Cited by 1Genomics and Chromatin DynamicsChromosomal and Genetic VariationsNuclear Structure and Function

The DOI matches its Crossref record; 6 of the 6 references it cites were found in a registry or an index.

Transposon targeting non-coding RNA transcription targets G/C-rich tracts and is facilitated by an intrinsically disordered protein in Tetrahymena

Open access

Published version of a preprint

Abstract

Tetrahymena is a well-established ciliate model organism, known for its nuclear dualism and unique mechanism for transposon defense, wherein transposons are kept within the highly heterochromatinized micronucleus (MIC), which is transcriptionally inert except during meiosis. The discovery of preferential transcription in the meiotic MIC at regions enriched with transposons and the identification of MIC transcription regulatory proteins emphasize the necessity to elucidate the underlying mechanisms driving this process. In this study, we demonstrate that G/C-rich tracts are overrepresented in meiotic non-coding RNA (ncRNA) transcription regions and that RNA polymerase II (Pol II) is highly enriched at and around these tracts. Further analysis revealed that Pol II's association with G/C-rich tracts is not abolished in cells lacking Rib1, a Mediator complex-associated protein essential for MIC ncRNA biogenesis. Nevertheless, in the absence of Rib1, Pol II showed abnormal association with the meiotic MIC chromatin, suggesting that Rib1 is critical for maintaining Pol II's binding specificity. Through Rib1 truncation analysis, we found that the intrinsically disordered region, which contains putative phase-separating peptides, is crucial for its function. Disruption of phase-separation, either by deleting these peptides or by treating cells with a phase-separation disruption reagent, leads to aberrant localization of both Rib1 and Pol II on the MIC chromatin, implicating that Rib1 likely facilitates the MIC ncRNA transcription via phase-separation.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s11427-025-3103-x

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Show all 6 references

Research works printed but not linked: 111

  1. Al-Hadid, Q., and Yang, Y. (2016). R-loop: an emerging regulator of chromatin dynamics. Acta Biochim Biophys Sin 48, 623–631. · DOI
  2. Alberti, S., Saha, S., Woodruff, J.B., Franzmann, T.M., Wang, J., and Hyman, A.A. (2018). A user’s guide for phase separation assays with purified proteins. J Mol Biol 430, 4806–4820. · DOI
  3. Allen, S.E., and Nowacki, M. (2020). Roles of noncoding RNAs in ciliate genome architecture. J Mol Biol 432, 4186–4198. · DOI
  4. Aronica, L., Bednenko, J., Noto, T., DeSouza, L.V., Siu, K.W.M., Loidl, J., Pearlman, R. E., Gorovsky, M.A., and Mochizuki, K. (2008). Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA elimination in Tetrahymena. Genes Dev 22, 2228–2241. · DOI
  5. Bailey, T.L., and Birol, I. (2021). STREME: accurate and versatile sequence motif discovery. Bioinformatics 37, 2834–2840. · DOI
  6. Boeynaems, S., Alberti, S., Fawzi, N.L., Mittag, T., Polymenidou, M., Rousseau, F., Schymkowitz, J., Shorter, J., Wolozin, B., Van Den Bosch, L., et al. (2018). Protein phase separation: a new phase in cell biology. Trends Cell Biol 28, 420–435. · DOI
  7. Brázda, V., Kolomazník, J., Lýsek, J., Bartas, M., Fojta, M., Šťastný, J., Mergny, J.L., and Hancock, J. (2019). G4Hunter web application: a web server for G-quadruplex prediction. Bioinformatics 35, 3493–3495. · DOI
  8. Buenrostro, J.D., Wu, B., Litzenburger, U.M., Ruff, D., Gonzales, M.L., Snyder, M.P., Chang, H.Y., and Greenleaf, W.J. (2015). Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523, 486–490. · DOI · Paper page
  9. Cai, X., Zhai, Z., Noto, T., Dong, G., Wang, X., Liucong, M., Liu, Y., Agreiter, C., Loidl, J., Mochizuki, K., et al. (2025). A specialized TFIIB is required for transcription of transposon-targeting noncoding RNAs. Nucleic Acids Res 53, gkaf427. · DOI
  10. Carle, C.M., Zaher, H.S., and Chalker, D.L. (2016). A parallel G quadruplex-binding protein regulates the boundaries of DNA elimination events of Tetrahymena thermophila. PLoS Genet 12, e1005842. · DOI
  11. Cassidy-Hanley, D., Bowen, J., Lee, J.H., Cole, E., VerPlank, L.A., Gaertig, J., Gorovsky, M.A., and Bruns, P.J. (1997). Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics 146, 135–147. · DOI
  12. Chalker, D.L., Meyer, E., and Mochizuki, K. (2013). Epigenetics of ciliates. Cold Spring Harb Perspect Biol 5, a017764. · DOI
  13. Chalker, D.L., and Yao, M.C. (2001). Nongenic, bidirectional transcription precedes and may promote developmental DNA deletion in Tetrahymena thermophila. Genes Dev 15, 1287–1298. · DOI
  14. Chen, Y., Simeone, A., Melidis, L., Cuesta, S.M., Tannahill, D., and Balasubramanian, S. (2024). An upstream G-quadruplex DNA structure can stimulate gene transcription. ACS Chem Biol 19, 736–742. · DOI
  15. Cheng, C.Y., Vogt, A., Mochizuki, K., Yao, M.C., and Bloom, K.S. (2010). A domesticated piggyBac transposase plays key roles in heterochromatin dynamics and DNA cleavage during programmed DNA deletion in Tetrahymena thermophila. Mol Biol Cell 21, 1753–1762. · DOI
  16. Cho, W.K., Spille, J.H., Hecht, M., Lee, C., Li, C., Grube, V., and Cisse, I.I. (2018). Mediator and RNA polymerase II clusters associate in transcription-dependent condensates. Science 361, 412–415. · DOI · Paper page
  17. Couzin, J. (2002). Breakthrough of the year. Small RNAs make big splash. Science 298, 2296–2297. · DOI
  18. Coyne, R.S., Chalker, D.L., and Yao, M.C. (1996). Genome downsizing during ciliate development: nuclear division of labor through chromosome restructuring. Annu Rev Genet 30, 557–578. · DOI
  19. Dong, F., Cheng, X., Wan, J., Li, Q., Du, W., Li, W., Sun, X., and Wu, X. (2025). Transcriptional condensates enrich phosphorylated PRMT2 to stimulate H3R8me2a deposition and hypoxic response in glioblastoma. Sci China Life Sci doi: https://doi.org/10.1007/s11427-025-2959-x. · DOI
  20. Drews, F., Boenigk, J., and Simon, M. (2022). Paramecium epigenetics in development and proliferation. J Eukaryot Microbiol 69, e12914. · DOI
  21. Eisen, J.A., Coyne, R.S., Wu, M., Wu, D., Thiagarajan, M., Wortman, J.R., Badger, J.H., Ren, Q., Amedeo, P., Jones, K.M., et al. (2006). Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4, e286. · DOI
  22. Erdős, G., Pajkos, M., and Dosztányi, Z. (2021). IUPred3: prediction of protein disorder enhanced with unambiguous experimental annotation and visualization of evolutionary conservation. Nucleic Acids Res 49, W297–W303. · DOI
  23. Esain-Garcia, I., Kirchner, A., Melidis, L., Tavares, R.C.A., Dhir, S., Simeone, A., Yu, Z., Madden, S.K., Hermann, R., Tannahill, D., et al. (2024). G-quadruplex DNA structure is a positive regulator of MYC transcription. Proc Natl Acad Sci USA 121, e2320240121. · DOI
  24. Gao, J., Jing, J., Shang, G., Chen, C., Duan, M., Yu, W., Wang, K., Luo, J., Song, M., Chen, K., et al. (2024). TDRD1 phase separation drives intermitochondrial cement assembly to promote piRNA biogenesis and fertility. Dev Cell 59, 2704–2718.e6. · DOI
  25. Gao, Y., Solberg, T., Wang, C., and Gao, F. (2023). Small RNA-mediated genome rearrangement pathways in ciliates. Trends Genet 39, 94–97. · DOI
  26. Gibson, D.G., Young, L., Chuang, R.Y., Venter, J.C., Hutchison Iii, C.A., and Smith, H. O. (2009). Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6, 343–345. · DOI
  27. Godiska, R., James, C., and Yao, M.C. (1993). A distant 10-bp sequence specifies the boundaries of a programmed DNA deletion in Tetrahymena. Genes Dev 7, 2357–2365. · DOI
  28. Godiska, R., and Yao, M.C. (1990). A programmed site-specific DNA rearrangement in Tetrahymena thermophila requires flanking polypurine tracts. Cell 61, 1237–1246. · DOI
  29. Gorovsky, M.A. (1970). Studies on nuclear structure and function in Tetrahymena pyriformis. J Cell Biol 47, 619–630. · DOI
  30. Gruchota, J., Denby Wilkes, C., Arnaiz, O., Sperling, L., and Nowak, J.K. (2017). A meiosis-specific Spt5 homolog involved in non-coding transcription. Nucleic Acids Res 45, gkw1318. · DOI
  31. Guzikowski, N.J., and Kavalali, E.T. (2024). Functional specificity of liquid-liquid phase separation at the synapse. Nat Commun 15, 10103. · DOI
  32. Hamilton, E.P., Kapusta, A., Huvos, P.E., Bidwell, S.L., Zafar, N., Tang, H., Hadjithomas, M., Krishnakumar, V., Badger, J.H., Caler, E.V., et al. (2016). Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome. eLife 5, e19090. · DOI
  33. Hänsel-Hertsch, R., Beraldi, D., Lensing, S.V., Marsico, G., Zyner, K., Parry, A., Di Antonio, M., Pike, J., Kimura, H., Narita, M., et al. (2016). G-quadruplex structures mark human regulatory chromatin. Nat Genet 48, 1267–1272. · DOI · Paper page
  34. Hao, H., Lian, Y., Ren, C., Yang, S., Zhao, M., Bo, T., Xu, J., and Wang, W. (2024). RebL1 is required for macronuclear structure stability and gametogenesis in Tetrahymena thermophila. Mar Life Sci Technol 6, 183–197. · DOI
  35. Iwamoto, M., Mori, C., Osakada, H., Koujin, T., Hiraoka, Y., and Haraguchi, T. (2018). Nuclear localization signal targeting to macronucleus and micronucleus in binucleated ciliate Tetrahymena thermophila. Genes Cells 23, 568–579. · DOI
  36. Jiang, Y., Chen, X., Wang, C., Lyu, L., Al-Farraj, S.A., Stover, N.A., and Gao, F. (2025). Genes and proteins expressed at different life cycle stages in the model protist Euplotes vannus revealed by both transcriptomic and proteomic approaches. Sci China Life Sci 68, 232–248. · DOI
  37. Jin, D., Li, C., Chen, X., Byerly, A., Stover, N.A., Zhang, T., Shao, C., and Wang, Y. (2023). Comparative genome analysis of three euplotid protists provides insights into the evolution of nanochromosomes in unicellular eukaryotic organisms. Mar Life Sci Technol 5, 300–315. · DOI
  38. Kataoka, K., and Mochizuki, K. (2017). Heterochromatin aggregation during DNA elimination in Tetrahymena is facilitated by a prion-like protein. J Cell Sci 130, 480–489. · DOI
  39. Kataoka, K., Schoeberl, U.E., and Mochizuki, K. (2010). Modules for C-terminal epitope tagging of Tetrahymena genes. J Microbiol Methods 82, 342–346. · DOI
  40. Kaya-Okur, H.S., Wu, S.J., Codomo, C.A., Pledger, E.S., Bryson, T.D., Henikoff, J.G., Ahmad, K., and Henikoff, S. (2019). CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat Commun 10, 1930. · DOI · Paper page
  41. Kroschwald, S., Maharana, S., and Simon, A. (2017). Hexanediol: a chemical probe to investigate the material properties of membrane-less compartments. Matters doi: https://doi.org/10.19185/matters.201702000010. · DOI
  42. Lancaster, A.K., Nutter-Upham, A., Lindquist, S., and King, O.D. (2014). PLAAC: a web and command-line application to identify proteins with prion-like amino acid composition. Bioinformatics 30, 2501–2502. · DOI
  43. Langmead, B., and Salzberg, S.L. (2012). Fast gapped-read alignment with Bowtie 2. Nat Methods 9, 357–359. · DOI · Paper page
  44. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10, R25. · DOI · Paper page
  45. Lee, C.Y., McNerney, C., Ma, K., Zhao, W., Wang, A., and Myong, S. (2020). R-loop induced G-quadruplex in non-template promotes transcription by successive R-loop formation. Nat Commun 11, 3392. · DOI
  46. Lee, S.R., and Collins, K. (2006). Two classes of endogenous small RNAs in Tetrahymena thermophila. Genes Dev 20, 28–33. · DOI
  47. Leer, J.C., Tiryaki, D., and Westergaard, O. (1979). Termination of transcription in nucleoli isolated from Tetrahymena. Proc Natl Acad Sci USA 76, 5563–5566. · DOI
  48. Li, C., Wang, H., Yin, Z., Fang, P., Xiao, R., Xiang, Y., Wang, W., Li, Q., Huang, B., Huang, J., et al. (2021a). Ligand-induced native G-quadruplex stabilization impairs transcription initiation. Genome Res 31, 1546–1560. · DOI
  49. Li, L., Williams, P., Ren, W., Wang, M.Y., Gao, Z., Miao, W., Huang, M., Song, J., and Wang, Y. (2021b). YY1 interacts with guanine quadruplexes to regulate DNA looping and gene expression. Nat Chem Biol 17, 161–168. · DOI
  50. Lin, Y., Mori, E., Kato, M., Xiang, S., Wu, L., Kwon, I., and McKnight, S.L. (2016). Toxic PR poly-dipeptides encoded by the C9orf72 repeat expansion target LC domain polymers. Cell 167, 789–802.e12. · DOI
  51. Liu, C., Fu, S., Yi, C., Liu, Y., Huang, Y., Guo, X., Zhang, K., Liu, Q., Birchler, J.A., and Han, F. (2024). Unveiling the distinctive traits of functional rye centromeres: minisatellites, retrotransposons, and R-loop formation. Sci China Life Sci 67, 1989–2002. · DOI
  52. Liu, X., Jiang, S., Ma, L., Qu, J., Zhao, L., Zhu, X., and Ding, J. (2021). Time-dependent effect of 1,6-hexanediol on biomolecular condensates and 3D chromatin organization. Genome Biol 22, 230. · DOI
  53. Liu, Y., Su, H., Zhang, J., Liu, Y., Feng, C., and Han, F. (2020). Back-spliced RNA from retrotransposon binds to centromere and regulates centromeric chromatin loops in maize. PLoS Biol 18, e3000582. · DOI
  54. Liu, Y., Taverna, S.D., Muratore, T.L., Shabanowitz, J., Hunt, D.F., and Allis, C.D. (2007). RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev 21, 1530–1545. · DOI
  55. Loidl, J., Lukaszewicz, A., Howard-Till, R.A., and Koestler, T. (2012). The Tetrahymena meiotic chromosome bouquet is organized by centromeres and promotes interhomolog recombination. J Cell Sci 125, 5873–5880. · DOI
  56. Lombardi, E.P., and Londoño-Vallejo, A. (2020). A guide to computational methods for G-quadruplex prediction. Nucleic Acids Res 48, 1603. · DOI
  57. Long, H., Johri, P., Gout, J.F., Ni, J., Hao, Y., Licknack, T., Wang, Y., Pan, J., Jiménez-Marín, B., and Lynch, M. (2023). Paramecium genetics, genomics, and evolution. Annu Rev Genet 57, 391–410. · DOI
  58. Lopez-Delisle, L., Rabbani, L., Wolff, J., Bhardwaj, V., Backofen, R., Grüning, B., Ramírez, F., Manke, T., and Peter, R. (2021). pyGenomeTracks: reproducible plots for multivariate genomic datasets. Bioinformatics 37, 422–423. · DOI
  59. Lyu, L., Zhang, X., Gao, Y., Zhang, T., Fu, J., Stover, N.A., and Gao, F. (2024). From germline genome to highly fragmented somatic genome: genome-wide DNA rearrangement during the sexual process in ciliated protists. Mar Life Sci Technol 6, 31–49. · DOI
  60. Maeshima, K., Iida, S., and Tamura, S. (2021). Physical nature of chromatin in the nucleus. Cold Spring Harb Perspect Biol 13, a040675. · DOI
  61. Malone, C.D., Anderson, A.M., Motl, J.A., Rexer, C.H., and Chalker, D.L. (2005). Germ line transcripts are processed by a dicer-like protein that is essential for developmentally programmed genome rearrangements of Tetrahymena thermophila. Mol Cell Biol 25, 9151–9164. · DOI
  62. Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17, 10. · DOI · Paper page
  63. Mochizuki, K. (2008). High efficiency transformation of Tetrahymena using a codon-optimized neomycin resistance gene. Gene 425, 79–83. · DOI
  64. Mochizuki, K., Fine, N.A., Fujisawa, T., and Gorovsky, M.A. (2002). Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110, 689–699. · DOI
  65. Mochizuki, K., and Gorovsky, M.A. (2004). RNA polymerase II localizes in Tetrahymena thermophila meiotic micronuclei when micronuclear transcription associated with genome rearrangement occurs. Eukaryot Cell 3, 1233–1240. · DOI
  66. Mochizuki, K., and Gorovsky, M.A. (2005). A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev 19, 77–89. · DOI
  67. Mochizuki, K., and Kurth, H.M. (2013). Loading and pre-loading processes generate a distinct siRNA population in Tetrahymena. Biochem Biophys Res Commun 436, 497–502. · DOI
  68. Murthy, A.C., Dignon, G.L., Kan, Y., Zerze, G.H., Parekh, S.H., Mittal, J., and Fawzi, N. L. (2019). Molecular interactions underlying liquid-liquid phase separation of the FUS low-complexity domain. Nat Struct Mol Biol 26, 637–648. · DOI · Paper page
  69. Namitz, K.E.W., Showalter, S.A., and Cosgrove, M.S. (2023). Phase separation promotes a highly active oligomeric scaffold of the MLL1 core complex for regulation of histone H3K4 methylation. J Biol Chem 299, 105204. · DOI
  70. Noto, T., Kataoka, K., Suhren, J.H., Hayashi, A., Woolcock, K.J., Gorovsky, M.A., and Mochizuki, K. (2015). Small-RNA-mediated genome-wide trans-recognition network in Tetrahymena DNA elimination. Mol Cell 59, 229–242. · DOI
  71. Noto, T., Kurth, H.M., Kataoka, K., Aronica, L., DeSouza, L.V., Siu, K.W.M., Pearlman, R.E., Gorovsky, M.A., and Mochizuki, K. (2010). The Tetrahymena argonaute-binding protein Giw1p directs a mature argonaute-siRNA complex to the nucleus. Cell 140, 692–703. · DOI
  72. Noto, T., and Mochizuki, K. (2017). Whats, hows and whys of programmed DNA elimination in Tetrahymena. Open Biol 7, 170172. · DOI
  73. Noto, T., and Mochizuki, K. (2018). Small RNA-mediated trans-nuclear and trans-element communications in Tetrahymena DNA elimination. Curr Biol 28, 1938–1949.e5. · DOI · Paper page
  74. Orias, E., Cervantes, M.D., and Hamilton, E.P. (2011). Tetrahymena thermophila, a unicellular eukaryote with separate germline and somatic genomes. Res Microbiol 162, 578–586. · DOI
  75. Owsian, D., Gruchota, J., Arnaiz, O., and Nowak, J.K. (2022). The transient Spt4-Spt5 complex as an upstream regulator of non-coding RNAs during development. Nucleic Acids Res 50, 2603–2620. · DOI
  76. Raikhel, N., Paulin, J.J., and Skarlato, S.O. (1981). Mitosis of micronuclei during division and regeneration in the ciliate Stentor coeruleus 1. J Protozool 28, 103–107. · DOI
  77. Raikov, I.B., Karadzhan, B.P., Kaur, R., and Mignot, J.P. (1989). Nuclear fine structure at interphase and during encystment in two forms of the testacean Arcella vulgaris. Eur J Protistol 24, 369–380. · DOI
  78. Ramírez, F., Ryan, D.P., Grüning, B., Bhardwaj, V., Kilpert, F., Richter, A.S., Heyne, S., Dündar, F., and Manke, T. (2016). deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res 44, W160–W165. · DOI · Paper page
  79. Richter, W.F., Nayak, S., Iwasa, J., and Taatjes, D.J. (2022). The Mediator complex as a master regulator of transcription by RNA polymerase II. Nat Rev Mol Cell Biol 23, 732–749. · DOI
  80. Robinson, J., Raguseo, F., Nuccio, S.P., Liano, D., and Di Antonio, M. (2021). DNA G-quadruplex structures: more than simple roadblocks to transcription? Nucleic Acids Res 49, 8419–8431. · DOI
  81. Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., and Mesirov, J.P. (2011). Integrative genomics viewer. Nat Biotechnol 29, 24–26. · DOI · Paper page
  82. Ruehle, M.D., Orias, E., and Pearson, C.G. (2016). Tetrahymena as a unicellular model eukaryote: genetic and genomic tools. Genetics 203, 649–665. · DOI
  83. Sabari, B.R., Dall’Agnese, A., Boija, A., Klein, I.A., Coffey, E.L., Shrinivas, K., Abraham, B.J., Hannett, N.M., Zamudio, A.V., Manteiga, J.C., et al. (2018). Coactivator condensation at super-enhancers links phase separation and gene control. Science 361, eaar3958. · DOI · Paper page
  84. Santana-Garcia, W., Castro-Mondragon, J.A., Padilla-Gálvez, M., Nguyen, N.T.T., Elizondo-Salas, A., Ksouri, N., Gerbes, F., Thieffry, D., Vincens, P., Contreras-Moreira, B., et al. (2022). RSAT 2022: regulatory sequence analysis tools. Nucleic Acids Res 50, W670–W676. · DOI
  85. Saveliev, S.V., and Cox, M.M. (1994). The fate of deleted DNA produced during programmed genomic deletion events in Tetrahymena thermophila. Nucleic Acids Res 22, 5695–5701. · DOI
  86. Saveliev, S.V. (2001). Product analysis illuminates the final steps of IES deletion in Tetrahymena thermophila. EMBO J 20, 3251–3261. · DOI
  87. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat Methods 9, 676–682. · DOI · Paper page
  88. Schoeberl, U.E., Kurth, H.M., Noto, T., and Mochizuki, K. (2012). Biased transcription and selective degradation of small RNAs shape the pattern of DNA elimination in Tetrahymena. Genes Dev 26, 1729–1742. · DOI
  89. Shehzada, S., Noto, T., Saksouk, J., and Mochizuki, K. (2024). A SUMO E3 ligase promotes long non-coding RNA transcription to regulate small RNA-directed DNA elimination. eLife 13, e95337. · DOI
  90. Sheng, Y., Duan, L., Cheng, T., Qiao, Y., Stover, N.A., and Gao, S. (2020). The completed macronuclear genome of a model ciliate Tetrahymena thermophila and its application in genome scrambling and copy number analyses. Sci China Life Sci 63, 1534–1542. · DOI
  91. Skarlato, S. (1982). Electron microscope study of the micronuclei of the ciliate Stentor coeruleus during meiosis. Protistologica 18, 281–288.
  92. Spiegel, J., Cuesta, S.M., Adhikari, S., Hänsel-Hertsch, R., Tannahill, D., and Balasubramanian, S. (2021). G-quadruplexes are transcription factor binding hubs in human chromatin. Genome Biol 22, 117. · DOI
  93. Sugai, T., and Hiwatashi, K. (1974). Cytologic and autoradiographic studies of the micronucleus at meiotic prophase in Tetrahymena pyriformis. J Protozool 21, 542–548. · DOI
  94. Sun, J., Qu, J., Zhao, C., Zhang, X., Liu, X., Wang, J., Wei, C., Liu, X., Wang, M., Zeng, P., et al. (2024). Precise prediction of phase-separation key residues by machine learning. Nat Commun 15, 2662. · DOI
  95. Taverna, S.D., Coyne, R.S., and Allis, C.D. (2002). Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell 110, 701–711. · DOI
  96. Tian, M., Cai, X., Liu, Y., Liucong, M., and Howard-Till, R. (2022). A practical reference for studying meiosis in the model ciliate Tetrahymena thermophila. Mar Life Sci Technol 4, 595–608. · DOI
  97. Tian, M., Mochizuki, K., and Loidl, J. (2019). Non-coding RNA transcription in Tetrahymena meiotic nuclei requires dedicated mediator complex-associated proteins. Curr Biol 29, 2359–2370.e5. · DOI
  98. UniProt Consortium. (2025). UniProt: the universal protein knowledgebase in 2025. Nucleic Acids Res 53, D609–D617. · DOI · Paper page
  99. Vogt, A., and Mochizuki, K. (2013). A domesticated piggyBac transposase interacts with heterochromatin and catalyzes reproducible DNA elimination in Tetrahymena. PLoS Genet 9, e1004032. · DOI
  100. Wang, G., Wang, S., Chai, X., Zhang, J., Yang, W., Jiang, C., Chen, K., Miao, W., and Xiong, J. (2021). A strategy for complete telomere-to-telomere assembly of ciliate macronuclear genome using ultra-high coverage Nanopore data. Comput Struct Biotechnol J 19, 1928–1932. · DOI
  101. Wang, W., Li, D., Xu, Q., Cheng, J., Yu, Z., Li, G., Qiao, S., Pan, J., Wang, H., Shi, J., et al. (2024). G-quadruplexes promote the motility in MAZ phase-separated condensates to activate CCND1 expression and contribute to hepatocarcinogenesis. Nat Commun 15, 1045. · DOI
  102. Wolfe, J., Hunter, B., and Adair, W.S. (1976). A cytological study of micronuclear elongation during conjugation in Tetrahymena. Chromosoma 55, 289–308. · DOI
  103. Woo, T.T., Chao, J.L., and Yao, M.C. (2016). Dynamic distributions of long double-stranded RNA in Tetrahymena during nuclear development and genome rearrangements. J Cell Sci 129, 1046–1058. · DOI
  104. Wulfridge, P., and Sarma, K. (2024). Intertwining roles of R-loops and G-quadruplexes in DNA repair, transcription and genome organization. Nat Cell Biol 26, 1025–1036. · DOI
  105. Wulfridge, P., Yan, Q., Rell, N., Doherty, J., Jacobson, S., Offley, S., Deliard, S., Feng, K., Phillips-Cremins, J.E., Gardini, A., et al. (2023). G-quadruplexes associated with R-loops promote CTCF binding. Mol Cell 83, 3064–3079.e5. · DOI
  106. Yao, M.C., Yao, C.H., and Monks, B. (1990). The controlling sequence for site-specific chromosome breakage in Tetrahymena. Cell 63, 763–772. · DOI
  107. Ye, F., Chen, X., Li, Y., Ju, A., Sheng, Y., Duan, L., Zhang, J., Zhang, Z., Al-Rasheid, K. A.S., Stover, N.A., et al. (2025). Comprehensive genome annotation of the model ciliate Tetrahymena thermophila by in-depth epigenetic and transcriptomic profiling. Nucleic Acids Res 53, gkae1177. · DOI
  108. Yuan, J., He, X., and Wang, Y. (2023). G-quadruplex DNA contributes to RNA polymerase II-mediated 3D chromatin architecture. Nucleic Acids Res 51, 8434–8446. · DOI
  109. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., et al. (2008). Model-based analysis of ChIP-Seq (MACS). Genome Biol 9, R137. · DOI · Paper page
  110. Zhao, X., Xiong, J., Mao, F., Sheng, Y., Chen, X., Feng, L., Dui, W., Yang, W., Kapusta, A., Feschotte, C., et al. (2019). RNAi-dependent Polycomb repression controls transposable elements in Tetrahymena. Genes Dev 33, 348–364. · DOI
  111. Zhu, C., Si, X., Hou, X., Xu, P., Gao, J., Tang, Y., Weng, C., Xu, M., Yan, Q., Jin, Q., et al. (2025). piRNA gene density and SUMOylation organize piRNA transcriptional condensate formation. Nat Struct Mol Biol 32, 1503–1516. · DOI

Metadata

Authors
Cai, X., Liu, Y., Li, J., Zhao, Z., Yao, X., Zhai, Z., Liucong, M., Liu, Y., Wang, X., Mochizuki, K., & Tian, M.
Affiliations
  • Ocean University of China (CN)
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
Tian, Miao
Venue
Science China Life Sciences
Published
2026-02-26
Volume
69
Issue
7
Pages
2156-2172
ISSN
  • 1674-7305 (ISSN-L)
  • 1869-1889
OpenAlex
W7133187627
Cited by
1
References
6
Citations by year
2026: 1
FWCI
2.09
Type
journal article
Language
en
Open access
Locations
  • Science China Life Sciences (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
Funders
  • European Commission (HORIZON2020, 101024333)
  • National Natural Science Foundation of China (32370451)
  • Natural Science Foundation of Shandong Province (ZR2022JQ13)
  • Fundamental Research Funds for the Central Universities (202241003)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
Keywords
Tetrahymena, micronuclei, transposon defense, RNA polymerase II, Mediator complex, intrinsically disordered proteins, phase separation, meiosis, heterochromatin, transcriptional regulation
MeSH terms
DNA Transposable Elements, Heterochromatin, Meiosis, RNA Polymerase II, Tetrahymena, Transcription, Genetic, Protozoan Proteins, RNA, Untranslated

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review