Retrotransposon gag-like 1 (RTL1) and the molecular evolution of self-targeting imprinted microRNAs.


Journal

Biology direct
ISSN: 1745-6150
Titre abrégé: Biol Direct
Pays: England
ID NLM: 101258412

Informations de publication

Date de publication:
22 10 2019
Historique:
received: 30 04 2019
accepted: 26 09 2019
entrez: 24 10 2019
pubmed: 24 10 2019
medline: 9 6 2020
Statut: epublish

Résumé

Transcription of the antisense strand of RTL1 produces a sense mRNA that is targeted for degradation by antisense microRNAs transcribed from the sense strand. Translation of the mRNA produces a retrotransposon-derived protein that is implicated in placental development. The sense and antisense transcripts are oppositely imprinted: sense mRNAs are expressed from the paternally-derived chromosome, antisense microRNAs from the maternally-derived chromosome. Two microRNAs at the RTL1 locus, miR-431 and the rodent-specific miR-434, are derived from within tandem repeats. We present an evolutionary model for the establishment of a new self-targeting microRNA derived from within a tandem repeat that inhibits production of RTL1 protein when maternally-derived in heterozygotes but not when paternally-derived. The interaction of sense and antisense transcripts can be interpreted as a form of communication between maternally-derived and paternally-derived RTL1 alleles that possesses many of the features of a greenbeard effect. This interaction is evolutionary stable, unlike a typical greenbeard effect, because of the necessary complementarity between microRNAs and mRNA transcribed from opposite strands of the same double helix. We conjecture that microRNAs and mRNA cooperate to reduce demands on mothers when an allele is paired with itself in homozygous offspring. This article was reviewed by Eugene Berezikov and Bernard Crespi.

Sections du résumé

BACKGROUND
Transcription of the antisense strand of RTL1 produces a sense mRNA that is targeted for degradation by antisense microRNAs transcribed from the sense strand. Translation of the mRNA produces a retrotransposon-derived protein that is implicated in placental development. The sense and antisense transcripts are oppositely imprinted: sense mRNAs are expressed from the paternally-derived chromosome, antisense microRNAs from the maternally-derived chromosome.
RESULTS
Two microRNAs at the RTL1 locus, miR-431 and the rodent-specific miR-434, are derived from within tandem repeats. We present an evolutionary model for the establishment of a new self-targeting microRNA derived from within a tandem repeat that inhibits production of RTL1 protein when maternally-derived in heterozygotes but not when paternally-derived.
CONCLUSIONS
The interaction of sense and antisense transcripts can be interpreted as a form of communication between maternally-derived and paternally-derived RTL1 alleles that possesses many of the features of a greenbeard effect. This interaction is evolutionary stable, unlike a typical greenbeard effect, because of the necessary complementarity between microRNAs and mRNA transcribed from opposite strands of the same double helix. We conjecture that microRNAs and mRNA cooperate to reduce demands on mothers when an allele is paired with itself in homozygous offspring.
REVIEWERS
This article was reviewed by Eugene Berezikov and Bernard Crespi.

Identifiants

pubmed: 31640745
doi: 10.1186/s13062-019-0250-0
pii: 10.1186/s13062-019-0250-0
pmc: PMC6805670
doi:

Substances chimiques

MicroRNAs 0
Pregnancy Proteins 0
RTL1 protein, human 0
Retroelements 0
Rtl1 protein, mouse 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

18

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Auteurs

Avantika Mainieri (A)

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.

David Haig (D)

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA. dhaig@oeb.harvard.edu.

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Classifications MeSH