Natural genetic engineering: A programmed chromosome/DNA elimination

Kloc, Małgorzata; Kubiak, Jacek Z.; Ghobrial, Rafik M.

doi:10.1016/j.ydbio.2022.03.008

Cited by 11 publications

(12 citation statements)

References 92 publications

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“…Programmed DNA elimination was first described by Boveri in the 1880s, yet the molecular details, mechanistic underpinnings, and functional importance of PDE are largely unknown, particular in multicellular organisms. [5][6][7][8][9] Functional studies on metazoa PDE are lacking, largely due to the absence of a tractable model, where animals with mutations that alter the PDE process can be analyzed. In this study, we illustrate that O. tipulae, a free-living nematode with a 60-Mb genome, can be used as a functional and genetic model to study PDE.…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, programmed DNA elimination (PDE) is a dramatic form of genome change with large amounts of DNA, ranging from 0.5 to 95% of the genome, eliminated during development. [5][6][7][8][9] PDE is highly selective and reproducible and is an integral part of biology for diverse organisms.…”

Section: Introductionmentioning

confidence: 99%

“…15,16,28 A common theme emerging from these recent genomics studies is the removal of both germline-expressed genes and repetitive sequences during PDE. [5][6][7][8][9] This suggests that one function of PDE in metazoa is to permanently silence certain germline sequences potentially harmful to somatic cells. 6 PDE is also used for sex determination, 7,13,15 remodeling chromosome ends and splitting fused chromosomes, 22 and appears to be a mechanism for novel gene and chromosome evolution.…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…6 PDE is also used for sex determination, 7,13,15 remodeling chromosome ends and splitting fused chromosomes, 22 and appears to be a mechanism for novel gene and chromosome evolution. 6,8,9 Despite the detailed genomic and cytological descriptions of PDE in many organisms, functional and mechanistic studies of metazoan PDE are limited. 29,30 Mechanistic insights for PDE, including the contributions and roles of transposable elements and small RNAs, have primarily been gleaned from single-cell ciliates.…”

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confidence: 99%

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The Nematode Oscheius tipulae as A Genetic Model for Programmed DNA Elimination

Dockendorff

Estrem

Reed

et al. 2022

Preprint

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Programmed DNA elimination (PDE) is a notable exception to the paradigm of genome integrity. In metazoa, PDE often occurs during early embryogenesis, coincident with germline to somatic cell differentiation. During PDE, portions of genomic DNA are lost, resulting in reduced somatic genomes. Recent studies have described the sequences lost and chromosome behavior in metazoa. However, a system for studying the mechanisms and consequences of PDE in metazoa is lacking. Here, we established a functional and genetic model for PDE in the free-living nematode Oscheius tipulae, a member of the Rhabditidae family, which includes Caenorhabditis elegans. O. tipulae was recently suggested to eliminate DNA. Using staged embryos, we show that O. tipulae PDE occurs during embryogenesis at the 2-16 cell stages, similar to the human/pig parasitic nematode Ascaris. We identified a conserved motif, named Sequence For Elimination (SFE), for all 12 break sites on the six chromosomes at the junction of retained and eliminated DNA. SFE mutants exhibit a "fail-to-eliminate" phenotype only at the modified sites. END-seq revealed that breaks can occur at multiple positions within the SFE, with extensive end resection followed by telomere addition to both retained and eliminated ends. We identified through END-seq in the wild-type embryos, genome sequencing of SFE mutants, and comparative genomics of 23 wild isolates a large number of functional SFEs at the chromosome ends. We suggest these alternative SFEs provide flexibility in the sequences eliminated and a fail-safe mechanism for PDE. These studies establish O. tipulae as a new, attractive model to study the mechanisms and consequences of PDE in a metazoan.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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The Nematode Oscheius tipulae as A Genetic Model for Programmed DNA Elimination

Dockendorff

Estrem

Reed

et al. 2022

Preprint

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Molecular characterization of eliminated chromosomes in Hessian fly (Mayetiola destructor (Say))

Crane

Cambron

et al. 2023

Chromosome Res

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Like other cecidomyiid Diptera, Hessian fly has stable S chromosomes and dispensable E chromosomes that are retained only in the germ line. Amplified fragment length polymorphisms (AFLP), suppressive subtractive hybridization (SSH), fluorescent in-situ hybridization (FISH), and sequencing were used to investigate similarities and differences between S and E chromosomes. More than 99.9% of AFLP bands were identical between separated ovary and somatic tissue, but one band was unique to ovary and resembled Worf, a non-LTR retrotransposon. Arrayed clones, derived by SSH of somatic from ovarian DNA, showed no clones that were unique to ovary. FISH with BAC clones revealed a diagnostic banding pattern of BAC positions on both autosomes and both sex chromosomes, and each E chromosome shared a pattern with one of the S chromosomes. Sequencing analysis showed that E chromosomes are nearly identical to S chromosomes, since no sequence could be confirmed to belong only to E chromosomes. There were a few questionably E-specific sequences that are candidates for further investigation. Thus, the E chromosomes appear to be derived from S chromosomes by the acquisition or conversion of sequences that produce the negatively heteropycnotic region around the centromere.

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