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

Abstract

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.

The genome sequence of the avian vampire fly (Philornis downsi), an invasive nest parasite of Darwin's finches in Galapagos

“…Furthermore, TE may also be a critical mechanism of adaptive evolution, as has been shown in an invasive ant species (Schrader et al, 2014). Analysis of transposable elements in P. downsi and across other dipteran genomes showed a strong positive correlation between genome size and repeat content (Figure 2a), consistent with similar findings across other taxa (Lynch, 2007;Lamichhaney et al, 2021). Interestingly, P. downsi had a higher number of DNA transposons (Class II TEs) than any other compared genome, including M. domestica, S.…”

“…The mean number of exons per gene is fewer in P. downsi compared to the other two species. (Kapusta et al, 2017;Lamichhaney et al, 2021), and important contributors to the evolutionary potential of an organism (Pourrajab and Hekmatimoghaddam, 2021). We characterized the transposable elements in the P. downsi genome using homology-based (Smit Hubley P., 2013) and de-novo approaches (Flynn et al, 2019).…”

Genome size evolution in the diverse insect order Trichoptera

“…Thus, the shift to large genomes in these lineages does not appear to be due to a single (or few) shared ancient events, rather the they maintain dynamic turnover in composition in their large genomes. Mutational bias affecting pathways tied to TEregulation may affect insertion/deletion ratios and subsequently lead to lineage-specific shifts in genome size equilibrium (67). Such changes may be stochastic (e.g., due to drift), or linked to traits that evolve on independent trajectories as lineages diverge, and are thereby constrained by phylogeny.…”

Profile of Scott Edwards

“…One way to shrink a genome is to reduce the proliferation of transposable elements, which are pieces of DNA that can copy and paste themselves throughout an organism's genome. Edwards and colleagues identified Piwi genes in the frog that are known to suppress transposable elements (1). "We know that transposable elements often proliferate in the germline, and so we were very excited when we found evidence for gene duplication of Piwi-interacting RNA genes, as well as really high expression in the germline as opposed to other tissues.…”

“…Zoologist and curator of ornithology of Harvard's Museum of Comparative Zoology, Edwards was elected to the National Academy of Sciences in 2015. Although Edwards primarily uses birds as models to study molecular evolution and biodiversity, he took a foray into amphibians in his Inaugural Article (1), analyzing the diminutive genome of the ornate burrowing frog. In the past, he has documented rapid genomic shifts in green anole lizards in response to winter storms in the southern United States and examined the genome sizes of organisms, ranging from bacteriophages to dinosaurs (2)(3)(4).…”