piRNAs and Evolutionary Trajectories in Genome Size and Content

Mueller, Rachel Lockridge

doi:10.1007/s00239-017-9818-4

Cited by 9 publications

(6 citation statements)

References 17 publications

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“…Maintenance of genomic integrity over generations is a key selective process as rapid "cut/copy and paste" mechanisms of TEs constantly threaten genomic stability (81). To counter this, specific silencing pathways involving Piwi and piRNA genes are known to be widely employed across eukaryotic lineages (51,52). In animals, these silencing pathways are particularly important in germline cells as a major line of defense to withstand genomic instability (54).…”

Section: Discussionmentioning

confidence: 99%

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A bird-like genome from a frog: Mechanisms of genome size reduction in the ornate burrowing frog, Platyplectrum ornatum

Lamichhaney

Catullo

Keogh

et al. 2021

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

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The diversity of genome sizes across the tree of life is of key interest in evolutionary biology. Various correlates of variation in genome size, such as accumulation of transposable elements (TEs) or rate of DNA gain and loss, are well known, but the underlying molecular mechanisms driving or constraining genome size are poorly understood. Here, we study one of the smallest genomes among frogs characterized thus far, that of the ornate burrowing frog (Platyplectrum ornatum) from Australia, and compare it to other published frog and vertebrate genomes to examine the forces driving reduction in genome size. At ∼1.06 gigabases (Gb), the P. ornatum genome is like that of birds, revealing four major mechanisms underlying TE dynamics: reduced abundance of all major classes of TEs; increased net deletion bias in TEs; drastic reduction in intron lengths; and expansion via gene duplication of the repertoire of TE-suppressing Piwi genes, accompanied by increased expression of Piwi-interacting RNA (piRNA)-based TE-silencing pathway genes in germline cells. Transcriptomes from multiple tissues in both sexes corroborate these results and provide insight into sex-differentiation pathways in Platyplectrum. Genome skimming of two closely related frog species (Lechriodus fletcheri and Limnodynastes fletcheri) confirms a reduction in TEs as a major driver of genome reduction in Platyplectrum and supports a macroevolutionary scenario of small genome size in frogs driven by convergence in life history, especially rapid tadpole development and tadpole diet. The P. ornatum genome offers a model for future comparative studies on mechanisms of genome size reduction in amphibians and vertebrates generally.

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Section: Discussionmentioning

confidence: 99%

“…Piwi-Interacting RNAs. Piwi proteins and Piwi-interacting RNAs (piRNAs) play key roles in suppressing TEs (51,52). A recent study in fish with miniaturized genomes suggested copy number expansion of Piwi genes as a potential driver of reduced TE abundances via transposon silencing (12).…”

Section: Diversification and Increased Expression Of Piwi Proteins Andmentioning

confidence: 99%

A bird-like genome from a frog: Mechanisms of genome size reduction in the ornate burrowing frog, Platyplectrum ornatum

Lamichhaney

Catullo

Keogh

et al. 2021

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

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“…The expansion of the genome is not out of control. Studies have uncovered the Piwi-interacting RNA (piRNA) pathway, a small RNA genome defense system that suppresses TE activity in the animal germline (Mueller, 2017 ). piRNAs limit the expansion of genome size by guiding the transcription and post-transcriptional silencing of TEs through base complementarity.…”

Section: Discussionmentioning

confidence: 99%

The Evolutionary Patterns of Genome Size in Ensifera (Insecta: Orthoptera)

et al. 2021

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Genomic size variation has long been a focus for biologists. However, due to the lack of genome size data, the mechanisms behind this variation and the biological significance of insect genome size are rarely studied systematically. The detailed taxonomy and phylogeny of the Ensifera, as well as the extensive documentation concerning their morphological, ecological, behavioral, and distributional characteristics, make them a strong model for studying the important scientific problem of genome size variation. However, data on the genome size of Ensifera are rather sparse. In our study, we used flow cytometry to determine the genome size of 32 species of Ensifera, the smallest one being only 1C = 0.952 pg with the largest species up to 1C = 19.135 pg, representing a 20-fold range. This provides a broader blueprint for the genome size variation of Orthoptera than was previously available. We also completed the assembly of nine mitochondrial genomes and combined mitochondrial genome data from public databases to construct phylogenetic trees containing 32 species of Ensifera and three outgroups. Based on these inferred phylogenetic trees, we detected the phylogenetic signal of genome size variation in Ensifera and found that it was strong in both males and females. Phylogenetic comparative analyses revealed that there were no correlations between genome size and body size or flight ability in Tettigoniidae. Reconstruction of ancestral genome size revealed that the genome size of Ensifera evolved in a complex pattern, in which the genome size of the grylloid clade tended to decrease while that of the non-grylloid clade expanded significantly albeit with fluctuations. However, the evolutionary mechanisms underlying variation of genome size in Ensifera are still unknown.

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“…How these forces interact to generate genome size diversity across the tree of life remains incompletely understood. Groups of related species that vary in TE load and genome size provide critical model systems for studying this fundamental question [24] .…”

Section: Introductionmentioning

confidence: 99%

Gigantic Genomes Provide Empirical Tests of Transposable Element Dynamics Models

Wang

Itgen

Wang

et al. 2021

Genomics, Proteomics &Amp; Bioinformatics

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Transposable elements (TEs) are a major determinant of eukaryotic genome size . The collective properties of a genomic TE community reveal the history of TE/host evolutionary dynamics and impact present-day host structure and function, from genome to organism levels. In rare cases, TE community/genome size has greatly expanded in animals, associated with increased cell size and changes to anatomy and physiology. Here, we characterize the TE landscape of the genome and transcriptome in an amphibian with a giant genome — the caecilian Ichthyophis bannanicus , which we show has a genome size of 12.2 Gb. Amphibians are an important model system because the clade includes independent cases of genomic gigantism. The I. bannanicus genome differs compositionally from other giant amphibian genomes, but shares a low rate of ectopic recombination-mediated deletion. We examine TE activity using expression and divergence plots; TEs account for 15% of somatic transcription, and most superfamilies appear active. We quantify TE diversity in the caecilian, as well as other vertebrates with a range of genome sizes, using diversity indices commonly applied in community ecology. We synthesize previous models that integrate TE abundance, diversity, and activity, and test whether the caecilian meets model predictions for genomes with high TE abundance. We propose thorough, consistent characterization of TEs to strengthen future comparative analyses. Such analyses will ultimately be required to reveal whether the divergent TE assemblages found across convergent gigantic genomes reflect fundamental shared features of TE/host genome evolutionary dynamics.

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piRNAs and Evolutionary Trajectories in Genome Size and Content

Cited by 9 publications

References 17 publications

A bird-like genome from a frog: Mechanisms of genome size reduction in the ornate burrowing frog, Platyplectrum ornatum

A bird-like genome from a frog: Mechanisms of genome size reduction in the ornate burrowing frog, Platyplectrum ornatum

The Evolutionary Patterns of Genome Size in Ensifera (Insecta: Orthoptera)

Gigantic Genomes Provide Empirical Tests of Transposable Element Dynamics Models

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