Hitchhiking on chromosomes: A persistence strategy shared by diverse selfish DNA elements

Sau, Soumitra; Ghosh, Santanu; Liu, Yen-Ting; Ma, Chien-Hui; Jayaram, Makkuni

doi:10.1016/j.plasmid.2019.01.004

Cited by 16 publications

(22 citation statements)

References 101 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Such mechanisms have been uncovered in other eukaryotic, non-microalgal species. For example, maintenance of viral episomes in mammalian cells and plasmids in S. cerevisiae have been attributed to chromosome tethering and hitchhiking mechanisms (Ghosh et al, 2007;Liu et al, 2008;McBride, 2008;Sau et al, 2019). In yeast synthetic biology research, episomal DNA sequences have been characterised based on traits including transformation efficiency, copy number, transgene expression and plasmid stability of clonal populations (Bouton and Smith, 1986;Nakamura et al, 2018;Gu et al, 2019).…”

Section: Clonal Variegation Is Broadly Distributed In Ee But Discretementioning

confidence: 99%

Metabolic Engineering Strategies in Diatoms Reveal Unique Phenotypes and Genetic Configurations With Implications for Algal Genetics and Synthetic Biology

George

Kahlke

Abbriano

et al. 2020

Front. Bioeng. Biotechnol.

View full text Add to dashboard Cite

Section: Clonal Variegation Is Broadly Distributed In Ee But Discretementioning

confidence: 99%

Metabolic Engineering Strategies in Diatoms Reveal Unique Phenotypes and Genetic Configurations With Implications for Algal Genetics and Synthetic Biology

George

Kahlke

Abbriano

et al. 2020

Front. Bioeng. Biotechnol.

View full text Add to dashboard Cite

“…The multi-copy 2-micron plasmid of Saccharomyces cerevisiae, present as 40-60 molecules per haploid genome content, is the most well characterized among yeast DNA plasmids [11][12][13][14]. Current evidence suggests that plasmid molecules are organized into clusters of 3-5 foci that act as units of segregation during cell division [15][16][17].…”

Section: Introductionmentioning

confidence: 99%

“…The plasmid genome has a bi-partite functional organization, namely, a replication-partitioning module and a copy number amplification module. Plasmid molecules duplicated by the host replication machinery [18] are segregated equally (or nearly so) to daughter cells by the plasmid-coded Rep1 and Rep2 proteins acting in conjunction with the cis-acting STB locus [12][13][14]. The Flp site-specific recombination/amplification system housed by the plasmid compensates for copy number reduction resulting from rare missegregation events.…”

Section: Introductionmentioning

confidence: 99%

The selfish yeast plasmid utilizes the condensin complex and condensed chromatin for faithful partitioning

et al. 2021

Self Cite

View full text Add to dashboard Cite

Equipartitioning by chromosome association and copy number correction by DNA amplification are at the heart of the evolutionary success of the selfish yeast 2-micron plasmid. The present analysis reveals frequent plasmid presence near telomeres (TELs) and centromeres (CENs) in mitotic cells, with a preference towards the former. Inactivation of Cdc14 causes plasmid missegregation, which is correlated to the non-disjunction of TELs (and of rDNA) under this condition. Induced missegregation of chromosome XII, one of the largest yeast chromosomes which harbors the rDNA array and is highly dependent on the condensin complex for proper disjunction, increases 2-micron plasmid missegregation. This is not the case when chromosome III, one of the smallest chromosomes, is forced to missegregate. Plasmid stability decreases when the condensin subunit Brn1 is inactivated. Brn1 is recruited to the plasmid partitioning locus (STB) with the assistance of the plasmid-coded partitioning proteins Rep1 and Rep2. Furthermore, in a dihybrid assay, Brn1 interacts with Rep1-Rep2. Taken together, these findings support a role for condensin and/or condensed chromatin in 2-micron plasmid propagation. They suggest that condensed chromosome loci are among favored sites utilized by the plasmid for its chromosome-associated segregation. By homing to condensed/quiescent chromosome locales, and not over-perturbing genome homeostasis, the plasmid may minimize fitness conflicts with its host. Analogous persistence strategies may be utilized by other extrachromosomal selfish genomes, for example, episomes of mammalian viruses that hitchhike on host chromosomes for their stable maintenance.

show abstract

“…The yeast 2-micron plasmid, nearly ubiquitous among Saccharomyces yeast strains, is a highly optimized extrachromosomal selfish DNA element [1–4]. The plasmid resides in the nucleus, offers no apparent fitness advantage to its host, and does not impose any significant disadvantage at its normal copy number of 40–60 molecules per haploid chromosome set.…”

Section: Introductionmentioning

confidence: 99%

A Flp-SUMO hybrid recombinase reveals multi-layered copy number control of a selfish DNA element through post-translational modification

Su²,

Maciaszek

et al. 2019

PLoS Genet

Self Cite

View full text Add to dashboard Cite

Mechanisms for highly efficient chromosome-associated equal segregation, and for maintenance of steady state copy number, are at the heart of the evolutionary success of the 2-micron plasmid as a stable multi-copy extra-chromosomal selfish DNA element present in the yeast nucleus. The Flp site-specific recombination system housed by the plasmid, which is central to plasmid copy number maintenance, is regulated at multiple levels. Transcription of the FLP gene is fine-tuned by the repressor function of the plasmid-coded partitioning proteins Rep1 and Rep2 and their antagonist Raf1, which is also plasmid-coded. In addition, the Flp protein is regulated by the host’s post-translational modification machinery. Utilizing a Flp-SUMO fusion protein, which functionally mimics naturally sumoylated Flp, we demonstrate that the modification signals ubiquitination of Flp, followed by its proteasome-mediated degradation. Furthermore, reduced binding affinity and cooperativity of the modified Flp decrease its association with the plasmid FRT (Flp recombination target) sites, and/or increase its dissociation from them. The resulting attenuation of strand cleavage and recombination events safeguards against runaway increase in plasmid copy number, which is deleterious to the host—and indirectly—to the plasmid. These results have broader relevance to potential mechanisms by which selfish genomes minimize fitness conflicts with host genomes by holding in check the extra genetic load they pose.

show abstract

Hitchhiking on chromosomes: A persistence strategy shared by diverse selfish DNA elements

Cited by 16 publications

References 101 publications

Metabolic Engineering Strategies in Diatoms Reveal Unique Phenotypes and Genetic Configurations With Implications for Algal Genetics and Synthetic Biology

Metabolic Engineering Strategies in Diatoms Reveal Unique Phenotypes and Genetic Configurations With Implications for Algal Genetics and Synthetic Biology

The selfish yeast plasmid utilizes the condensin complex and condensed chromatin for faithful partitioning

A Flp-SUMO hybrid recombinase reveals multi-layered copy number control of a selfish DNA element through post-translational modification

Contact Info

Product

Resources

About