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Published on: September 11, 2022
Horizontally transferred mitochondrial DNA tracts become circular by microhomology-mediated repair pathways
M Emilia Roulet1, Luis Federico Ceriotti1,2, Leonardo Gatica-Soria1,2
1IBAM, Universidad Nacional de Cuyo, CONICET, Facultad de Ciencias Agrarias, Almirante Brown 500, Chacras de Coria, M5528AHB, Mendoza, Argentina.
Abstract:
The holoparasitic plant Lophophytum mirabile exhibits remarkable levels of mitochondrial horizontal gene transfer (HGT). Gathering comparative data from other individuals and host plants can provide insights into the HGT process. We sequenced the mitochondrial genome (mtDNA) from individuals of two species of Lophophytum and from mimosoid hosts. We applied a stringent phylogenomic approach to elucidate the origin of the whole mtDNAs, estimate the timing of the transfers, and understand the molecular mechanisms involved. Ancestral and recent HGT events replaced and enlarged the multichromosomal mtDNA of Lophophytum spp., with the foreign DNA ascending to 74%. A total of 14 foreign mitochondrial chromosomes originated from continuous regions in the host mtDNA flanked by short direct repeats. These foreign tracts are circularized by microhomology-mediated repair pathways and replicate independently until they are lost or they eventually recombine with other chromosomes. The foreign noncoding chromosomes are variably present in the population and likely evolve by genetic drift. We present the 'circle-mediated HGT' model in which foreign mitochondrial DNA tracts become circular and are maintained as plasmid-like molecules. This model challenges the conventional belief that foreign DNA must be integrated into the recipient genome for successful HGT.
Insights
Horizontal gene transfer (HGT) in Lophophytum plants involves foreign mitochondrial DNA (mtDNA) forming independent circular molecules. This "circle-mediated HGT" challenges traditional integration models for genetic material transfer.
Area of Science:
- Plant genomics
- Mitochondrial genetics
- Horizontal gene transfer
Background:
- The holoparasitic plant Lophophytum mirabile shows extensive mitochondrial horizontal gene transfer (HGT).
- Understanding HGT mechanisms requires comparative data from related species and their hosts.
Purpose of the Study:
- To investigate the origin and timing of mitochondrial HGT in Lophophytum species.
- To elucidate the molecular mechanisms driving extensive HGT in plant mitochondria.
- To propose a novel model for mitochondrial HGT.
Main Methods:
- Sequencing of mitochondrial genomes (mtDNA) from Lophophytum species and mimosoid hosts.
- Application of stringent phylogenomic analyses to trace gene origins.
- Investigation of DNA repair pathways involved in foreign DNA integration.
Main Results:
- Ancestral and recent HGT events significantly altered Lophophytum spp. mtDNA, with foreign DNA comprising up to 74%.
- Fourteen foreign mitochondrial chromosomes originated from host mtDNA, flanked by direct repeats and circularized.
- Foreign noncoding chromosomes exist independently and are subject to genetic drift.
Conclusions:
- A novel 'circle-mediated HGT' model is proposed, where foreign DNA forms independent, plasmid-like circular molecules.
- This model suggests successful HGT does not require integration into the recipient genome.
- The findings challenge conventional understanding of gene transfer mechanisms in eukaryotes.
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