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Intact rDNA arrays of Potentilla-origin detected in Erythronium nucleus suggest recent eudicot-to-monocot horizontal transfer

View ORCID ProfileLászló Bartha, View ORCID ProfileTerezie Mandáková, View ORCID ProfileAleš Kovařík, View ORCID ProfilePaul-Adrian Bulzu, View ORCID ProfileNathalie Rodde, View ORCID ProfileVáclav Mahelka, View ORCID ProfileMartin A. Lysak, View ORCID ProfileMargaux-Alison Fustier, View ORCID ProfileJan Šafář, View ORCID ProfilePetr Cápal, View ORCID ProfileLujza Keresztes, View ORCID ProfileHoria L. Banciu
doi: https://doi.org/10.1101/2021.12.15.472635
László Bartha
aMolecular Biology Center, Interdisciplinary Research Institute on Bio-Nano-Sciences, Babeş-Bolyai University, 400271 Cluj-Napoca, Romania
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  • ORCID record for László Bartha
  • For correspondence: lbartha.ubbcluj@yahoo.com
Terezie Mandáková
bCentral European Institute of Technology (CEITEC), Masaryk University, 625 00 Brno, Czech Republic
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  • ORCID record for Terezie Mandáková
Aleš Kovařík
cLaboratory of Molecular Epigenetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, 61265 Brno, Czech Republic
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  • ORCID record for Aleš Kovařík
Paul-Adrian Bulzu
dDepartment of Aquatic Microbial Ecology, Institute of Hydrobiology, Biology Centre of the Academy of Sciences of the Czech Republic, 370 05 České Budějovice, Czech Republic
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Nathalie Rodde
eFrench Plant Genomic Resource Center, INRAE-CNRGV, 31320 Castanet Tolosan, France
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Václav Mahelka
fInstitute of Botany, Czech Academy of Sciences, 25243 Průhonice, Czech Republic
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  • ORCID record for Václav Mahelka
Martin A. Lysak
bCentral European Institute of Technology (CEITEC), Masaryk University, 625 00 Brno, Czech Republic
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  • ORCID record for Martin A. Lysak
Margaux-Alison Fustier
eFrench Plant Genomic Resource Center, INRAE-CNRGV, 31320 Castanet Tolosan, France
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  • ORCID record for Margaux-Alison Fustier
Jan Šafář
gInstitute of Experimental Botany of the Czech Academy of Sciences, Centre of the Region Haná for Biotechnological and Agricultural Research, 779 00 Olomouc, Czech Republic
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Petr Cápal
gInstitute of Experimental Botany of the Czech Academy of Sciences, Centre of the Region Haná for Biotechnological and Agricultural Research, 779 00 Olomouc, Czech Republic
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Lujza Keresztes
hHungarian Department of Biology and Ecology, Babeş-Bolyai University, 400006 Cluj-Napoca, Romania
iCentre of Systems Biology, Biodiversity and Bioresources (3B), Babeş-Bolyai University, 400006 Cluj-Napoca, Romania
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Horia L. Banciu
aMolecular Biology Center, Interdisciplinary Research Institute on Bio-Nano-Sciences, Babeş-Bolyai University, 400271 Cluj-Napoca, Romania
iCentre of Systems Biology, Biodiversity and Bioresources (3B), Babeş-Bolyai University, 400006 Cluj-Napoca, Romania
jDepartment of Molecular Biology and Biotechnology, Faculty of Biology and Geology, Babeş-Bolyai University, 400006 Cluj-Napoca, Romania
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Abstract

The occurrence of horizontal gene transfer (HGT) in Eukarya is increasingly gaining recognition. Nuclear-to-nuclear jump of DNA between plant species at high phylogenetic distance and devoid of intimate association (e.g., parasitism) is still scarcely reported. Within eukaryotes, components of ribosomal DNA (rDNA) multigene family have been found to be horizontally transferred in protists, fungi and grasses. However, in neither case HGT occurred between phylogenetic families, nor the transferred rDNA remained tandemly arrayed and transcriptionally active in the recipient organism. This study aimed to characterize an alien eudicot-type of 45S nuclear rDNA, assumingly transferred horizontally to the genome of monocot European Erythronium (Liliaceae). Genome skimming coupled by PacBio HiFi sequencing of a BAC clone were applied to determine DNA sequence of the alien rDNA. A clear phylogenetic signal traced the origin of the alien rDNA of Erythronium back to the Argentea clade of Potentilla (Rosaceae) and deemed the transfer to have occurred in the common ancestor of E. dens-canis and E. caucasicum. Though being discontinuous, transferred rDNA preserved its general tandemly arrayed feature in the host organism. Southern blotting, molecular cytogenetics, and sequencing of a BAC clone derived from flow-sorted nuclei indicated integration of the alien rDNA into the recipient’s nuclear genome. Unprecedently, dicot-type alien rDNA was found to be transcribed in the monocot Erythronium albeit much less efficiently than the native counterpart. This study adds a new example to the growing list of naturally transgenic plants while holding the scientific community continually in suspense about the mode of DNA transfer.

Significance Statement Ribosomal DNA is an essential component of all cellular genomes. In plants, accidental movement of rDNA via horizontal gene transfer has only been reported in sexually incompatible grasses (monocots) where it involved non-functional rDNA units. In this study, we propose that evolutionary trajectories of eudicots and monocots were bypassed by the jump of rDNA from a Potentilla species (Rosaceae) to a common ancestor of Erythronium dens-canis and E. caucasicum (Liliaceae). The alien eudicot-type rDNA appeared relatively well conserved in the examined host Erythronium genome, being able to be expressed while preserving its general tandemly repeated feature, evidences that have no match in earlier literature.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Competing Interest Statement: The authors declare no conflict of interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 16, 2021.
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Intact rDNA arrays of Potentilla-origin detected in Erythronium nucleus suggest recent eudicot-to-monocot horizontal transfer
László Bartha, Terezie Mandáková, Aleš Kovařík, Paul-Adrian Bulzu, Nathalie Rodde, Václav Mahelka, Martin A. Lysak, Margaux-Alison Fustier, Jan Šafář, Petr Cápal, Lujza Keresztes, Horia L. Banciu
bioRxiv 2021.12.15.472635; doi: https://doi.org/10.1101/2021.12.15.472635
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Intact rDNA arrays of Potentilla-origin detected in Erythronium nucleus suggest recent eudicot-to-monocot horizontal transfer
László Bartha, Terezie Mandáková, Aleš Kovařík, Paul-Adrian Bulzu, Nathalie Rodde, Václav Mahelka, Martin A. Lysak, Margaux-Alison Fustier, Jan Šafář, Petr Cápal, Lujza Keresztes, Horia L. Banciu
bioRxiv 2021.12.15.472635; doi: https://doi.org/10.1101/2021.12.15.472635

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