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High nucleotide substitution rates associated with retrotransposon proliferation drive dynamic secretome evolution in smut pathogens

JRL Depotter, B Ökmen, MK Ebert, J Beckers, Kruse Jb, M Thines, G Doehlemann
doi: https://doi.org/10.1101/2021.04.23.441129
JRL Depotter
aUniversity of Cologne, CEPLAS, Institute for Plant Sciences, Cologne, Germany
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B Ökmen
aUniversity of Cologne, CEPLAS, Institute for Plant Sciences, Cologne, Germany
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MK Ebert
aUniversity of Cologne, CEPLAS, Institute for Plant Sciences, Cologne, Germany
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J Beckers
aUniversity of Cologne, CEPLAS, Institute for Plant Sciences, Cologne, Germany
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Kruse Jb
cInstitute of Ecology, Evolution and Diversity, Goethe University Frankfurt, Frankfurt a. M., Germany
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M Thines
bSenckenberg Biodiversity and Climate Research Centre (BiK-F), Frankfurt a. M., Germany
cInstitute of Ecology, Evolution and Diversity, Goethe University Frankfurt, Frankfurt a. M., Germany
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G Doehlemann
aUniversity of Cologne, CEPLAS, Institute for Plant Sciences, Cologne, Germany
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  • For correspondence: g.doehlemann@uni-koeln.de
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Abstract

Transposable elements (TEs) play a pivotal role in shaping diversity in eukaryotic genomes. The covered smut pathogen on barley, Ustilago hordei, encountered a recent genome expansion. Using long reads, we assembled genomes of 6 U. hordei strains and 3 sister species, to study this genome expansion. We found that larger genome sizes can mainly be attributed to a higher genome fraction of long terminal repeat retrotransposons (LTR-RTs). In the studied smut genomes, LTR-RTs fractions are the largest in U. hordei and are positively correlated to the mating-type locus sizes, which is up to ∼560 kb in U. hordei. Furthermore, LTR-RTs were found to be associated with higher nucleotide substitution levels, as these higher levels occur more clustered in smut species with a recent LTR-RT proliferation. Moreover, genes in genome regions with higher nucleotide substitution levels generally reside closer to LTR-RTs than other genome regions. Genome regions with many nucleotide substitutions encountered an especially high fraction of CG substitutions, which is not observed for LTR-RT sequences. The high nucleotide substitution levels particularly accelerate the evolution of secretome genes, as their more flexible nature results that substitutions often lead to amino acid alterations.

Importance Genomic alteration can be generated through various means, in which transposable elements (TEs) can play a pivotal role. Their mobility causes mutagenesis in itself and can disrupt the function of the sequences they insert into. Indirectly, they also impact genome evolution as their repetitive nature facilitates non-homologous recombination. Furthermore, TEs have been linked to specific epigenetic genome organizations. We report a recent TE proliferation in the genome of the barley covered smut fungus, Ustilago hordei. This proliferation is associated with a distinct nucleotide substitution regime that has a higher rate and a higher fraction of CG substitutions. This different regime shapes the evolution of genes in subjected genome regions. Our findings highlight that TEs may influence the error-rate of DNA polymerase in a hitherto unknown fashion.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted January 09, 2022.
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High nucleotide substitution rates associated with retrotransposon proliferation drive dynamic secretome evolution in smut pathogens
JRL Depotter, B Ökmen, MK Ebert, J Beckers, Kruse Jb, M Thines, G Doehlemann
bioRxiv 2021.04.23.441129; doi: https://doi.org/10.1101/2021.04.23.441129
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High nucleotide substitution rates associated with retrotransposon proliferation drive dynamic secretome evolution in smut pathogens
JRL Depotter, B Ökmen, MK Ebert, J Beckers, Kruse Jb, M Thines, G Doehlemann
bioRxiv 2021.04.23.441129; doi: https://doi.org/10.1101/2021.04.23.441129

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