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Comprehensive mapping of transposable elements reveals distinct patterns of element accumulation on chromosomes of wild beetles

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Abstract

Over the past decades, transposable elements (TEs) have been shown to play important roles shaping genome architecture and as major promoters of genetic diversification and evolution of species. Likewise, TE accumulation is tightly linked to heterochromatinization and centromeric dynamics, which can ultimately contribute to speciation. Despite growing efforts to characterize the repeat landscape of species, few studies have focused on mapping the accumulation profiles of TEs on chromosomes. The few studies on repeat accumulation profiles in populations are biased towards model organisms and inbred lineages. Here, we present a cytomolecular analysis of six mobilome-extracted elements on multiple individuals from a population of a species of wild-captured beetle, Dichotomius schiffleri, aiming to investigate patterns of TE accumulation and uncover possible trends of their chromosomal distribution. Compiling TE distribution data from several individuals allowed us to make generalizations regarding variation of TEs at the gross chromosome level unlikely to have been achieved using a single individual, or even from a whole-genome assembly. We found that (1) transposable elements have differential accumulation profiles on D. schiffleri chromosomes and (2) specific chromosomes have their own TE accumulation landscape. The remarkable variability of their genomic distribution suggests that TEs are likely candidates to contribute to the evolution of heterochromatin architecture and promote high genetic variability in species that otherwise display conserved karyotypes. Therefore, this variation likely contributed to genome evolution and species diversification in Dichotomius.

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Data availability

DNA sequences of the clones used in this study are deposited in GenBank (https://www.ncbi.nlm.nih.gov/nuccore/)

Abbreviations

TEs:

Transposable elements

TP:

Transposase region

RT:

Reverse transcriptase

FISH:

Fluorescence in situ hybridization

Xyr :

“Rod” configuration of sex chromosomes

IBAMA :

Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (Brazilian Institute of Environment and Renewable Natural Resources)

SISBIO :

Sistema de Autorização e Informação em Biodiversidade (Biodiversity Authorization and Information System)

CAPES:

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (Brazilian Funding Organization - Coordination for the Improvement of Higher Education Personnel)

PNPD:

National Postdoctoral Program

FACEPE:

Fundação de Amparo a Ciência e Tecnologia do Estado de Pernambuco (Brazilian Funding Organization - Science and Technology Foundation of the State of Pernambuco)

CNPq:

Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brazilian Funding Organization - National Council for Scientific and Technological Development)

LBGI :

Laboratório de Biodiversidade e Genética de Insetos (Biodiversity and Insect Genetics Laboratory)

References

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Code availability

Accession codes of GenBank: MT636862, MT636863, MT636866, MT636868, MT636869 and MT636871.

Funding

Costa RGCC was supported with a Master’s scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES); Sotero-Caio CG and Amorim IC were supported with postdoctoral fellowships PNPD/CAPES, process numbers 88882.306325/2018-01 and 88882.317331/2019-01, respectively. This work was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) with the grant PQ-2 to Moura RC, process number 305298/2014-3; and by Fundação de Amparo à Ciência e Tecnologia de Pernambuco (FACEPE), APQ process number 0777-2.02/15.

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Authors

Contributions

ICA performed research, analyzed the data, produced the images, and helped writing of the manuscript; CGSC helped analyzing the data and wrote the paper; RGCC performed all FISH experiments, helped analyzing the data, and helped writing the first version of the manuscript; CX performed research, analyzed the data, and helped writing of the manuscript; RCM conceived and designed the study and analyzed the data and helped writing of the manuscript. All authors read and approve the manuscript submission

Corresponding author

Correspondence to Rita de Cássia de Moura.

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The authors declare no competing interests.

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Responsible Editor: Andreas Houben

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Amorim, I.C., Sotero-Caio, C.G., Costa, R.G.C. et al. Comprehensive mapping of transposable elements reveals distinct patterns of element accumulation on chromosomes of wild beetles. Chromosome Res 29, 203–218 (2021). https://doi.org/10.1007/s10577-021-09655-4

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  • DOI: https://doi.org/10.1007/s10577-021-09655-4

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