Transposon debris in ciliate genomes

Feng, Yi; Landweber, Laura F.

doi:10.1371/journal.pbio.3001354

Cited by 5 publications

(4 citation statements)

References 13 publications

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“…This also suggests that TBE1 and TBE2 expanded in Oxytricha after its divergence from other hypotrichous ciliates. As illustrated in Figure 2—figure supplement 1 , the MIC genome contexts of TBEs in Oxytricha and Tetmemena are similar, with many TE insertions within IESs, consistent with either IESs as hotspots for TE insertion or with the model ( Klobutcher and Herrick, 1997 ) that some TE insertions may have generated IESs, as demonstrated in Paramecium ( Sellis et al, 2021 ; Feng and Landweber, 2021 ). Subsequent sequence evolution at the edges of IES/MDS pointers ( DuBois and Prescott, 1995 ) can give rise to boundaries that no longer correspond precisely to TBE ends.…”

Section: Resultssupporting

confidence: 61%

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

Feng

Neme

Beh

et al. 2022

eLife

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Ciliates are microbial eukaryotes that undergo extensive programmed genome rearrangement, a natural genome editing process that converts long germline chromosomes into smaller gene-rich somatic chromosomes. Three well-studied ciliates include Oxytricha trifallax, Tetrahymena thermophila and Paramecium tetraurelia, but only the Oxytricha lineage has a massively scrambled genome, whose assembly during development requires hundreds of thousands of precise programmed DNA joining events, representing the most complex genome dynamics of any known organism. Here we study the emergence of such complex genomes by examining the origin and evolution of discontinuous and scrambled genes in the Oxytricha lineage. This study compares six genomes from three species, the germline and somatic genomes for Euplotes woodruffi, Tetmemena sp., and the model ciliate Oxytricha trifallax. To complement existing data, we sequenced, assembled and annotated the germline and somatic genomes of Euplotes woodruffi, which provides an outgroup, and the germline genome of Tetmemena sp.. We find that the germline genome of Tetmemena is as massively scrambled and interrupted as Oxytricha's : 13.6% of its gene loci require programmed translocations and/or inversions, with some genes requiring hundreds of precise gene editing events during development. This study revealed that the earlier-diverged spirotrich, E. woodruffi, also has a scrambled genome, but only roughly half as many loci (7.3%) are scrambled. Furthermore, its scrambled genes are less complex, together supporting the position of Euplotes as a possible evolutionary intermediate in this lineage, in the process of accumulating complex evolutionary genome rearrangements, all of which require extensive repair to assemble functional coding regions. Comparative analysis also reveals that scrambled loci are often associated with local duplications, supporting a gradual model for the origin of complex, scrambled genomes via many small events of DNA duplication and decay.

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Section: Resultssupporting

confidence: 61%

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

Feng

Neme

Beh

et al. 2022

eLife

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“…Transposon proliferation stops (“abdication”) when its transposase is domesticated by a host promoter, releasing the transposons from purifying selection, whereupon their sequences erode by drift (“fade”). Depictions of the IBAF model usually show all the transposons expressing transposases during “bloom”, i.e., functioning as autonomous transposons ( 4 , 54 ). This is reasonable for Tetrahymena and Oxytricha , which have hundreds of germline-encoded transposases that vastly outnumber those in the somatic genome ( SI Appendix , Table S4 ).…”

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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“…This also suggests that TBE1 and TBE2 expanded in Oxytricha after its divergence from other hypotrichous ciliates. As illustrated in Figure S1, the MIC genome contexts of TBEs in Oxytricha and Tetmemena are similar, with many TE insertions within IESs, suggesting that some TE insertions may have generated IESs, as demonstrated in Paramecium (50,51). For further discussion of the conservation of TBE locations, see the section, "Oxytricha and Tetmemena share conserved rearrangement junctions'' below.…”

Section: Germline Genome Expansion Via Repetitive Elementsmentioning

confidence: 88%

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

Feng

Neme

Beh

et al. 2022

Preprint

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SummaryCiliates are microbial eukaryotes that undergo extensive programmed genome rearrangement that converts long germline chromosomes into smaller gene-rich somatic chromosomes. Three well-studied ciliates include Oxytricha trifallax, Tetrahymena thermophila and Paramecium tetraurelia, but only the Oxytricha lineage has a massively scrambled genome whose assembly requires hundreds of thousands of precise DNA joining events. Here we study the emergence of genome complexity by examining the origin and evolution of discontinuous and scrambled genes in the Oxytricha lineage.We sequenced, assembled and annotated the germline and somatic genomes of Euplotes woodruffi and the germline genome of Tetmemena sp., and compared their genome rearrangement features to that of the model ciliate Oxytricha trifallax. The germline genome of Tetmemena is as massively scrambled and interrupted as Oxytricha’s: 13.6% of its gene loci rearrange via translocations and/or inversions. This study revealed that the earlier-diverged spirotrich, E. woodruffi, also has a scrambled genome, but approximately half as many loci (7.3%) are scrambled, supporting its position as a possible evolutionary intermediate in this lineage, in the process of accumulating complex genome rearrangements. Scrambled loci are more often associated with local duplications, supporting a simple model for the origin of scrambled genes via DNA duplication and decay.

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Transposon debris in ciliate genomes

Cited by 5 publications

References 13 publications

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

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

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

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