Functional Study of Genes Essential for Autogamy and Nuclear Reorganization in Paramecium

Nowak, J; Gromadka, Robert; Juszczuk, Marek; Jerka‐Dziadosz, Maria; Maliszewska, Kamila; Mucchielli, Marie-Hélène; Goût, Jean-François; Arnaiz, Olivier; Agier, Nicolas; Tang, Thomas S. Y.; Aggerbeck, Lawrence P.; Cohen, Jean; Delacroix, Hervé; Sperling, Linda; Herbert, Christopher J.; Zagulski, Marek; Bétermier, Mireille

doi:10.1128/ec.00258-10

Cited by 18 publications

(18 citation statements)

References 43 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Only a handful of key factors playing role in Paramecium genome development have been described so far [3] , [15] , [16] , [21] , [35] . A common feature of all these genes is the transcriptional upregulation during sexual reproduction.…”

Section: Resultsmentioning

confidence: 99%

Pdsg1 and Pdsg2, Novel Proteins Involved in Developmental Genome Remodelling in Paramecium

et al. 2014

View full text Add to dashboard Cite

The epigenetic influence of maternal cells on the development of their progeny has long been studied in various eukaryotes. Multicellular organisms usually provide their zygotes not only with nutrients but also with functional elements required for proper development, such as coding and non-coding RNAs. These maternally deposited RNAs exhibit a variety of functions, from regulating gene expression to assuring genome integrity. In ciliates, such as Paramecium these RNAs participate in the programming of large-scale genome reorganization during development, distinguishing germline-limited DNA, which is excised, from somatic-destined DNA. Only a handful of proteins playing roles in this process have been identified so far, including typical RNAi-derived factors such as Dicer-like and Piwi proteins. Here we report and characterize two novel proteins, Pdsg1 and Pdsg2 (Paramecium protein involved in Development of the Somatic Genome 1 and 2), involved in Paramecium genome reorganization. We show that these proteins are necessary for the excision of germline-limited DNA during development and the survival of sexual progeny. Knockdown of PDSG1 and PDSG2 genes affects the populations of small RNAs known to be involved in the programming of DNA elimination (scanRNAs and iesRNAs) and chromatin modification patterns during development. Our results suggest an association between RNA-mediated trans-generational epigenetic signal and chromatin modifications in the process of Paramecium genome reorganization.

show abstract

Section: Resultsmentioning

confidence: 99%

Pdsg1 and Pdsg2, Novel Proteins Involved in Developmental Genome Remodelling in Paramecium

et al. 2014

View full text Add to dashboard Cite

show abstract

“…For TFIIS2a and 2b , we also performed double silencing experiments by mixing induced bacteria designed to silence individual genes. The effect of each RNAi was first examined for ~8 vegetative divisions by monitoring cell division rate and general morphology, as described in [ 40 ]. None of the silencing experiments gave an obvious phenotype during this period of vegetative growth.…”

Section: Resultsmentioning

confidence: 99%

TFIIS-Dependent Non-coding Transcription Regulates Developmental Genome Rearrangements

Maliszewska‐Olejniczak

Gruchota

Gromadka

et al. 2015

PLoS Genet

Self Cite

View full text Add to dashboard Cite

Because of their nuclear dimorphism, ciliates provide a unique opportunity to study the role of non-coding RNAs (ncRNAs) in the communication between germline and somatic lineages. In these unicellular eukaryotes, a new somatic nucleus develops at each sexual cycle from a copy of the zygotic (germline) nucleus, while the old somatic nucleus degenerates. In the ciliate Paramecium tetraurelia, the genome is massively rearranged during this process through the reproducible elimination of repeated sequences and the precise excision of over 45,000 short, single-copy Internal Eliminated Sequences (IESs). Different types of ncRNAs resulting from genome-wide transcription were shown to be involved in the epigenetic regulation of genome rearrangements. To understand how ncRNAs are produced from the entire genome, we have focused on a homolog of the TFIIS elongation factor, which regulates RNA polymerase II transcriptional pausing. Six TFIIS-paralogs, representing four distinct families, can be found in P. tetraurelia genome. Using RNA interference, we showed that TFIIS4, which encodes a development-specific TFIIS protein, is essential for the formation of a functional somatic genome. Molecular analyses and high-throughput DNA sequencing upon TFIIS4 RNAi demonstrated that TFIIS4 is involved in all kinds of genome rearrangements, including excision of ~48% of IESs. Localization of a GFP-TFIIS4 fusion revealed that TFIIS4 appears specifically in the new somatic nucleus at an early developmental stage, before IES excision. RT-PCR experiments showed that TFIIS4 is necessary for the synthesis of IES-containing non-coding transcripts. We propose that these IES+ transcripts originate from the developing somatic nucleus and serve as pairing substrates for germline-specific short RNAs that target elimination of their homologous sequences. Our study, therefore, connects the onset of zygotic non coding transcription to the control of genome plasticity in Paramecium, and establishes for the first time a specific role of TFIIS in non-coding transcription in eukaryotes.

show abstract

“…Dissociation of Twi1p from scnRNAs paired with maternal ncRNAs might result in scnRNA degradation and recycling of Twi1p (Aronica et al, 2008). In Paramecium, the putative RNA helicase Ptmb.220p is required for DNA rearrangements and might play a role similar to its Tetrahymena counterpart Ema1p (Nowak et al, 2011). The RNA‐binding, GW repeat‐containing Nowa1 and 2 proteins in Paramecium , which are required for the excision of mcIESs and transposons, localise to the parental macronucleus and have been suggested to participate in the scanning process (Nowacki et al, 2005), but further work is needed to precisely determine their role.…”

Section: Rna‐guided Programmed Genome Rearrangementsmentioning

confidence: 99%

RNA‐guided DNA rearrangements in ciliates: Is the best genome defence a good offence?

Coyne

Lhuillier-Akakpo

Duharcourt

2012

Biology of the Cell

View full text Add to dashboard Cite

Genomes, like crazy patchwork quilts, are stitched together over evolutionary time from diverse elements, including some unwelcome invaders. To deal with parasitic mobile elements, most eukaryotes employ a genome self-defensive manoeuvre to recognise and silence such elements by homology-dependent interactions with RNA-protein complexes that alter chromatin. Ciliated protozoa employ more 'offensive' tactics by actually unstitching and reassembling their somatic genomes at every sexual generation to eliminate transposons and their remnants, using as patterns the maternal genomes that were rearranged in the previous cycle. Genetic and genomic studies of the distant relatives Paramecium and Tetrahymena have begun to reveal how such events are carried out with remarkable precision. Whole genome, non-coding transcripts from the maternal genome are compared with transcripts from the zygotic genome that are processed through an RNA interference (RNAi)-related process. Sequences found only in the latter are targeted for elimination by the resulting short 'scanRNAs' in many thousand DNA splicing reactions initiated by a domesticated transposase. The involvement of widely conserved mechanisms and protein factors clearly shows the relatedness of these phenomena to RNAi-mediated heterochromatic gene silencing. Such malleability of the genome on a generational time scale also has profound evolutionary implications, possibly including the epigenetic inheritance of acquired adaptive traits.

show abstract

Functional Study of Genes Essential for Autogamy and Nuclear Reorganization in Paramecium

Cited by 18 publications

References 43 publications

Pdsg1 and Pdsg2, Novel Proteins Involved in Developmental Genome Remodelling in Paramecium

Pdsg1 and Pdsg2, Novel Proteins Involved in Developmental Genome Remodelling in Paramecium

TFIIS-Dependent Non-coding Transcription Regulates Developmental Genome Rearrangements

RNA‐guided DNA rearrangements in ciliates: Is the best genome defence a good offence?

Contact Info

Product

Resources

About