Rampant nuclear insertion of mtDNA across diverse lineages within Orthoptera (Insecta).

Matthew J Moulton,Michael F Whiting,Hojun Song

doi:10.1371/journal.pone.0110508

Matthew J Moulton, Michael F Whiting + Show 1 more

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https://doi.org/10.1371/journal.pone.0110508

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Abstract

Nuclear mitochondrial pseudogenes (numts) are non-functional fragments of mtDNA inserted into the nuclear genome. Numts are prevalent across eukaryotes and a positive correlation is known to exist between the number of numts and the genome size. Most numt surveys have relied on model organisms with fully sequenced nuclear genomes, but such analyses have limited utilities for making a generalization about the patterns of numt accumulation for any given clade. Among insects, the order Orthoptera is known to have the largest nuclear genome and it is also reported to include several species with a large number of numts. In this study, we use Orthoptera as a case study to document the diversity and abundance of numts by generating numts of three mitochondrial loci across 28 orthopteran families, representing the phylogenetic diversity of the order. We discover that numts are rampant in all lineages, but there is no discernable and consistent pattern of numt accumulation among different lineages. Likewise, we do not find any evidence that a certain mitochondrial gene is more prone to nuclear insertion than others. We also find that numt insertion must have occurred continuously and frequently throughout the diversification of Orthoptera. Although most numts are the result of recent nuclear insertion, we find evidence of very ancient numt insertion shared by highly divergent families dating back to the Jurassic period. Finally, we discuss several factors contributing to the extreme prevalence of numts in Orthoptera and highlight the importance of exploring the utility of numts in evolutionary studies.

Highlights

It has been twenty years since the coining of the term ‘‘numts’’to refer to nuclear mitochondrial pseudogenes [1], which are nonfunctional fragments of mtDNA inserted into the nucleus [2].Initially considered abnormal and rare [3,4], numts have since been reported from many divergent lineages of eukaryotes [2,5,6]and it is predicted that as more genomes are sequenced more numts will be discovered [5]
Among c oxidase subunit 2 (COII)-like numts, we found two clades, one of which consisted of numts from Lentula (Lentulidae), Prionotropis (Pamphagidae), and Ellipes (Tridactylidae), and another clade consisting of numts from Lentula and Prionotropis
We show that numts of multiple mitochondrial genes (COI, COII, and NADH dehydrogenase subunit 5 (ND5)) are extremely prevalent in every single family examined, representing members of all 14 known superfamilies across Orthoptera

Summary

Introduction

It has been twenty years since the coining of the term ‘‘numts’’to refer to nuclear mitochondrial pseudogenes [1], which are nonfunctional fragments of mtDNA inserted into the nucleus [2].Initially considered abnormal and rare [3,4], numts have since been reported from many divergent lineages of eukaryotes [2,5,6]and it is predicted that as more genomes are sequenced more numts will be discovered [5]. To refer to nuclear mitochondrial pseudogenes [1], which are nonfunctional fragments of mtDNA inserted into the nucleus [2]. It has been well documented that mtDNA frequently escapes to the nucleus [7,8,9,10], and these mitochondrial fragments can be inserted into the chromosome during the repair of double-strand breaks in a mechanism known as non-homologous end-joining [11,12]. Once inserted into the nuclear genome, numts become non-functional because of the differences in genetic code between mitochondrial and nuclear genomes [2,8,13]. 21], the exact mechanism of numt insertion and subsequent maintenance is still not fully understood [5]. Numts can be coamplified with mtDNA using conserved primers via conventional polymerase chain reactions [10,22,23,24,25,26,27,28]

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