Subtelomeric Transcription and its Regulation

Kwapisz, Marta; Morillon, Antonin

doi:10.1016/j.jmb.2020.01.026

Cited by 34 publications

(34 citation statements)

References 186 publications

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“…Besides, the Suber elements and the Spacer sequences are transcribed. These putatively non-coding but spliced and polyadenylated transcripts are similar to sub-TERRA and other subtelomeric transcripts, as described in multiple organisms (Azzalin and Lingner 2015;Kwapisz and Morillon 2020), with potential functions in telomere maintenance that remain to be investigated. The 5¢ part of the Spacer element functions as a promoter, active essentially at dusk and during the first phase of night in a light-dark cycle, concomitantly with replication and histone deposition (Strenkert et al 2019).…”

Section: A Comprehensive Description Of the Architecture Of Subtelomeres In C Reinhardtiimentioning

confidence: 75%

Architecture and evolution of subtelomeres in the unicellular green algaChlamydomonas reinhardtii

Chaux-Jukic

O’Donnell

Craig

et al. 2021

Preprint

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In most eukaryotes, subtelomeres are dynamic genomic regions populated by multi-copy sequences of different origins, which can promote segmental duplications and chromosomal rearrangements. However, their repetitive nature has complicated the efforts to sequence them, analyze their structure and infer how they evolved. Here, we use recent and forthcoming genome assemblies of Chlamydomonas reinhardtii based on long-read sequencing to comprehensively describe the subtelomere architecture of the 17 chromosomes of this model unicellular green alga. We identify three main repeated elements present at subtelomeres, which we call Sultan, Subtile and Suber, alongside three chromosome extremities with ribosomal DNA as the only identified component of their subtelomeres. The most common architecture, present in 27 out of 34 subtelomeres, is an array of 1 to 46 tandem copies of Sultan elements adjacent to the telomere and followed by a transcribed centromere-proximal Spacer sequence, a G-rich microsatellite and a region rich in transposable elements. Sequence similarity analyses suggest that Sultan elements underwent segmental duplications within each subtelomere and rearranged between subtelomeres at a much lower frequency. Comparison of genomic sequences of three laboratory strains and a wild isolate of C. reinhardtii shows that the overall subtelomeric architecture was already present in their last common ancestor, although subtelomeric rearrangements are on-going at the species level. Analysis of other green algae reveals the presence of species-specific repeated elements, highly conserved across subtelomeres and unrelated to the Sultan element, but with a subtelomere structure similar to C. reinhardtii. Overall, our work uncovers the complexity and evolution of subtelomere architecture in green algae.

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Section: A Comprehensive Description Of the Architecture Of Subtelomeres In C Reinhardtiimentioning

confidence: 75%

Architecture and evolution of subtelomeres in the unicellular green algaChlamydomonas reinhardtii

Chaux-Jukic

O’Donnell

Craig

et al. 2021

Preprint

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“…The downstream region of the subtelomere is transcribed and no longer methylated, thus defining a euchromatic domain, which encompasses all TEs and distal subtelomeric genes. The putatively non-coding but spliced and polyadenylated transcripts emanating from the Spacer are similar to sub-TERRA and other subtelomeric transcripts, as described in multiple organisms ( 29 , 92 ), with potential functions in telomere maintenance that remain to be investigated.…”

Section: Discussionmentioning

confidence: 95%

Architecture and evolution of subtelomeres in the unicellular green algaChlamydomonas reinhardtii

Chaux-Jukic

O’Donnell

Craig

et al. 2021

Nucleic Acids Research

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In most eukaryotes, subtelomeres are dynamic genomic regions populated by multi-copy sequences of different origins, which can promote segmental duplications and chromosomal rearrangements. However, their repetitive nature has complicated the efforts to sequence them, analyse their structure and infer how they evolved. Here, we use recent genome assemblies of Chlamydomonas reinhardtii based on long-read sequencing to comprehensively describe the subtelomere architecture of the 17 chromosomes of this model unicellular green alga. We identify three main repeated elements present at subtelomeres, which we call Sultan, Subtile and Suber, alongside three chromosome extremities with ribosomal DNA as the only identified component of their subtelomeres. The most common architecture, present in 27 out of 34 subtelomeres, is a heterochromatic array of Sultan elements adjacent to the telomere, followed by a transcribed Spacer sequence, a G-rich microsatellite and transposable elements. Sequence similarity analyses suggest that Sultan elements underwent segmental duplications within each subtelomere and rearranged between subtelomeres at a much lower frequency. Analysis of other green algae reveals species-specific repeated elements that are shared across subtelomeres, with an overall organization similar to C. reinhardtii. This work uncovers the complexity and evolution of subtelomere architecture in green algae.

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“…Genes near these regions are subject to transcriptional repression, also known as position-effect variegation, which is highly conserved in higher organisms 3 , 4 . The proper organization of this transcriptionally silent heterochromatin is important to maintain telomere length, genome integrity, and chromosome segregation fidelity 5 , 6 . Disruption or loss of silent chromatin may lead to chromosomal instability, a hallmark and causal factor of tumorigenesis and cell aging 6 – 10 .…”

Section: Introductionmentioning

confidence: 99%

Metabolic regulation of telomere silencing by SESAME complex-catalyzed H3T11 phosphorylation

Zhang

et al. 2021

Nat Commun

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Telomeres are organized into a heterochromatin structure and maintenance of silent heterochromatin is required for chromosome stability. How telomere heterochromatin is dynamically regulated in response to stimuli remains unknown. Pyruvate kinase Pyk1 forms a complex named SESAME (Serine-responsive SAM-containing Metabolic Enzyme complex) to regulate gene expression by phosphorylating histone H3T11 (H3pT11). Here, we identify a function of SESAME in regulating telomere heterochromatin structure. SESAME phosphorylates H3T11 at telomeres, which maintains SIR (silent information regulator) complex occupancy at telomeres and protects Sir2 from degradation by autophagy. Moreover, SESAME-catalyzed H3pT11 directly represses autophagy-related gene expression to further prevent autophagy-mediated Sir2 degradation. By promoting H3pT11, serine increases Sir2 protein levels and enhances telomere silencing. Loss of H3pT11 leads to reduced Sir2 and compromised telomere silencing during chronological aging. Together, our study provides insights into dynamic regulation of silent heterochromatin by histone modifications and autophagy in response to cell metabolism and aging.

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Subtelomeric Transcription and its Regulation

Cited by 34 publications

References 186 publications

Architecture and evolution of subtelomeres in the unicellular green algaChlamydomonas reinhardtii

Architecture and evolution of subtelomeres in the unicellular green algaChlamydomonas reinhardtii

Architecture and evolution of subtelomeres in the unicellular green algaChlamydomonas reinhardtii

Metabolic regulation of telomere silencing by SESAME complex-catalyzed H3T11 phosphorylation

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