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Open Access Research article

An evolutionary preserved intergenic spacer in gadiform mitogenomes generates a long noncoding RNA

Tor Erik Jørgensen1, Ingrid Bakke2, Anita Ursvik3, Morten Andreassen3, Truls Moum1 and Steinar D Johansen13*

Author Affiliations

1 Marine Genomics group, Faculty of Biosciences and Aquaculture, University of Nordland, Bodø, Norway

2 Department of Biotechnology, Norwegian University of Science and Technology, Trondheim, Norway

3 Department of Medical Biology, Faculty of Health Sciences, UiT – Norwegian Arctic University, MH-building Breivika, Tromsø, N-9037, Norway

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BMC Evolutionary Biology 2014, 14:182  doi:10.1186/s12862-014-0182-3

Published: 22 August 2014

Abstract

Background

Vertebrate mitogenomes are economically organized and usually lack intergenic sequences other than the control region. Intergenic spacers located between the tRNAThr and tRNAPro genes (“T-P spacers”) have been observed in several taxa, including gadiform species, but information about their biological roles and putative functions is still lacking.

Results

Sequence characterization of the complete European hake Merluccius merluccius mitogenome identified a complex T-P spacer ranging in size from 223–532 bp. Further analyses of 32 gadiform species, representing 8 families and 28 genera, revealed the evolutionary preserved presence of T-P spacers across all taxa. Molecular complexity of the T-P spacers was found to be coherent with the phylogenetic relationships, supporting a common ancestral origin and gain of function during codfish evolution. Intraspecific variation of T-P spacer sequences was assessed in 225 Atlantic cod specimens and revealed 26 haplotypes. Pyrosequencing data representing the mito-transcriptome poly (A) fraction in Atlantic cod identified an abundant H-strand specific long noncoding RNA of about 375 nt. The T-P spacer corresponded to the 5’ part of this transcript, which terminated within the control region in a tail-to-tail configuration with the L-strand specific transcript (the 7S RNA).

Conclusions

The T-P spacer is inferred to be evolutionary preserved in gadiform mitogenomes due to gain of function through a long noncoding RNA. We suggest that the T-P spacer adds stability to the H-strand specific long noncoding RNA by forming stable hairpin structures and additional protein binding sites.

Keywords:
Atlantic cod; European hake; Heteroplasmy; lncRNA; Mitogenome