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Successful COG8 and PDF overlap is mediated by alterations in splicing and polyadenylation signals

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Abstract

Although gene-free areas compose the great majority of eukaryotic genomes, a significant fraction of genes overlaps, i.e., unique nucleotide sequences are part of more than one transcription unit. In this work, the evolutionary history and origin of a same-strand gene overlap is dissected through the analysis of COG8 (component of oligomeric Golgi complex 8) and PDF (peptide deformylase). Comparative genomic surveys reveal that the relative locations of these two genes have been changing over the last 445 million years from distinct chromosomal locations in fish to overlapping in rodents and primates, indicating that the overlap between these genes precedes their divergence. The overlap between the two genes was initiated by the gain of a novel splice donor site between the COG8 stop codon and PDF initiation codon. Splicing is accomplished by the use of the PDF acceptor, leading COG8 to share the 3′end with PDF. In primates, loss of the ancestral polyadenylation signal for COG8 makes the overlap between COG8 and PDF mandatory, while in mouse and rat concurrent overlapping and non-overlapping Cog8 transcripts exist. Altogether, we demonstrate that the origin, evolution and preservation of the COG8/PDF same-strand overlap follow similar mechanistic steps as those documented for antisense overlaps where gain and/or loss of splice sites and polyadenylation signals seems to drive the process.

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Abbreviations

COG8 :

Conserved oligomeric Golgi complex subunit 8

PDF :

Peptide deformylase

EST:

Expressed sequence tag

UTR:

Untranslated region

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Acknowledgments

This work was supported by the Fundação para a Ciencia e a Tecnologia (FCT) grants SFRH/BD/44264/2008 to I.P.-C., SFRH/BD/23657/2005 to R.Q., Ciência 2008-ICAAM and research project POCTI/CBO/48218/2002 to L.T.C. and by POPH-QREN-Tipologia 4.2-Scientific employment promotion funded by the European Social Fund and by national funds from the Ministry of Science, Technology and Higher Education (MCTES) to L.A., and partially by research project FCOMP-01-0124-FEDER-007167 sponsored by FCT, COMPETE program and by FEDER funds. The Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP) is an Associate Laboratory of the Portuguese MCTES and is partially supported by FCT.

Conflict of interest

The authors declare that no conflict of interest exists.

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Authors and Affiliations

  1. IPATIMUP, Institute of Molecular Pathology and Immunology, University of Porto, Rua Dr Roberto Frias, s/n, 4200-465, Porto, Portugal

    Isabel Pereira-Castro, Rita Quental, Luís T. da Costa, António Amorim & Luisa Azevedo

  2. FMUP, Faculty of Medicine, University of Porto, Porto, Portugal

    Isabel Pereira-Castro & Luís T. da Costa

  3. FCUP, Faculty of Sciences, University of Porto, Porto, Portugal

    Rita Quental & António Amorim

  4. ICAAM, Institute of Agricultural and Environmental Mediterranean Sciences, University of Evora, Evora, Portugal

    Luís T. da Costa

Authors
  1. Isabel Pereira-Castro
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  2. Rita Quental
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  3. Luís T. da Costa
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  5. Luisa Azevedo
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Correspondence to Isabel Pereira-Castro.

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Pereira-Castro, I., Quental, R., da Costa, L.T. et al. Successful COG8 and PDF overlap is mediated by alterations in splicing and polyadenylation signals. Hum Genet 131, 265–274 (2012). https://doi.org/10.1007/s00439-011-1075-9

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