The selfish yeast plasmid exploits a SWI/SNF-type chromatin remodeling complex for hitchhiking on chromosomes and ensuring high-fidelity propagation

Extra-chromosomal selfish DNA elements can evade the risk of being lost at every generation by behaving as chromosome appendages, thereby ensuring high fidelity segregation and stable persistence in host cell populations. The yeast 2-micron plasmid and episomes of the mammalian gammaherpes and papil...

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Bibliographic Details
Published in:PLoS genetics 2023-10, Vol.19 (10), p.e1010986-e1010986
Main Authors: Ma, Chien-Hui, Kumar, Deepanshu, Jayaram, Makkuni, Ghosh, Santanu K, Iyer, Vishwanath R
Format: Article
Language:English
Subjects:
Analysis
Bias
Biology and Life Sciences
Cell cycle
Cell division
Cells
Chromatin
Chromatin remodeling
Chromosomes
Fidelity
Gene loci
Genomes
Genomics
Identification and classification
Localization
Noncoding DNA
Papilloma
Papillomavirus infections
Plasmids
Propagation
Proteins
Transfer RNA
Yeast
Yeast fungi
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Summary:Extra-chromosomal selfish DNA elements can evade the risk of being lost at every generation by behaving as chromosome appendages, thereby ensuring high fidelity segregation and stable persistence in host cell populations. The yeast 2-micron plasmid and episomes of the mammalian gammaherpes and papilloma viruses that tether to chromosomes and segregate by hitchhiking on them exemplify this strategy. We document for the first time the utilization of a SWI/SNF-type chromatin remodeling complex as a conduit for chromosome association by a selfish element. One principal mechanism for chromosome tethering by the 2-micron plasmid is the bridging interaction of the plasmid partitioning proteins (Rep1 and Rep2) with the yeast RSC2 complex and the plasmid partitioning locus STB. We substantiate this model by multiple lines of evidence derived from genomics, cell biology and interaction analyses. We describe a Rep-STB bypass system in which a plasmid engineered to non-covalently associate with the RSC complex mimics segregation by chromosome hitchhiking. Given the ubiquitous prevalence of SWI/SNF family chromatin remodeling complexes among eukaryotes, it is likely that the 2-micron plasmid paradigm or analogous ones will be encountered among other eukaryotic selfish elements.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1010986