Abstract

BackgroundThe evolution of animal mitochondrial (mt) genomes has resulted in a highly conserved structure: a single compact circular chromosome approximately 14 to 20 kb long. Within the last two decades exceptions to this conserved structure, such as the division of the genome into multiple chromosomes, have been reported in a diverse set of metazoans. We report on the two circle multipartite mt genome of a newly described cyst nematode, Globodera ellingtonae.ResultsThe G. ellingtonae mt genome was found to be comprised of two circles, each larger than any other multipartite circular mt chromosome yet reported, and both were larger than the single mt circle of the model nematode Caenorhabditis elegans. The genetic content of the genome was disproportionately divided between the two circles, although they shared a ~6.5 kb non-coding region. The 17.8 kb circle (mtDNA-I) contained ten protein-coding genes and two tRNA genes, whereas the 14.4 kb circle (mtDNA-II) contained two protein-coding genes, 20 tRNA genes and both rRNA genes. Perhaps correlated with this division of genetic content, the copy number of mtDNA-II was more than four-fold that of mtDNA-I in individual nematodes. The difference in copy number increased between second-stage and fourth-stage juveniles.ConclusionsThe segregation of gene types to different mt circles in G. ellingtonae could provide benefit by localizing gene functional types to independent transcriptional units. This is the first report of both two-circle and several-circle mt genomes within a single genus. The differential copy number associated with this multipartite mt organization could provide a model system for deconstructing mechanisms regulating mtDNA copy number both in somatic cells and during germline development.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3047-x) contains supplementary material, which is available to authorized users.

Highlights

  • The evolution of animal mitochondrial genomes has resulted in a highly conserved structure: a single compact circular chromosome approximately 14 to 20 kb long

  • Almost all metazoan mt genomes are composed of the same 12 to 13 electron transport chain (ETC) protein-coding genes, and the two ribosomal RNA and 22 transfer RNA genes used for the synthesis of those proteins

  • To begin to address that question, and as part of a broader genomic analysis of G. ellingtonae, we investigated the structure of the mt genome of this nematode

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Summary

Introduction

The evolution of animal mitochondrial (mt) genomes has resulted in a highly conserved structure: a single compact circular chromosome approximately 14 to 20 kb long. Almost all metazoan mt genomes are composed of the same 12 to 13 electron transport chain (ETC) protein-coding genes, and the two ribosomal RNA (rRNA) and 22 transfer RNA (tRNA) genes used for the synthesis of those proteins The order of these genes, is highly variable and sometimes even radically different between species in the same genus [1]. Individual genes must remain functionally intact for effective energy production by mitochondria Both small (e.g. point mutations) and large abnormalities (e.g. large-scale deletions) in mt genomes are known contributors to various human diseases, such as maternally-inherited Leigh syndrome and Kearns-Sayre syndrome [2]. By investigating cases of unusual metazoan mtDNA structure, we may gain insight into the maintenance of normal mtDNA and factors leading to disease associated abnormalities

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