingdomLaboratoire de Recherche en Sciences Végétales, UMR5546, Université de Toulouse, UPS, INP, CNRS, Auzeville-Tolosane, FranceCambridge Centre for Proteomics, Cambridge Systems Biology Centre and Department of Biochemistry, University of Cambridge, Cambridge, United KingdomLaboratoire de Recherche en Sciences Végétales, UMR5546, Université de Toulouse, UPS, INP, CNRS, Auzeville-Tolosane, FranceRecent studies have shown that hundreds of small proteins were occulted when protein-coding genes were annotated. These proteins, called alternative proteins, have failed to be annotated notably due to the short length of their open reading frame (less than 100 codons) or the enforced rule establishing that messenger RNAs (mRNAs) are monocistronic. Several alternative proteins were shown to be biologically active molecules and seem to be involved in a wide range of biological functions. However, genome-wide exploration of the alternative proteome is still limited to a few species. In the present article, we describe a deep peptidomics workflow which enabled the identification of 401 alternative proteins in Drosophila melanogaster. Subcellular localization, protein domains, and short linear motifs were predicted for 235 of the alternative proteins identified and point toward specific functions of these small proteins. Several alternative proteins had approximated abundances higher than their canonical counterparts, suggesting that these alternative proteins are actually the main products of their corresponding genes. Finally, we observed 14 alternative proteins with developmentally regulated expression patterns and 10 induced upon the heat-shock treatment of embryos, demonstrating stage or stress-specific production of alternative proteins.https://www.frontiersin.org/articles/10.3389/fcell.2022.901351/fullalternative proteinsshort open reading frame–encoded polypeptidemicroproteinpeptidomicsmass spectrometry
spellingShingle Bertrand Fabre
Bertrand Fabre
Sebastien A. Choteau
Carine Duboé
Carole Pichereaux
Carole Pichereaux
Carole Pichereaux
Audrey Montigny
Dagmara Korona
Michael J. Deery
Mylène Camus
Mylène Camus
Christine Brun
Christine Brun
Odile Burlet-Schiltz
Odile Burlet-Schiltz
Steven Russell
Jean-Philippe Combier
Kathryn S. Lilley
Serge Plaza
In Depth Exploration of the Alternative Proteome of Drosophila melanogaster
Frontiers in Cell and Developmental Biology
alternative proteins
short open reading frame–encoded polypeptide
microprotein
peptidomics
mass spectrometry
title In Depth Exploration of the Alternative Proteome of Drosophila melanogaster
title_full In Depth Exploration of the Alternative Proteome of Drosophila melanogaster
title_fullStr In Depth Exploration of the Alternative Proteome of Drosophila melanogaster
title_full_unstemmed In Depth Exploration of the Alternative Proteome of Drosophila melanogaster
title_short In Depth Exploration of the Alternative Proteome of Drosophila melanogaster
title_sort in depth exploration of the alternative proteome of drosophila melanogaster
topic alternative proteins
short open reading frame–encoded polypeptide
microprotein
peptidomics
mass spectrometry
url https://www.frontiersin.org/articles/10.3389/fcell.2022.901351/full
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