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Distinct types of short open reading frames are translated in plant cells

View ORCID ProfileIgor Fesenko, Ilya Kirov, Andrey Kniazev, Regina Khazigaleeva, Vassili Lazarev, Daria Kharlampieva, Ekaterina Grafskaia, Viktor Zgoda, Ivan Butenko, Georgy Arapidi, Anna Mamaeva, Vadim Ivanov, Vadim Govorun
doi: https://doi.org/10.1101/213736
Igor Fesenko
1Laboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
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  • ORCID record for Igor Fesenko
  • For correspondence: fesigor@gmail.com
Ilya Kirov
1Laboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
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Andrey Kniazev
1Laboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
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Regina Khazigaleeva
1Laboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
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Vassili Lazarev
2Federal Research and Clinical Centre of Physical-Chemical Medicine, Moscow, Russian Federation
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Daria Kharlampieva
2Federal Research and Clinical Centre of Physical-Chemical Medicine, Moscow, Russian Federation
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Ekaterina Grafskaia
2Federal Research and Clinical Centre of Physical-Chemical Medicine, Moscow, Russian Federation
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Viktor Zgoda
3Laboratory of System Biology, Institute of Biomedical Chemistry, Moscow, Russian Federation
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Ivan Butenko
2Federal Research and Clinical Centre of Physical-Chemical Medicine, Moscow, Russian Federation
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Georgy Arapidi
1Laboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
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Anna Mamaeva
1Laboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
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Vadim Ivanov
1Laboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
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Vadim Govorun
1Laboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
2Federal Research and Clinical Centre of Physical-Chemical Medicine, Moscow, Russian Federation
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ABSTRACT

Genomes contain millions of short (<100 codons) open reading frames (sORFs), which are usually dismissed during gene annotation. Nevertheless, peptides encoded by such sORFs can play important biological roles, and their impact on cellular processes has long been underestimated. Here, we analyzed approximately 70,000 transcribed sORFs in the model plant Physcomitrella patens (moss). Several distinct classes of sORFs that differ in terms of their position on transcripts and the level of evolutionary conservation are present in the moss genome. Over 5000 sORFs were conserved in at least one of ten plant species examined. Mass spectrometry analysis of proteomic and peptidomic datasets suggested that 584 sORFs located on distinct parts of mRNAs and long non-coding RNAs (lncRNAs) are translated, including 73 conservative sORFs. Translational analysis of the sORFs and main ORFs at a single locus suggested the existence of genes that code for multiple proteins and peptides with tissue-specific expression. Alternative splicing is likely involved in the excision of translatable sORFs from such transcripts. We identified a group of sORFs homologous to known protein domains and suggested they function as small interfering peptides. Functional analysis of candidate lncRNA-encoded peptides showed it to be involved in regulating growth and differentiation in moss. The high evolutionary rate and wide translation of sORFs suggest that they may provide a reservoir of potentially active peptides and their importance as a raw material for gene evolution. Our results thus open new avenues for discovering novel, biologically active peptides in the plant kingdom.

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Posted June 01, 2018.
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Distinct types of short open reading frames are translated in plant cells
Igor Fesenko, Ilya Kirov, Andrey Kniazev, Regina Khazigaleeva, Vassili Lazarev, Daria Kharlampieva, Ekaterina Grafskaia, Viktor Zgoda, Ivan Butenko, Georgy Arapidi, Anna Mamaeva, Vadim Ivanov, Vadim Govorun
bioRxiv 213736; doi: https://doi.org/10.1101/213736
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Distinct types of short open reading frames are translated in plant cells
Igor Fesenko, Ilya Kirov, Andrey Kniazev, Regina Khazigaleeva, Vassili Lazarev, Daria Kharlampieva, Ekaterina Grafskaia, Viktor Zgoda, Ivan Butenko, Georgy Arapidi, Anna Mamaeva, Vadim Ivanov, Vadim Govorun
bioRxiv 213736; doi: https://doi.org/10.1101/213736

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