One Cell, Two Gears: Extensive Somatic Genome Plasticity Accompanies High Germline Genome Stability in <i>Paramecium</i>

Catania, Francesco; Rothering, Rebecca; Vitali, Valerio

doi:10.1093/gbe/evab263

Cited by 4 publications

(4 citation statements)

References 63 publications

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“…The genome defense model may lead one to dismiss IES retention in the somatic genome as excisase inefficiency or MIC contamination of the library; however, IES excision is not all-or-nothing but a continuum. Experimental evolution experiments in Paramecium suggest IES retention variability is itself a plastic and evolvable trait with consequences for somatic genotypic diversity ( 60 , 61 ). Assembly algorithms tend to present an oversimplified, “pristine” view of somatic genomes, because they collapse repetitive and lower-coverage regions, which are characteristic of mobile elements and partially retained IESs.…”

Section: Discussionmentioning

confidence: 99%

MITE infestation accommodated by genome editing in the germline genome of the ciliate Blepharisma

Seah

Singh

Emmerich

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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During their development following sexual conjugation, ciliates excise numerous internal eliminated sequences (IESs) from a copy of the germline genome to produce the functional somatic genome. Most IESs are thought to have originated from transposons, but the presumed homology is often obscured by sequence decay. To obtain more representative perspectives on the nature of IESs and ciliate genome editing, we assembled 40,000 IESs of Blepharisma stoltei , a species belonging to a lineage (Heterotrichea) that diverged early from those of the intensively studied model ciliate species. About a quarter of IESs were short (<115 bp), largely nonrepetitive, and with a pronounced ~10 bp periodicity in length; the remainder were longer (up to 7 kbp) and nonperiodic and contained abundant interspersed repeats. Contrary to the expectation from current models, the assembled Blepharisma germline genome encodes few transposases. Instead, its most abundant repeat (8,000 copies) is a Miniature Inverted-repeat Transposable Element (MITE), apparently a deletion derivative of a germline-limited Pogo-family transposon. We hypothesize that MITEs are an important source of IESs whose proliferation is eventually self-limiting and that rather than defending the germline genomes against mobile elements, transposase domestication actually facilitates the accumulation of junk DNA.

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Section: Discussionmentioning

confidence: 99%

MITE infestation accommodated by genome editing in the germline genome of the ciliate Blepharisma

Seah

Singh

Emmerich

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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show abstract

“…The genome defense model may lead one to dismiss IES retention in the somatic genome as excisase inefficiency or MIC contamination of the library, however, IES excision is not all-or-nothing but a continuum. Experimental evolution experiments in Paramecium suggest IES retention variability is itself a plastic and evolvable trait with consequences for somatic genotypic diversity (Catania et al, 2021; Vitali et al, 2019). Assembly algorithms tend to present an oversimplified, “pristine” view of somatic genomes, because they collapse repetitive and lower-coverage regions, which are characteristic of mobile elements and partially retained IESs.…”

Section: Discussionmentioning

confidence: 99%

MITE infestation of germline accommodated by genome editing in Blepharisma

Seah

Singh

Emmerich

et al. 2022

Preprint

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During a sophisticated developmental process, ciliates excise numerous internally eliminated sequences (IESs) from a germline genome copy, producing a functional somatic genome. Most IESs ultimately originate from transposons but homology is obscured by sequence decay. To obtain more representative perspectives on ciliate genome editing, we assembled forty thousand IESs of Blepharisma stoltei, from a much earlier-diverging lineage than existing models. Short IESs (< 115 bp) were largely non-repetitive, with a pronounced ~10 bp length periodicity, whereas longer IESs (max 7 kbp) were non-periodic and contained abundant interspersed repeats. Contrary to current models, the Blepharisma germline genome encodes few transposases. Instead, its most abundant repeat (8000 copies) was a Miniature Inverted-repeat Transposable Element (MITE), apparently a deletion derivative of a germline-limited Pogo-family transposon. We propose MITEs as an important and eventually self-limiting IES source. Rather than defending germline genomes against mobile elements, we argue that transposase domestication actually facilitates junk DNA accumulation.

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“…For example, IESs are usually eliminated during the development of the new macronucleus. Occasionally, however, some IESs are retained in a small fraction of the alleles of a given locus in the macronucleus, especially under nonoptimal growth conditions, thereby introducing a unique structural form of somatic mutation (20,126). Although the fitness effects of mutations are also critical to evolution, for ciliates, this problem has only been explored in T. thermophila, which has a mean fitness effect of 0.11, that is, an average 11% fitness drop per mutation, similar to what has been found in other organisms (35,128), and thus this is a subject worthy of more research in the future (74).…”

Section: The Population-genetic Environmentmentioning

confidence: 99%

Paramecium Genetics, Genomics, and Evolution

Long,

Johri,

Gout

et al. 2023

Annu. Rev. Genet.

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The ciliate genus Paramecium served as one of the first model systems in microbial eukaryotic genetics, contributing much to the early understanding of phenomena as diverse as genome rearrangement, cryptic speciation, cytoplasmic inheritance, and endosymbiosis, as well as more recently to the evolution of mating types, introns, and roles of small RNAs in DNA processing. Substantial progress has recently been made in the area of comparative and population genomics. Paramecium species combine some of the lowest known mutation rates with some of the largest known effective populations, along with likely very high recombination rates, thereby harboring a population-genetic environment that promotes an exceptionally efficient capacity for selection. As a consequence, the genomes are extraordinarily streamlined, with very small intergenic regions combined with small numbers of tiny introns. The subject of the bulk of Paramecium research, the ancient Paramecium aurelia species complex, is descended from two whole-genome duplication events that retain high degrees of synteny, thereby providing an exceptional platform for studying the fates of duplicate genes. Despite having a common ancestor dating to several hundred million years ago, the known descendant species are morphologically indistinguishable, raising significant questions about the common view that gene duplications lead to the origins of evolutionary novelties.

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One Cell, Two Gears: Extensive Somatic Genome Plasticity Accompanies High Germline Genome Stability in Paramecium

Cited by 4 publications

References 63 publications

MITE infestation accommodated by genome editing in the germline genome of the ciliate Blepharisma

MITE infestation accommodated by genome editing in the germline genome of the ciliate Blepharisma

MITE infestation of germline accommodated by genome editing in Blepharisma

Paramecium Genetics, Genomics, and Evolution

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