Abstract

BackgroundAlthough horizontal gene transfer (HGT) is a widely accepted force in the evolution of prokaryotic genomes, its role in the evolution of eukaryotic genomes remains hotly debated. Some bdelloid rotifers that are resistant to extreme desiccation and radiation undergo a very high level of HGT, whereas in another desiccation-resistant invertebrate, the tardigrade, the pattern does not exist. Overall, the DNA double-strand breaks (DSBs) induced by prolonged desiccation have been postulated to open a gateway to the nuclear genome for exogenous DNA integration and thus to facilitate the HGT process, thereby enhancing the rate of endosymbiotic DNA transfer (EDT).ResultsWe first surveyed the abundance of nuclear mitochondrial DNAs (NUMTs) and nuclear plastid DNAs (NUPTs) in five eukaryotes that are highly resistant to desiccation: the bdelloid rotifers Adineta vaga and Adineta ricciae, the tardigrade Ramazzottius varieornatus, and the resurrection plants Dorcoceras hygrometricum and Selaginella tamariscina. Excessive NUMTs or NUPTs were not detected. Furthermore, we compared 24 groups of desiccation-tolerant organisms with their relatively less desiccation-tolerant relatives but did not find a significant difference in NUMT/NUPT contents.ConclusionsDesiccation may induce DSBs, but it is unlikely to dramatically increase the frequency of exogenous sequence integration in most eukaryotes. The capture of exogenous DNA sequences is possible only when DSBs are repaired through a subtype of non-homologous end joining, named alternative end joining (alt-EJ). Due to the deleterious effects of the resulting insertion mutations, alt-EJ is less frequently initiated than other mechanisms.

Highlights

  • Horizontal gene transfer (HGT) is a widely accepted force in the evolution of prokaryotic genomes, its role in the evolution of eukaryotic genomes remains hotly debated

  • Mitochondrial DNA segments recently inserted into nuclear genomes are termed nuclear mitochondrial DNAs (NUMTs), whereas plastid DNA segments recently inserted into nuclear genomes are termed nuclear plastid DNAs (NUPTs)

  • For a trade-off between genome quality and sample size, we evaluated the effects of genome assembly level on the detected abundances of NUMTs/NUPTs using a phylogenetic comparative method, phylogenetic generalized least squares (PGLS)

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Summary

Introduction

Horizontal gene transfer (HGT) is a widely accepted force in the evolution of prokaryotic genomes, its role in the evolution of eukaryotic genomes remains hotly debated. Horizontal gene transfer (HGT, termed lateral gene transfer) is the movement of genetic materials between organisms rather than from parent to offspring [1, 2]. Compared with HGT, gene transfer from the organellar genome to the nuclear genome, termed endosymbiotic gene transfer (EGT), has been widely observed and well accepted in eukaryotes [2, 18, 19]. The effective transfer of functional protein-coding genes has slowed or even stopped in some lineages, the process of DNA fragment transfer from organelle to nucleus still actively occurs in most eukaryotic lineages [19,20,21,22]. NUMTs and NUPTs are collectively termed nuclear organelle DNA (norgDNA) [23]

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