Transposons contribute to the functional diversification of the head, gut, and ovary transcriptomes across<i>Drosophila</i>natural strains

Coronado-Zamora, Marta; Pérez, Josefa González

doi:10.1101/2022.12.02.518890

Cited by 6 publications

(10 citation statements)

References 89 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We identified a regulatory allele of the Cad96Ca gene, a transposable element inserted in its 3'UTR (Cad96Ca [I-element] ), which showed a strong signature of selection in all D907 and Mix selection lines. TE insertions in the 3'UTR of coding genes are associated with reduced levels of gene expression in flies 46 , humans and mice 47 , which may be mediated by a post-transcriptional TE silencing mechanism 43 . We found that the genetic variation spanning the Cad96Ca locus was maintained in the D907 ancestral population by the presence of the large chromosomal inversion In(3R)C, probably by preventing genetic homogenization within this chromosomal segment 38 .…”

Section: Discussionmentioning

confidence: 99%

The mechanistic basis of genetic assimilation in natural fly populations

Cavalli,

Sabarís,

Schuettengruber

et al. 2024

Preprint

Self Cite

View full text Add to dashboard Cite

Genetic assimilation is a process by which a trait originally driven by the environment becomes independent of the initial cue and is expressed constitutively in a population. More than seven decades have passed since Waddington's pioneering demonstration of the acquisition of morphological traits through genetic assimilation, but the underlying mechanism remains unknown. Here, we address this gap by performing a multi-omic analysis of Waddington's genetic assimilation using the ectopic veins phenocopy in Drosophila as a model. Our study reveals the assimilation of ectopic veins in both outbred and inbred fly natural populations, despite their initially limited genetic diversity. The assimilation of ectopic veins is driven by the selection of regulatory alleles already present in the ancestral populations, including downregulation of the Cad96Ca tyrosine kinase gene by the insertion of a transposable element in its 3' untranslated region. The genetic variation at this locus in the inbred population is maintained by a large chromosomal inversion. In outbred populations, the evolution of ectopic veins results from a polygenic response shaped by the selective environment. Our results support a model in which selection for multiple pre-existing alleles in the ancestral population, rather than stress-induced genetic or epigenetic variation, drives the evolution of ectopic veins in natural fly populations.

show abstract

Section: Discussionmentioning

confidence: 99%

The mechanistic basis of genetic assimilation in natural fly populations

Cavalli,

Sabarís,

Schuettengruber

et al. 2024

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Keeping in mind, that correlations do not indicate direction and can also be caused by indirect relationships, several plausible explanations exist for these positive interactions. Firstly, some TEs can function as cis -acting regulatory elements capable of influencing the expression of nearby genes, which have been mentioned to be tissue-specifically co-opted TEs (Sentmanat and Elgin 2012; Wolf et al 2020; Coronado-Zamora and González 2023). Additionally, it is conceivable that the expression levels of KRAB-ZNF genes themselves are influenced by their ability to sense the presence and activity of TEs within the genome (Pontis et al 2019; Senft and Macfarlan 2021).…”

Section: Discussionmentioning

confidence: 99%

Regulatory networks of KRAB zinc finger genes and transposable elements changed during human brain evolution and disease

Chen,

Maupas,

Nowick

2023

Preprint

View full text Add to dashboard Cite

Transposable elements (TEs), with their ability to change positions within a genome, have paradoxically been seen as both a potentially deleterious genomic phenomenon and a potent driving force behind evolution. The genome-protecting KRAB zinc finger (KRAB-ZNF) proteins play a critical role in repressing TE expression within mammalian genomes, engaging in a dynamic interplay. This interplay was suggested to evolve according to an arms-race model, wherein TEs strive to transpose within the genome and KRAB-ZNFs adapt to suppress them. Despite indications of the involvement of TEs and KRAB-ZNFs in brain evolution and disease, a systematic analysis of their interactions is still lacking. In this study, we explored the functional connections between KRAB-ZNFs and TEs in the context of human brain evolution and Alzheimer’s disease (AD). We conducted an analysis of KRAB-ZNF genes and TEs expression patterns and networks using two independent RNA-seq datasets: (1) data from 33 human and multiple non-human primate brain regions, and (2) data from the temporal cortex and cerebellum of both healthy individuals and AD patients. To efficiently compare the regulatory networks across species, we developed the TEKRABber R package, which enables estimating TE and KRAB-ZNF expression levels and pairwise correlations between them, facilitating cross-species regulatory network comparisons. Our analysis highlighted species-specific expression variations, with many recently evolved TEs and KRAB-ZNF genes being differentially expressed between species, emphasizing their impact on evolution. Focusing on one-to-one negative correlations between TEs and KRAB-ZNF genes (negative TE:KRAB-ZNF), we found that many of those correlations engage recently evolved TEs and KRAB-ZNF genes and are specific to humans. Integrating findings from the second dataset, we identified 2492 human-specific negative TE:KRAB-ZNF pairs uniquely detectable in the healthy human temporal cortex, suggesting dysregulation in AD brains. A distinct subcluster in the network formed by these 2492 pairs consists of Alu elements, underscoring their unique role in human brain evolution and disease. Our results deepens insights into primate brain evolution and offer a new perspective on human neurodegenerative disease through the analysis of the negative TE:KRAB-ZNF regulatory network.Graphical Abstract

show abstract

“…Since CYP genes also have other functions than detoxification, and they were overrepresented in our results, we suggest that their differential expression might also be associated with developmental pathways in larvae. (115,116). Therefore, further analysis in the biological role of up-regulated CYP genes in D. m. wrigleyi and D. buzzatii might be assessed.…”

Section: Gene Expression In Larvae Is One Of the Factors Shaping The ...mentioning

confidence: 99%

Transposable elements as evolutionary driving force to host shift in cactophilicDrosophilaspecies

Oliveira,

Larue,

Nunes

et al. 2024

Preprint

View full text Add to dashboard Cite

BackgroundThe host shift in insects has been considered a key process with potential to collaborate with ecological speciation. Both genomics and transcriptomics variation has been attributed to such process, in which gene families with functions for host location, acceptance and usage have been proposed to evolve. In this context, cactophilicDrosophilaspecies are an excellent model to study host shift effects, since they use a wide-range of cacti as hosts, and many species have cacti-hosts preference. Despite the potential adaptive role of TEs by generating genetic variability between species and populations, the extent of TEs′ contribution to host shift remains unexplored.ResultsHere, we performed genomics and transcriptomics analyses in seven genomes of cactophilic species/subspecies to investigate how TEs interact with genes likely to be associated with host shift. Our results revealed transposition bursts between species, and an enrichment of TEs at promoter regions of host shift-related genes. Pairwise differential expression analysis between species with different preferential hosts in larvae and head tissues demonstrated divergence on gene expression associated with host location in head, whereas for the larvae we found higher differential expression of genes related to usage/detoxification. Although TEs′ presence does not affect overall gene expression, we observed 2.1% of genes generating gene-TE chimeric transcripts, including those with function affecting host preference. In addition, Helitrons were often observed interacting with genes as a cis-regulatory element.ConclusionsOur combined genomics and transcriptomics approaches provide new insights regarding the evolutionary role of TEs on the context of ecological speciation.

show abstract

Transposons contribute to the functional diversification of the head, gut, and ovary transcriptomes acrossDrosophilanatural strains

Cited by 6 publications

References 89 publications

The mechanistic basis of genetic assimilation in natural fly populations

The mechanistic basis of genetic assimilation in natural fly populations

Regulatory networks of KRAB zinc finger genes and transposable elements changed during human brain evolution and disease

Transposable elements as evolutionary driving force to host shift in cactophilicDrosophilaspecies

Contact Info

Product

Resources

About