Paramecium epigenetics in development and proliferation.
RNA
RNA interference
ciliate
genome rearrangement
transgenerational inheritance
Journal
The Journal of eukaryotic microbiology
ISSN: 1550-7408
Titre abrégé: J Eukaryot Microbiol
Pays: United States
ID NLM: 9306405
Informations de publication
Date de publication:
09 2022
09 2022
Historique:
pubmed:
2
4
2022
medline:
16
9
2022
entrez:
1
4
2022
Statut:
ppublish
Résumé
The term epigenetics is used for any layer of genetic information aside from the DNA base-sequence information. Mammalian epigenetic research increased our understanding of chromatin dynamics in terms of cytosine methylation and histone modification during differentiation, aging, and disease. Instead, ciliate epigenetics focused more on small RNA-mediated effects. On the one hand, these do concern the transport of RNA from parental to daughter nuclei, representing a regulated transfer of epigenetic information across generations. On the other hand, studies of Paramecium, Tetrahymena, Oxytricha, and Stylonychia revealed an almost unique function of transgenerational RNA. Rather than solely controlling chromatin dynamics, they control sexual progeny's DNA content quantitatively and qualitatively. Thus epigenetics seems to control genetics, at least genetics of the vegetative macronucleus. This combination offers ciliates, in particular, an epigenetically controlled genetic variability. This review summarizes the epigenetic mechanisms that contribute to macronuclear heterogeneity and relates these to nuclear dimorphism. This system's adaptive and evolutionary possibilities raise the critical question of whether such a system is limited to unicellular organisms or binuclear cells. We discuss here the relevance of ciliate genetics and epigenetics to multicellular organisms.
Substances chimiques
Chromatin
0
RNA
63231-63-0
DNA
9007-49-2
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12914Subventions
Organisme : DFG
ID : SI1397/3-1
Informations de copyright
© 2022 The Authors. Journal of Eukaryotic Microbiology published by Wiley Periodicals LLC on behalf of International Society of Protistologists.
Références
Abello, A., Régnier, V., Arnaiz, O., Le Bars, R., Bétermier, M. & Bischerour, J. (2020) Functional diversification of Paramecium Ku80 paralogs safeguards genome integrity during precise programmed DNA elimination. PLoS Genetics, 16, e1008723.
Adl, S.M., Simpson, A.G.B., Lane, C.E., Lukeš, J., Bass, D., Bowser, S.S. et al. (2012) The revised classification of eukaryotes. Journal of Eukaryotic Microbiology, 59, 429-493.
Allen, S.E., Hug, I., Pabian, S., Rzeszutek, I., Hoehener, C. & Nowacki, M. (2017) Circular concatemers of ultra-short DNA segments produce regulatory RNAs. Cell, 168, 990-999.e7.
Allen, S.E. & Nowacki, M. (2020) Roles of noncoding RNAs in ciliate genome architecture. Journal of Molecular Biology, 432, 4186-4198.
Arnaiz, O., Goût, J.-F., Bétermier, M., Bouhouche, K., Cohen, J., Duret, L. et al. (2010) Gene expression in a paleopolyploid: a transcriptome resource for the ciliate Paramecium tetraurelia. BMC Genomics, 11, 547.
Arnaiz, O., Mathy, N., Baudry, C., Malinsky, S., Aury, J.-M., Denby Wilkes, C. et al. (2012) The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences. PLoS Genetics, 8, e1002984.
Ashe, A., Sapetschnig, A., Weick, E.-M., Mitchell, J., Bagijn, M.P., Cording, A.C. et al. (2012) piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell, 150, 88-99.
Aury, J.-M., Jaillon, O., Duret, L., Noel, B., Jubin, C., Porcel, B.M. et al. (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature, 444, 171-178.
Baranasic, D., Oppermann, T., Cheaib, M., Cullum, J., Schmidt, H. & Simon, M. (2014) Genomic characterization of variable surface antigens reveals a telomere position effect as a prerequisite for RNA interference-mediated silencing in Paramecium tetraurelia. MBio, 5, e01328.
Baroin-Tourancheau, A., Delgado, P., Perasso, R. & Adoutte, A. (1992) A broad molecular phylogeny of ciliates: identification of major evolutionary trends and radiations within the phylum. Proceedings of the National Academy of Sciences of the United States of America, 89, 9764-9768.
Berger, J.D. (1988) The cell cycle and regulation of cell mass and macronuclear DNA content. In: Görtz, H.-D. (Ed.) Paramecium. Berlin, Heidelberg: Springer Berlin Heidelberg, pp. 97-119.
Bétermier, M., Duharcourt, S., Seitz, H. & Meyer, E. (2000) Timing of developmentally programmed excision and circularization of Paramecium internal eliminated sequences. Molecular and cellular biology, 20.5, 1553-1561.
Bischerour, J., Bhullar, S., Denby, W.C., Régnier, V., Mathy, N., Dubois, E. et al. (2018) Six domesticated PiggyBac transposases together carry out programmed DNA elimination in Paramecium. eLife, 7, e37927.
Blackburn, E.H. & Gall, J.G. (1978) A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. Journal of Molecular Biology, 120, 33-53.
Boenigk, J. (2021) Boenigk, Biologie - Arbeitsbuch für Studium und Oberstufe. Berlin, Heidelberg: Springer Berlin Heidelberg.
Bouhouche, K., Gout, J.-F., Kapusta, A., Bétermier, M. & Meyer, E. (2011) Functional specialization of Piwi proteins in Paramecium tetraurelia from post-transcriptional gene silencing to genome remodelling. Nucleic Acids Research, 39, 4249-4264.
Bourque, G. (2009) Transposable elements in gene regulation and in the evolution of vertebrate genomes. Current Opinion in Genetics & Development, 19, 607-612.
Bracht, J.R., Fang, W., Goldman, A.D., Dolzhenko, E., Stein, E.M. & Landweber, L.F. (2013) Genomes on the edge: programmed genome instability in ciliates. Cell, 152, 406-416.
Braun, J., Nabergall, L., Neme, R., Landweber, L.F., Saito, M. & Jonoska, N. (2018) Russian doll genes and complex chromosome rearrangements in Oxytricha trifallax. G3 (Bethesda), 8, 1669-1674.
Burki, F., Roger, A.J., Brown, M.W. & Simpson, A.G.B. (2020) The new tree of eukaryotes. Trends in Ecology & Evolution, 35, 43-55.
Burns, J., Kukushkin, D., Chen, X., Landweber, L.F., Saito, M. & Jonoska, N. (2016) Recurring patterns among scrambled genes in the encrypted genome of the ciliate Oxytricha trifallax. Journal of Theoretical Biology, 410, 171-180.
Carbone, L., Alan Harris, R., Gnerre, S., Veeramah, K.R., Lorente-Galdos, B., Huddleston, J. et al. (2014) Gibbon genome and the fast karyotype evolution of small apes. Nature, 513, 195-201.
Carbone, L., Vessere, G.M., ten Hallers, B.F.H., Zhu, B., Osoegawa, K., Mootnick, A. et al. (2006) A high-resolution map of synteny disruptions in gibbon and human genomes. PLoS Genetics, 2, e223.
Carradec, Q., Götz, U., Arnaiz, O., Pouch, J., Simon, M., Meyer, E. et al. (2015) Primary and secondary siRNA synthesis triggered by RNAs from food bacteria in the ciliate Paramecium tetraurelia. Nucleic Acids Research, 43, 1818-1833.
Cassidy-Hanley, D., Bisharyan, Y., Fridman, V., Gerber, J., Lin, C., Orias, E. et al. (2005) Genome-wide characterization of Tetrahymena thermophila chromosome breakage sites. II. Physical and genetic mapping. Genetics, 170, 1623-1631.
Catania, F., Rothering, R. & Vitali, V. (2021) One cell, two gears: extensive somatic genome plasticity accompanies high germline genome stability in Paramecium. Genome Biology and Evolution, 13(12), evab263.
Cecere, G. (2021) Small RNAs in epigenetic inheritance: from mechanisms to trait transmission. FEBS Letters, 595, 2953-2977.
Cerutti, H. & Casas-Mollano, J.A. (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Current Genetics, 50, 81-99.
Chalker, D.L. & Yao, M.-C. (2011) DNA elimination in ciliates: transposon domestication and genome surveillance. Annual Review of Genetics, 45, 227-246.
Chen, X., Bracht, J., Goldman, A., Dolzhenko, E., Clay, D., Swart, E. et al. (2014) The architecture of a scrambled genome reveals massive levels of genomic rearrangement during development. Cell, 158, 1187-1198.
Chen, X., Jung, S., Beh, L.Y., Eddy, S.R. & Landweber, L.F. (2015) Combinatorial DNA rearrangement facilitates the origin of new genes in ciliates. Genome Biology and Evolution, 7, 2859-2870.
Cheng, C.-Y., Orias, E., Leu, J.-Y. & Turkewitz, A.P. (2020) The evolution of germ-soma nuclear differentiation in eukaryotic unicells. Current Biology, 30, R502-R510.
Clark, T.G. & Forney, J.D. (2003) Free-living and parasitic ciliates. In Craig, A., & Scherf, A. eds, Antigenic variation. London: Academic Press, pp. 375-402.
Czech, B., Munafò, M., Ciabrelli, F., Eastwood, E.L., Fabry, M.H., Kneuss, E. et al. (2018) piRNA-guided genome defense: from biogenesis to silencing. Annual Review of Genetics, 52, 131-157.
Doerder, F.P. & DeBault, L.E. (1978) Life cycle variation and regulation of macronuclear DNA content in Tetrahymena thermophila. Chromosoma, 69, 1-19.
Drews, F., Karunanithi, S., Götz, U., Marker, S., deWijn, R., Pirritano, M. et al. (2021) Two Piwis with Ago-like functions silence somatic genes at the chromatin level. RNA Biology, 18, 757-769.
Drews, F., Salhab, A., Karunanithi, S., Cheaib, M., Jung, M., Schulz, M. et al. (2022) Broad domains of histone marks in the highly compact Paramecium macronuclear genome. Genome Research, 32, 710-725.
Dubois, E., Mathy, N., Régnier, V., Bischerour, J., Baudry, C., Trouslard, R. et al. (2017) Multimerization properties of PiggyMac, a domesticated piggyBac transposase involved in programmed genome rearrangements. Nucleic Acids Research, 45, 3204-3216.
Duharcourt, S., Butler, A. & Meyer, E. (1995) Epigenetic self-regulation of developmental excision of an internal eliminated sequence on Paramecium tetraurelia. Genes & Development, 9, 2065-2077.
Duharcourt, S., Keller, A.M. & Meyer, E. (1998) Homology-dependent maternal inhibition of developmental excision of internal eliminated sequences in Paramecium tetraurelia. Molecular and Cellular Biology, 18, 7075-7085.
Duret, L., Cohen, J., Jubin, C., Dessen, P., Goût, J.-F., Mousset, S. et al. (2008) Analysis of sequence variability in the macronuclear DNA of Paramecium tetraurelia: a somatic view of the germline. Genome Research, 18, 585-596.
Epstein, L.M. & Forney, J.D. (1984) Mendelian and non-mendelian mutations affecting surface antigen expression in Paramecium tetraurelia. Molecular and Cellular Biology, 4, 1583-1590.
Fang, W., Wang, X., Bracht, J.R., Nowacki, M. & Landweber, L.F. (2012) Piwi-interacting RNAs protect DNA against loss during Oxytricha genome rearrangement. Cell, 151, 1243-1255.
Foissner, W., Chao, A. & Katz, L.A. (2009) Diversity and geographic distribution of ciliates (Protista: Ciliophora). In: Foissner, W. & Hawksworth, D.L. (Eds.) Protist diversity and geographical distribution. Vol. 8. Topics in biodiversity and conservation. Dordrecht, Netherlands: Springer, pp. 111-129.
Finlay, B.J., Esteban, G.F. & Fenchel, T. (1998) Protozoan diversity: converging estimates of the global number of free-living ciliate species. Protist, 149(1), 29-37.
Forney, J.D. & Blackburn, E.H. (1988) Developmentally controlled telomere addition in wild-type and mutant paramecia. Molecular and Cellular Biology, 8, 251-258.
Frapporti, A., Miró, P.C., Arnaiz, O., Holoch, D., Kawaguchi, T., Humbert, A. et al. (2019) The Polycomb protein Ezl1 mediates H3K9 and H3K27 methylation to repress transposable elements in Paramecium. Nature Communications, 10, 2710.
Furrer, D.I., Swart, E.C., Kraft, M.F., Sandoval, P.Y. & Nowacki, M. (2017) Two sets of Piwi proteins are involved in distinct sRNA pathways leading to elimination of germline-specific DNA. Cell Reports, 20, 505-520.
Galvani, A. & Sperling, L. (2002) RNA interference by feeding in Paramecium. Trends in Genetics, 18, 11-12.
Gao, F., Roy, S.W. & Katz, L.A. (2015) Analyses of alternatively processed genes in ciliates provide insights into the origins of scrambled genomes and may provide a mechanism for speciation. MBio, 6 (1), e01998-14.
Gao, F., Song, W. & Katz, L.A. (2014) Genome structure drives patterns of gene family evolution in ciliates, a case study using Chilodonella uncinata (Protista, Ciliophora, Phyllopharyngea). Evolution, 68, 2287-2295.
Garnier, O., Serrano, V., Duharcourt, S. & Meyer, E. (2004) RNA-mediated programming of developmental genome rearrangements in Paramecium tetraurelia. Molecular and Cellular Biology, 24, 7370-7379.
Gilley, D. & Blackburn, E.H. (1994) Lack of telomere shortening during senescence in Paramecium. Proceedings of the National Academy of Sciences of the United States of America, 91, 1955-1958.
Gilley, D., Preer, J.R., Aufderheide, K.J. & Polisky, B. (1988) Autonomous replication and addition of telomerelike sequences to DNA microinjected into Paramecium tetraurelia macronuclei. Molecular and Cellular Biology, 8, 4765-4772.
Godiska, R., Aufderheide, K.J., Gilley, D., Hendrie, P., Fitzwater, T., Preer, L.B. et al. (1987) Transformation of Paramecium by microinjection of a cloned serotype gene. Proceedings of the National Academy of Sciences of the United States of America, 84, 7590-7594.
Götz, U., Marker, S., Cheaib, M., Andresen, K., Shrestha, S., Durai, D.A. et al. (2016) Two sets of RNAi components are required for heterochromatin formation in trans triggered by truncated transgenes. Nucleic Acids Research, 44, 5908-5923.
Gratias, A. & Bétermier, M. (2003) Processing of double-strand breaks is involved in the precise excision of paramecium internal eliminated sequences. Molecular and Cellular Biology, 23, 7152-7162.
Grattepanche, J.-D., Walker, L.M., Ott, B.M., Paim Pinto, D.L., Delwiche, C.F., Lane, C.E. et al.(2018) Microbial diversity in the eukaryotic SAR clade: illuminating the darkness between morphology and molecular data. BioEssays, 40, e1700198.
Greider, C.W. & Blackburn, E.H. (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell, 43, 405-413.
Gruchota, J., Denby, W.C., Arnaiz, O., Sperling, L. & Nowak, J.K. (2017) A meiosis-specific Spt5 homolog involved in non-coding transcription. Nucleic Acids Research, 45, 4722-4732.
Guérin, F., Arnaiz, O., Boggetto, N., Denby, W.C., Meyer, E., Sperling, L. et al. (2017) Flow cytometry sorting of nuclei enables the first global characterization of Paramecium germline DNA and transposable elements. BMC Genomics, 18, 327.
Hamilton, E., Bruns, P., Lin, C., Merriam, V., Orias, E., Vong, L. et al. (2005) Genome-wide characterization of tetrahymena thermophila chromosome breakage sites. I. Cloning and identification of functional sites. Genetics, 170, 1611-1621.
Hamilton, E.P., Kapusta, A., Huvos, P.E., Bidwell, S.L., Zafar, N., Tang, H. et al. (2016) Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome. eLife, 5, e19090.
Hammerschmidt, B., Schlegel, M., Lynn, D.H., Leipe, D.D., Sogin, M.L. & Raikov, I.B. (1996) Insights into the evolution of nuclear dualism in the ciliates revealed by phylogenetic analysis of rRNA sequences. Journal of Eukaryotic Microbiology, 43, 225-230.
Herrick, G. (1994) Germline-soma relationships in ciliated protozoa: the inception and evolution of nuclear dimorphism in one-celled animals. Seminars in Developmental Biology, 5, 3-12.
Heyse, G., Jönsson, F., Chang, W.-J. & Lipps, H.J. (2010) RNA-dependent control of gene amplification. Proceedings of the National Academy of Sciences of the United States of America, 107, 22134-22139.
Hoehener, C., Hug, I. & Nowacki, M. (2018) Dicer-like enzymes with sequence cleavage preferences. Cell, 173, 234-247.e7.
Houri-Zeevi, L., Korem, K.Y., Antonova, O. & Rechavi, O. (2020) Three rules explain transgenerational small RNA inheritance in C. elegans. Cell, 182, 1186-1197.e12.
Huang, S., Tao, X., Yuan, S., Zhang, Y., Li, P., Beilinson, H. et al. (2016) Discovery of an active RAG transposon illuminates the origins of V(D)J recombination. Cell, 166, 102-114.
Ignarski, M., Singh, A., Swart, E.C., Arambasic, M., Sandoval, P.Y. & Nowacki, M. (2014) Paramecium tetraurelia chromatin assembly factor-1-like protein PtCAF-1 is involved in RNA-mediated control of DNA elimination. Nucleic Acids Research, 42, 11952-11964.
Jangam, D., Feschotte, C. & Betrán, E. (2017) Transposable element domestication as an adaptation to evolutionary conflicts. Trends in Genetics, 33, 817-831.
Jenkins, R.A. (1977) The role of microtubules in macronuclear division of blepharisma *. The Journal of Protozoology, 24, 264-275.
Kabi, M. & Filion, G.J. (2021) Heterochromatin: did H3K9 methylation evolve to tame transposons? Genome Biology, 22, 325.
Kapusta, A., Matsuda, A., Marmignon, A., Ku, M., Silve, A., Meyer, E. et al. (2011) Highly precise and developmentally programmed genome assembly in Paramecium requires ligase IV-dependent end joining. PLoS Genetics, 7, e1002049.
Karunanithi, S., Oruganti, V., Marker, S., Rodriguez-Viana, A.M., Drews, F., Pirritano, M. et al. (2019) Exogenous RNAi mechanisms contribute to transcriptome adaptation by phased siRNA clusters in Paramecium. Nucleic Acids Research, 47, 8036-8049.
Karunanithi, S., Oruganti, V., de Wijn, R., Drews, F., Cheaib, M., Nordström, K. et al. (2020) Feeding exogenous dsRNA interferes with endogenous sRNA accumulation in Paramecium. DNA Research, 27, 1-10.
Katz, L.A. (2001) Evolution of nuclear dualism in ciliates: a reanalysis in light of recent molecular data. International Journal of Systematic and Evolutionary Microbiology, 51, 1587-1592.
Katz, L.A., Bornstein, J.G., Lasek-Nesselquist, E. & Muse, S.V. (2004) Dramatic diversity of ciliate histone H4 genes revealed by comparisons of patterns of substitutions and paralog divergences among eukaryotes. Molecular Biology and Evolution, 21, 555-562.
Katz, L.A. & Kovner, A.M. (2010) Alternative processing of scrambled genes generates protein diversity in the ciliate Chilodonella uncinata. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 314, 480-488.
Khurana, J.S., Wang, X., Chen, X., Perlman, D.H. & Landweber, L.F. (2014) Transcription-independent functions of an RNA polymerase II subunit, Rpb2, during genome rearrangement in the ciliate, Oxytricha trifallax. Genetics, 197, 839-849.
Klobutcher, L.A. & Herrick, G. (1997) Developmental genome reorganization in ciliated protozoa: the transposon link. Progress in Nucleic Acid Research and Molecular Biology, 56, 1-62.
Kovaleva, V.G. & Raikov, I.B. (1978) Diminution and re-synthesis of DNA during development and senescence of the? diploid? Macronuclei of the ciliate Trachelonema sulcata (Gymnostomata, Karyorelictida). Chromosoma, 67, 177-192.
Le Pen, J., Jiang, H., Di Domenico, T., Kneuss, E., Kosałka, J., Leung, C. et al. (2018) Terminal uridylyltransferases target RNA viruses as part of the innate immune system. Nature Structural & Molecular Biology, 25, 778-786.
Lee, S.R. & Collins, K. (2007) Physical and functional coupling of RNA-dependent RNA polymerase and Dicer in the biogenesis of endogenous siRNAs. Nature Structural & Molecular Biology, 14, 604-610.
Lepère, G., Bétermier, M., Meyer, E. & Duharcourt, S. (2008) Maternal noncoding transcripts antagonize the targeting of DNA elimination by scanRNAs in Paramecium tetraurelia. Genes & Development, 22, 1501-1512.
Lepère, G., Nowacki, M., Serrano, V., Gout, J.-F., Guglielmi, G., Duharcourt, S. et al. (2009) Silencing-associated and meiosis-specific small RNA pathways in Paramecium tetraurelia. Nucleic Acids Research, 37, 903-915.
Lhuillier-Akakpo, M., Frapporti, A., Denby, W.C., Matelot, M., Vervoort, M., Sperling, L. et al. (2014) Local effect of enhancer of zeste-like reveals cooperation of epigenetic and cis-acting determinants for zygotic genome rearrangements. PLoS Genetics, 10, e1004665.
Lindblad, K.A., Bracht, J.R., Williams, A.E. & Landweber, L.F. (2017) Thousands of RNA-cached copies of whole chromosomes are present in the ciliate Oxytricha during development. RNA, 23, 1200-1208.
Loidl, J. (2021) Tetrahymena meiosis: simple yet ingenious. PLoS Genetics, 17, e1009627.
Luteijn, M.J., van Bergeijk, P., Kaaij, L.J.T., Almeida, M.V., Roovers, E.F., Berezikov, E. et al. (2012) Extremely stable Piwi-induced gene silencing in Caenorhabditis elegans. EMBO Journal, 31, 3422-3430.
Maliszewska-Olejniczak, K., Gruchota, J., Gromadka, R., Denby, W.C., Arnaiz, O., Mathy, N. et al. (2015) TFIIS-dependent non-coding transcription regulates developmental genome rearrangements. PLoS Genetics, 11, e1005383.
Marker, S., Carradec, Q., Tanty, V., Arnaiz, O. & Meyer, E. (2014) A forward genetic screen reveals essential and non-essential RNAi factors in Paramecium tetraurelia. Nucleic Acids Research, 42, 7268-7280.
Marker, S., Le Mouël, A., Meyer, E. & Simon, M. (2010) Distinct RNA-dependent RNA polymerases are required for RNAi triggered by double-stranded RNA versus truncated transgenes in Paramecium tetraurelia. Nucleic Acids Research, 38, 4092-4107.
Marmignon, A., Bischerour, J., Silve, A., Fojcik, C., Dubois, E., Arnaiz, O. et al. (2014) Ku-mediated coupling of DNA cleavage and repair during programmed genome rearrangements in the ciliate Paramecium tetraurelia. PLoS Genetics, 10, e1004552.
Maurer-Alcalá, X.X. & Nowacki, M. (2019) Evolutionary origins and impacts of genome architecture in ciliates. Annals of the New York Academy of Sciences, 1447, 110-118.
Maurer-Alcalá, X.X., Yan, Y., Pilling, O.A., Knight, R. & Katz, L.A. (2018) Twisted tales: insights into genome diversity of ciliates using single-cell ’omics. Genome Biology and Evolution, 10, 1927-1939.
Meyer, E. (1992) Induction of specific macronuclear developmental mutations by microinjection of a cloned telomeric gene in Paramecium primaurelia. Genes & Development, 6, 211-222.
Meyer, E. & Keller, A.-M. (1996) A mendelian mutation affecting mating-type determination also affects developmental genomic rearrangements in Paramecium tetraurelita. Genetics, 143, 191-202.
Nekrasova, I., Nikitashina, V., Bhullar, S., Arnaiz, O., Singh, D.P., Meyer, E. et al. (2019) Loss of a fragile chromosome region leads to the screwy phenotype in Paramecium tetraurelia. Genes (Basel), 10(7), 513.
Nekrasova, I.V. & Potekhin, A.A. (2019) Diversity of RNA interference pathways in regulation of endogenous and exogenous sequences expression in ciliates Tetrahymena and Paramecium. Ecological Genetics, 17, 113-125.
Noto, T., Kataoka, K., Suhren, J.H., Hayashi, A., Woolcock, K.J., Gorovsky, M.A. et al. (2015) Small-RNA-mediated genome-wide trans-recognition network in tetrahymena DNA elimination. Molecular Cell, 59, 229-242.
Nowacki, M., Haye, J.E., Fang, W., Vijayan, V. & Landweber, L.F. (2010) RNA-mediated epigenetic regulation of DNA copy number. Proceedings of the National Academy of Sciences of the United States of America, 107, 22140-22144.
Nowacki, M., Higgins, B.P., Maquilan, G.M., Swart, E.C., Doak, T.G. & Landweber, L.F. (2009) A functional role for transposases in a large eukaryotic genome. Science, 324, 935-938.
Nowacki, M., Vijayan, V., Zhou, Y., Schotanus, K., Doak, T.G. & Landweber, L.F. (2008) RNA-mediated epigenetic programming of a genome-rearrangement pathway. Nature, 451, 153-158.
Orias, E. (1991a) Evolution of amitosis of the ciliate macronucleus: gain of the capacity to divide. The Journal of Protozoology, 38, 217-221.
Orias, E. (1991b) On the evolution of the karyorelict ciliate life cycle: heterophasic ciliates and the origin of ciliate binary fission. BioSystems, 25, 67-73.
Orias, E. & Flacks, M. (1975) Macronuclear genetics of Tetrahymena I. Random distribution of macronuclear gene copies in T. pyriformis, Syngen 1. Genetics, 79, 187-206.
Ovchinnikova, L.P. & Selivanova, G.V. (1965) Photometric study of the DNA content in the nuclei of Spirostomum ambiguum (Ciliata, Heterotricha). Acta Protozoologica, 3, 1-8.
Owsian, D., Gruchota, J., Arnaiz, O. & Nowak, J.K. (2022) The transient Spt4-Spt5 complex as an upstream regulator of non-coding RNAs during development. Nucleic Acids Research, 50(5), 2603-2620. https://doi.org/10.1093/nar/gkac106
Pina, C.M., Kawaguchi, T., Charmant, O., Michaud, A., Cohen, I., Humbert, A. et al. (2021) Paramecium Polycomb Repressive Complex 2 physically interacts with the small RNA binding PIWI protein to repress transposable elements. BioRxiv.
Postberg, J., Heyse, K., Cremer, M., Cremer, T. & Lipps, H.J. (2008) Spatial and temporal plasticity of chromatin during programmed DNA-reorganization in Stylonychia macronuclear development. Epigenetics Chromatin, 1, 3.
Postberg, J., Weil, P.P. & Pembaur, A. (2019) Biogenesis of developmental master regulatory 27nt-RNAs in stylonychia-can coding RNA turn into non-coding? Genes (Basel), 10, 940.
Preer, J.R. (1997) Whatever happened to paramecium genetics? Genetics, 145, 217-225.
Prescott, D.M. (1999) The evolutionary scrambling and developmental unscrambling of germline genes in hypotrichous ciliates. Nucleic Acids Research, 27, 1243-1250.
Raikov, I.B. (1976) Evolution of macronuclear organization. Annual Review of Genetics, 10, 413-440.
Raikov, I.B. (1982) The protozoan nucleus-morphology and evolution. The protozoan nucleus-morphology and evolution.
Raikov, I.B. (1985) Primitive never-dividing macronuclei of some lower ciliates. International Review of Cytology, 95, 267-325.
Raikov, I.B. (1994) The nuclear apparatus of some primitive ciliates, the karyorelictids: structure and divisional reorganization. Bolletino Di Zoologia, 61, 19-28.
Raikov, I.B., Cheissin, M. & Buze, E.G. (1963) A photometric study of DNA content of macro-and micronuclei in Paramecium caudatum, Nassula ornata and Loxodes magnus. Acta Protozoologica, 1, 25-30.
Raikov, I.B. & Karadzhan, B.P. (1985) Fine structure and cytochemistry of the nuclei of the primitive ciliate Tracheloraphis crassus (Karyorelictida). Protoplasma, 126, 114-129.
Rechavi, O., Houri-Ze’evi, L., Anava, S., Goh, W.S.S., Kerk, S.Y., Hannon, G.J. et al. (2014) Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell, 158, 277-287.
Ricci, F., Luporini, P., Alimenti, C. & Vallesi, A. (2021) Functional chimeric genes in ciliates: an instructive case from Euplotes raikovi. Gene, 767, 145186.
Sandoval, P.Y., Swart, E.C., Arambasic, M. & Nowacki, M. (2014) Functional diversification of Dicer-like proteins and small RNAs required for genome sculpting. Developmental Cell, 28, 174-188.
Sawka-Gądek, N., Potekhin, A., Singh, D.P., Grevtseva, I., Arnaiz, O., Penel, S. et al. (2021) Evolutionary plasticity of mating-type determination mechanisms in Paramecium aurelia sibling species. Genome Biology and Evolution, 13, evaa258.
Schoeberl, U.E. & Mochizuki, K. (2011) Keeping the soma free of transposons: programmed DNA elimination in ciliates. Journal of Biological Chemistry, 286, 37045-37052.
Sellis, D., Guérin, F., Arnaiz, O., Pett, W., Lerat, E., Boggetto, N. et al. (2021) Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes. PLoS Biology, 19, e3001309.
Sharma, U., Sun, F., Conine, C.C., Reichholf, B., Kukreja, S., Herzog, V.A. et al. (2018) Small RNAs are trafficked from the epididymis to developing mammalian sperm. Developmental Cell, 46, 481-494.e6.
Sheng, Y., Duan, L., Cheng, T., Qiao, Y., Stover, N.A. & Gao, S. (2020) The completed macronuclear genome of a model ciliate Tetrahymena thermophila and its application in genome scrambling and copy number analyses. Science China Life Sciences, 63, 1534-1542.
Shirayama, M., Seth, M., Lee, H.-C., Gu, W., Ishidate, T., Conte, D. et al. (2012) piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell, 150, 65-77.
Singh, D.P., Saudemont, B., Guglielmi, G., Arnaiz, O., Goût, J.-F., Prajer, M. et al. (2014) Genome-defence small RNAs exapted for epigenetic mating-type inheritance. Nature, 509, 447-452.
Sonneborn, T.M. (1937) Sex, sex inheritance and sex determination in Paramecium aurelia. Proceedings of the National Academy of Sciences of the United States of America, 23, 378-385.
Sonneborn, T.M. & Lesuer, A. (1948) Antigenic characters in Paramecium aurelia, variety 4; determination, inheritance and induced mutations. American Naturalist, 82, 69-78.
Spear, B.B. & Lauth, M.R. (1976) Polytene chromosomes of Oxytricha: biochemical and morphological changes during macronuclear development in a ciliated protozoan. Chromosoma, 54, 1-13.
Swart, E.C., Bracht, J.R., Magrini, V., Minx, P., Chen, X., Zhou, Y.I. et al. (2013) The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. PLoS Biology, 11, e1001473.
Swart, E.C., Wilkes, C.D., Sandoval, P.Y., Arambasic, M., Sperling, L. & Nowacki, M. (2014) Genome-wide analysis of genetic and epigenetic control of programmed DNA deletion. Nucleic Acids Research, 42, 8970-8983.
Tucker, J.B., Beisson, J., Roche, D.L. & Cohen, J. (1980) Microtubules and control of macronuclear “amitosis” in Paramecium. Journal of Cell Science, 44, 135-151.
de Vanssay, A., Touzeau, A., Arnaiz, O., Frapporti, A., Phipps, J. & Duharcourt, S. (2020) The Paramecium histone chaperone Spt16-1 is required for Pgm endonuclease function in programmed genome rearrangements. PLoS Genetics, 16, e1008949.
Vitali, V., Hagen, R. & Catania, F. (2019) Environmentally induced plasticity of programmed DNA elimination boosts somatic variability in Paramecium tetraurelia. Genome Research, 29, 1693-1704.
Vogt, A., Goldman, A.D., Mochizuki, K. & Landweber, L.F. (2013) Transposon domestication versus mutualism in ciliate genome rearrangements. PLoS Genetics, 9, e1003659.
Warren, I.A., Naville, M., Chalopin, D., Levin, P., Berger, C.S., Galiana, D. et al. (2015) Evolutionary impact of transposable elements on genomic diversity and lineage-specific innovation in vertebrates. Chromosome Research, 23, 505-531.
Xu, K., Doak, T.G., Lipps, H.J., Wang, J., Swart, E.C. & Chang, W.-J. (2012) Copy number variations of 11 macronuclear chromosomes and their gene expression in Oxytricha trifallax. Gene, 505, 75-80.
Yan, Y., Maurer-Alcalá, X.X., Knight, R., Kosakovsky Pond, S.L. & Katz, L.A. (2019) Single-cell transcriptomics reveal a correlation between genome architecture and gene family evolution in ciliates. MBio, 10, e02524-19.
Yan, Y., Rogers, A.J., Gao, F. & Katz, L.A. (2017) Unusual features of non-dividing somatic macronuclei in the ciliate class Karyorelictea. European Journal of Protistology, 61, 399-408.
Yao, M.-C. (2010) Modulating somatic DNA copy number through maternal RNA. Proceedings of the National Academy of Sciences of the United States of America, 107, 21951-21952.
Yerlici, V.T. & Landweber, L.F. (2014) Programmed genome rearrangements in the ciliate oxytricha. Microbiology Spectrum, 2, 2-6.
Yerlici, V.T., Lu, M.W., Hoge, C.R., Miller, R.V., Neme, R., Khurana, J.S. et al. (2019) Programmed genome rearrangements in Oxytricha produce transcriptionally active extrachromosomal circular DNA. Nucleic Acids Research, 47, 9741-9760.
Zufall, R.A., McGrath, C.L., Muse, S.V. & Katz, L.A. (2006) Genome architecture drives protein evolution in ciliates. Molecular Biology and Evolution, 23, 1681-1687.