The transcription factor Atf1 lowers the transition barrier for nucleosome-mediated establishment of heterochromatin

Fission yeasts are an ancient group of fungal species that diverged from each other from tens to hundreds of million years ago. Among them is the preeminent model organism Schizosaccharomyces pombe, which has significantly contributed to our understandings of molecular mechanisms underlying fundamental cellular processes. The availability of the genomes of S. pombe and three other fission yeast species S. japonicus, S. octosporus, and S. cryophilus has enabled cross-species comparisons that provide insights into the evolution of genes, pathways, and genomes. Here, we performed genome sequencing on the type strain of the recently identified fission yeast species S. osmophilus and obtained a complete mitochondrial genome and a nuclear genome assembly with gaps only at rRNA gene arrays. A total of 5098 protein-coding nuclear genes were annotated and orthologs for more than 95% of them were identified. Genome-based phylogenetic analysis showed that S. osmophilus is most closely related to S. octosporus and these two species diverged around 16 million years ago. To demonstrate the utility of this S. osmophilus reference genome, we conducted cross-species comparative analyses of centromeres, telomeres, transposons, the mating-type region, Cbp1 family proteins, and mitochondrial genomes. These analyses revealed conservation of repeat arrangements and sequence motifs in centromere cores, identified telomeric sequences composed of two types of repeats, delineated relationships among Tf1/sushi group retrotransposons, characterized the evolutionary origins and trajectories of Cbp1 family domesticated transposases, and discovered signs of interspecific transfer of two types of mitochondrial selfish elements.

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Section: Resultsmentioning

confidence: 99%

A high-quality reference genome for the fission yeast Schizosaccharomyces osmophilus

Jia

Zhang

Liang

et al. 2023

G3: Genes, Genomes, Genetics

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“…In S. pombe, two 8-bp Atf1-binding sites (ATGACGTA) located in the donor region, called s1 and s2, act redundantly with the RNAi pathway to promote the establishment of the donor region heterochromatin (Thon et al 1999;Nickels et al 2022). Our inspection of the donor region sequences of the other four fission yeast species showed that there are two, two, and four ATGACGTA sequences in the donor regions of S. cryophilus, S. osmophilus, and S. octosporus, respectively (Figure 5A).…”

Section: Cross-species Comparisons Of the Mating-type Regionmentioning

confidence: 99%

A high-quality reference genome for the fission yeastSchizosaccharomyces osmophilus

Jia

Zhang

Liang

et al. 2022

Preprint

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Fission yeasts are an ancient group of fungal species that diverged from each other from tens to hundreds of million years ago. Among them is the preeminent model organismSchizosaccharomyces pombe, which has significantly contributed to our understandings of molecular mechanisms underlying fundamental cellular processes. The availability of the genomes ofS. pombeand three other fission yeast speciesS. japonicus,S. octosporus, andS. cryophilushas enabled cross-species comparisons that provide insights into the evolution of genes, pathways, and genomes. Here, we performed genome sequencing on the type strain of the recently identified fission yeast speciesS. osmophilusand obtained a complete mitochondrial genome and a nuclear genome assembly with gaps only at rRNA gene arrays. A total of 5098 protein-coding nuclear genes were annotated and orthologs for more than 95% of them were identified. Genome-based phylogenetic analysis showed thatS. osmophilusis most closely related toS. octosporusand these two species diverged around 16 million years ago. To demonstrate the utility of thisS. osmophilusreference genome, we conducted cross-species comparative analyses of centromeres, telomeres, transposons, the mating-type region, Cbp1 family proteins, and mitochondrial genomes. These analyses revealed conservation of repeat arrangements and sequence motifs in centromere cores, identified telomeric sequences composed of two types of repeats, delineated relationships among Tf1/sushi group retrotransposons, characterized the evolutionary origins and trajectories of Cbp1 family domesticated transposases, and discovered signs of interspecific transfer of two types of mitochondrial selfish elements.

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“…; https://doi.org/10.1101/2023.03. 27.534317 doi: bioRxiv preprint recruit Clr4 to nucleate heterochromatin at these regions [16,[18][19][20][21][22][23][24]. The intrinsic capacities of Clr4 to both recognize H3K9me and methylate adjacent nucleosomes define the molecular basis of a "read-write" mechanism by which heterochromatin subsequently propagates throughout entire domains [25][26][27][28].…”

Section: Introductionmentioning

confidence: 99%

A dual, catalytic role for the fission yeast Ccr4-Not complex in gene silencing and heterochromatin spreading

Challal

Menant

Goksal

et al. 2023

Preprint

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Heterochromatic gene silencing relies on combinatorial control by specific histone modifications, the occurrence of transcription, and/or RNA degradation. Once nucleated, heterochromatin propagates within defined chromosomal regions and is maintained throughout cell divisions to warrant proper genome expression and integrity. The fission yeast Ccr4-Not complex has been involved in gene silencing, but its relative contribution to distinct heterochromatin domains and its role in nucleation versus spreading have remained elusive. Here, we unveil major functions for Ccr4-Not in silencing and heterochromatin spreading at the mating type locus and subtelomeres. Mutations of the catalytic subunits Caf1 or Mot2, involved in RNA deadenylation and protein ubiquitinylation respectively, result in impaired propagation of H3K9me3 and massive accumulation of nucleation-distal heterochromatic transcripts. Both silencing and spreading defects are suppressed upon disruption of the heterochromatin antagonizing factor Epe1. Overall, our results position the Ccr4-Not complex as a critical, dual regulator of heterochromatic gene silencing and spreading.

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The transcription factor Atf1 lowers the transition barrier for nucleosome-mediated establishment of heterochromatin

Cited by 15 publications

References 60 publications

A high-quality reference genome for the fission yeast Schizosaccharomyces osmophilus

A high-quality reference genome for the fission yeast Schizosaccharomyces osmophilus

A high-quality reference genome for the fission yeastSchizosaccharomyces osmophilus

A dual, catalytic role for the fission yeast Ccr4-Not complex in gene silencing and heterochromatin spreading

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