Chromosome-associated RNA–protein complexes promote pairing of homologous chromosomes during meiosis in Schizosaccharomyces pombe

Ding, Da‐Qiao; Okamasa, Kasumi; Katou, Yuki; Oya, Eriko; Nakayama, Jun‐ichi; Chikashige, Yuji; Shirahige, Katsuhiko; Haraguchi, Tokuko; Hiraoka, Yasushi

doi:10.1038/s41467-019-13609-0

Cited by 55 publications

(78 citation statements)

References 49 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…It has been found that subunits of SC in C. elegans are sensitive to aliphatic alcohols, thus have a liquid-liquid phase separation property (Rog et al 2017). We have shown that lncRNA-protein complexes in S. pombe exhibit phase separation properties, since 1,6-hexanediol treatment reversibly disassembled these complexes and disrupted the pairing of associated loci while the Rec8 axis remained in this treatment (Ding et al 2019). We then examined that if LinE in S. pombe also has liquid droplet properties.…”

Section: The Line Is a Stable Structurementioning

confidence: 78%

“…No SC central element-like transverse element has ever been found in S. pombe. The only structures observed in between homologous chromosomes are lncRNA/RNA-transcription termination protein complexes, which are liquid-liquid phase separation droplets that play an essential role in the recognition and pairing of homologous chromosomes (Ding et al 2019). Since the liquid crystalline-like, transverse elements of SC may play a direct role in crossover interference (Rog et al 2017), and no crossover interference exists in S. pombe, LinEs on the chromosome axis may play roles in crossover control in a different way from that of SC (Loidl 2006;Yamada et al 2017).…”

Section: Stability Of Linesmentioning

confidence: 99%

See 1 more Smart Citation

The Linear Element is a Stable Structure Along the Chromosome Axis in Fission Yeast

Ding

Matsuda

Okamasa

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

AbstractChromosomes structure changes dramatically upon entering meiosis to ensure the successful progression of meiosis-specific events. During this process, a multilayer proteinaceous structure called synaptonemal complex (SC) is formed in many eukaryotes. Instead, in the fission yeast Schizosaccharomyces pombe, linear elements (LinEs), which are structures related to an axial element of SC, form on the meiotic cohesin-based chromosome axis and are required for the formation of DNA double-strand breaks. In contrast to the well-organized SC structure, LinE structure had been observed only by silver-stained electron micrographs or in immuno-fluorescence stained spread nuclei. Thus, their fine structure and dynamics in intact living cells remain to be elucidated. In this study, we performed live cell imaging with wide-field fluorescence microscopy as well as 3D structured illumination microscopy (3D-SIM) for the four components of LinE, the Rec10, Rec25, Rec27 and Mug20. We found that LinEs consist of threads formed along the chromosome axes during the meiotic prophase. Rec10 binds to the chromosome itself and shapes into LinEs only in the presence of all the other LinE components. Rec25, Rec27, and Mug20 attach to the chromosome in the presence of Rec10. LinEs are stable in a short-time treatment with 1,6-hexanediol; and fluorescence recovery after photobleaching (FRAP) experiment reveals slow recovery from photobleaching, indicating a stable property of LinEs.

show abstract

Section: The Line Is a Stable Structurementioning

confidence: 78%

Section: Stability Of Linesmentioning

confidence: 99%

The Linear Element is a Stable Structure Along the Chromosome Axis in Fission Yeast

Ding

Matsuda

Okamasa

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…In particular, fission yeast expresses sme2, a meiosis-specific lncRNA that accumulates at its gene locus and mediates robust pairing [79]. In a recent study, several sme2 RNA-associated proteins (Smp) were identified and were found to be similarly required for robust pairing [80]. Acute addition of 1,6-hexanediol dissolves Smp foci and unpairs the sme2 RNA-decorated loci (Box 2).…”

Section: Phase Separation During Meiotic Recombinationmentioning

confidence: 99%

Phase Separation during Germline Development

Cheng

Schuh

2021

Trends in Cell Biology

View full text Add to dashboard Cite

Many non-membrane-bound compartments in cells organize by phase separation. Recent research implicates phase separation in different steps during germline development. Phase separation drives the formation and partitioning of germ granules that determine germ cell identity during early embryogenesis. Phase separation promotes the interactions between ribonucleoprotein particles and membrane-bound organelles to form the Balbiani body in Xenopus and zebrafish oocytes. Phase separation mediates pairing and synapsis of homologous chromosomes during meiotic recombination in various species. Phase separation enriches microtubule regulatory proteins and promotes acentrosomal spindle assembly in mammalian oocytes.

show abstract

“…In this context, the formation of inter-chromosomal interactions between loci sharing the same set of protein regulators would stabilize the association of partially-condensed homologue chromosomes. Fulfilling this prophecy, recent work demonstrated that homologue chromosome pairing in yeast relies on ribonucleoprotein (RNP) complexes involving locally-transcribed, meiosis-specific long non-coding RNAs (lncRNAs; Ding et al, 2019 ).…”

Section: Inter-chromosomal Genome Architecturementioning

confidence: 99%

RNA Biogenesis Instructs Functional Inter-Chromosomal Genome Architecture

Bertero

2021

Front. Genet.

View full text Add to dashboard Cite

Three-dimensional (3D) genome organization has emerged as an important layer of gene regulation in development and disease. The functional properties of chromatin folding within individual chromosomes (i.e., intra-chromosomal or in cis) have been studied extensively. On the other hand, interactions across different chromosomes (i.e., inter-chromosomal or in trans) have received less attention, being often regarded as background noise or technical artifacts. This viewpoint has been challenged by emerging evidence of functional relationships between specific trans chromatin interactions and epigenetic control, transcription, and splicing. Therefore, it is an intriguing possibility that the key processes involved in the biogenesis of RNAs may both shape and be in turn influenced by inter-chromosomal genome architecture. Here I present the rationale behind this hypothesis, and discuss a potential experimental framework aimed at its formal testing. I present a specific example in the cardiac myocyte, a well-studied post-mitotic cell whose development and response to stress are associated with marked rearrangements of chromatin topology both in cis and in trans. I argue that RNA polymerase II clusters (i.e., transcription factories) and foci of the cardiac-specific splicing regulator RBM20 (i.e., splicing factories) exemplify the existence of trans-interacting chromatin domains (TIDs) with important roles in cellular homeostasis. Overall, I propose that inter-molecular 3D proximity between co-regulated nucleic acids may be a pervasive functional mechanism in biology.

show abstract

Chromosome-associated RNA–protein complexes promote pairing of homologous chromosomes during meiosis in Schizosaccharomyces pombe

Cited by 55 publications

References 49 publications

The Linear Element is a Stable Structure Along the Chromosome Axis in Fission Yeast

The Linear Element is a Stable Structure Along the Chromosome Axis in Fission Yeast

Phase Separation during Germline Development

RNA Biogenesis Instructs Functional Inter-Chromosomal Genome Architecture

Contact Info

Product

Resources

About