Sequence-Specific Epigenetic Effects of the Maternal Somatic Genome on Developmental Rearrangements of the Zygotic Genome in<i>Paramecium primaurelia</i>

Meyer, Éric; Butler, Alain; Dubrana, Karine; Duharcourt, Sandra; Caron, François

doi:10.1128/mcb.17.7.3589

Cited by 38 publications

(27 citation statements)

References 45 publications

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“…6C). These molecular features are strikingly similar to those of transgene-induced internal deletions in P. primaurelia (27).…”

Section: Resultssupporting

confidence: 58%

“…Like the A gene deletion in d48, the induced macronuclear deletion is maternally transmitted to sexual progeny, although genetic analyses confirmed that the germ line genome of the micronuclei remains wild type. The maternal deletion effect was observed with all sequences tested, including noncoding sequences; targeting a subtelomeric gene resulted in terminal deletions, while targeting an internal sequence resulted in heterogeneous internal deletions of the homologous zygotic sequence (23,27). The sequence specificity of this trans-nuclear effect is therefore likely to be achieved by the pairing of homologous nucleic acids.…”

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confidence: 90%

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RNA-Mediated Programming of Developmental Genome Rearrangements in Paramecium tetraurelia

Garnier

Serrano

Duharcourt

et al. 2004

Molecular and Cellular Biology

128

135

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The germ line genome of ciliates is extensively rearranged during development of the somatic macronucleus. Numerous sequences are eliminated, while others are amplified to a high ploidy level. In the Paramecium aurelia group of species, transformation of the maternal macronucleus with transgenes at high copy numbers can induce the deletion of homologous genes in sexual progeny, when a new macronucleus develops from the wild-type germ line. We show that this trans-nuclear effect correlates with homology-dependent silencing of maternal genes before autogamy and with the accumulation of ϳ22-to 23-nucleotide (nt) RNA molecules. The same effects are induced by feeding cells before meiosis with bacteria containing double-stranded RNA, suggesting that small interfering RNA-like molecules can target deletions. Furthermore, experimentally induced macronuclear deletions are spontaneously reproduced in subsequent sexual generations, and reintroduction of the missing gene into the variant macronucleus restores developmental amplification in sexual progeny. We discuss the possible roles of the ϳ22-to 23-nt RNAs in the targeting of deletions and the implications for the RNA-mediated genome-scanning process that is thought to determine developmentally regulated rearrangements in ciliates.

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“…6C). These molecular features are strikingly similar to those of transgene-induced internal deletions in P. primaurelia (27).…”

Section: Resultssupporting

confidence: 58%

mentioning

confidence: 90%

RNA-Mediated Programming of Developmental Genome Rearrangements in Paramecium tetraurelia

Garnier

Serrano

Duharcourt

et al. 2004

Molecular and Cellular Biology

128

135

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“…4 shows hybridization of the blot with probe f, revealing the BstBI-MnlI fragment containing 51A-712. The retention of this IES is observed only in the postautogamous progeny of the clone transformed with the highest copy number of p51A-712mic (9.9 copies phg, lane 10; the weak signals in lanes 7 and 10 are due to a different effect of high-copy-number transformation with cloned macronuclear or micronuclear sequences, which causes imprecise deletions of the homologous regions of the germ line genome during development of a new macronucleus [8,26,30]). Retention of 51A-712 is not observed in the progeny of clones transformed with p51A-712mac, even at 15.6 copies phg, or with p29A6649mic.…”

Section: Resultsmentioning

confidence: 99%

“…The model easily accounts for the observed sequence specificity; furthermore, the dependence of inhibition efficiency on the length of IES flanking sequences could be explained by differences in pairing efficiency. Although there is no direct evidence, a transfer of nucleic acids between the two nuclei is also likely to be involved in another type of homology-dependent maternal effects on macronuclear development in Paramecium spp., affecting the level of amplification of macronucleus-destined sequences (27,28,30). RNA would seem to be a better candidate than DNA for a messenger molecule able to leave one nucleus and enter another.…”

Section: Discussionmentioning

confidence: 99%

Homology-Dependent Maternal Inhibition of Developmental Excision of Internal Eliminated Sequences inParamecium tetraurelia

Duharcourt

Keller

Meyer

1998

Molecular and Cellular Biology

110

124

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Thousands of single-copy internal eliminated sequences (IESs) are excised from the germ line genome of ciliates during development of the polygenomic somatic macronucleus, following sexual events. Paramecium IESs are short, noncoding elements that frequently interrupt coding sequences. No absolutely conserved sequence element, other than flanking 5-TA-3 direct repeats, has been identified among sequenced IESs; the mechanisms of their specific recognition and precise elimination are unknown. Previous work has revealed the existence of an epigenetic control of excision. It was shown that the presence of one IES in the vegetative macronucleus results in a specific inhibition of the excision of the same element during the development of a new macronucleus, in the following sexual generation. We have assessed the generality and sequence specificity of this transnuclear maternal control by studying the effects of macronuclear transformation with 13 different IESs. We show that at least five of them can be maintained in the new macronuclear genome; sequence specificity is complete both between genes and between different IESs in the same gene. In all cases, the degree of excision inhibition correlates with the copy number of the maternal IES, but each IES shows a characteristic inhibition efficiency. Short internal IES-like segments were found to be excised from two of the IESs when excision between normal boundaries was inhibited. Available data suggest that the sequence specificity of these maternal effects is mediated by pairing interactions between homologous nucleic acids.Ciliates are unicellular eukaryotes in which germ line and somatic functions are assumed by two kinds of nuclei coexisting in the same cytoplasm. The diploid micronuclei are transcriptionally silent during vegetative growth; their main function is to provide gametic nuclei upon meiosis. Vegetative transcription takes place in the polygenomic, somatic macronuclei that divide amitotically and are lost soon after meiosis. Following fertilization, both kinds of nuclei differentiate from copies of the diploid zygotic nucleus. Macronuclear development involves extensive rearrangements of the germ line genome: chromosomes are fragmented into shorter, acentric molecules, and tens of thousands of internally eliminated sequences (IESs) are removed from coding and noncoding sequences, in a reproducible and often highly precise manner. In addition, the genome is amplified to the final ploidy level, ϳ1,000n in Paramecium aurelia complex species (for general reviews, see references 5 and 34; for a review of IESs, see reference 19).All known Paramecium IESs are short (26 to 882 bp), ATrich, single-copy elements flanked by 5Ј-TA-3Ј direct repeats in the germ line sequence. Excision invariably leaves one of the TA repeats in the rearranged macronuclear sequence, suggesting that the same basic mechanism is used for all IESs. Although the excision mechanism is currently unknown, reaction products and intermediates have been identified in other ciliate species. In E...

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“…Until recently, the signals for chromosomal rearrangements were believed to be located predominantly in the zygotic nucleus, while the parental MAC, which eventually fragments and disappears, was thought to play a minimal role. Data on the role of the parental MAC in directing chromosomal rearrangements in the newly developing MACs of Paramecium and Tetrahymena (Duharcourt et al, 1995(Duharcourt et al, , 1998Meyer et al, 1997 ;Meyer & Duharcourt, 1996) provide a relatively plastic mechanism of chromosomal rearrangements that may have allowed for the observed diversity in chromosomal processing among ciliate MACs.…”

Section: A New Modelmentioning

confidence: 99%

Evolution of nuclear dualism in ciliates: a reanalysis in light of recent molecular data.

Katz¹

2001

International Journal of Systematic and Evolutionary Microbiology

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Ciliates are defined by the presence of dimorphic nuclei. Following conjugation, both the functional macronucleus (MAC) and the transcriptionally inactive germline micronucleus (MIC) develop from a zygotic nucleus. As the MAC develops, germline chromosomes are processed by excision of internal sequences, fragmentation and amplification of the remaining chromosomes. The extent of processing varies among lineages and, in all but one class of ciliates, the resulting MACs divide by an unusual process termed ' amitosis '. Research on these chromosomal rearrangements, largely from studies of only a handful of taxa from two of the nine classes of ciliates, has failed to find evidence of homologous processing among ciliate lineages. This observation, coupled with the structural diversity of MAC genomes among ciliates, led to the hypothesis of multiple origins of at least two MAC properties : (1) the ability to divide and (2) the mechanisms underlying chromosomal processing. Applying this logic to a more inclusive analysis of ciliate lineages, where an even greater diversity of MAC structure is observed, increases the potential number of origins of these MAC characteristics. Here, it is proposed that a single origin of a relatively plastic mechanism underlying MAC development better explains the observed diversity in MAC structure and processing among ciliates. Such a mechanism is suggested by the demonstration of epigenetic effects during MAC development in Paramecium and Tetrahymena.

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Sequence-Specific Epigenetic Effects of the Maternal Somatic Genome on Developmental Rearrangements of the Zygotic Genome inParamecium primaurelia

Cited by 38 publications

References 45 publications

RNA-Mediated Programming of Developmental Genome Rearrangements in Paramecium tetraurelia

RNA-Mediated Programming of Developmental Genome Rearrangements in Paramecium tetraurelia

Homology-Dependent Maternal Inhibition of Developmental Excision of Internal Eliminated Sequences inParamecium tetraurelia

Evolution of nuclear dualism in ciliates: a reanalysis in light of recent molecular data.

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