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Previous evolutionary models of duplicate gene evolution have overlooked the pivotal role of genome architecture. Here, we show that proximity-based regulatory recruitment by distally duplicated genes is an efficient mechanism for modulating tissue-specific production of preexisting proteins. By leveraging genomic asymmetries, we performed a coexpression analysis onDrosophila melanogastertissue data to show the generality of enhancer capture-divergence (ECD) as a significant evolutionary driver of asymmetric, distally duplicated genes. We use the recently evolved geneHP6/Umbreaas an example of the ECD process. By assaying genome-wide chromosomal conformations in multipleDrosophilaspecies, we show thatHP6/Umbreawas inserted near a preexisting, long-distance three-dimensional genomic interaction. We then use this data to identify a newly found enhancer (FLEE1), buried within the coding region of the highly conserved, essential geneMFS18, that likely neofunctionalizedHP6/Umbrea. Last, we demonstrate ancestral transcriptional coregulation ofHP6/Umbrea’s future insertion site, illustrating how enhancer capture provides a highly evolvable, one-step solution to Ohno’s dilemma.
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Origins of lineage‐specific elements via gene duplication, relocation, and regional rearrangement in Neurospora crassa
Abstract The origin of new genes has long been a central interest of evolutionary biologists. However, their novelty means that they evade reconstruction by the classical tools of evolutionary modelling. This evasion of deep ancestral investigation necessitates intensive study of model species within well‐sampled, recently diversified, clades. One such clade is the model genusNeurospora, members of which lack recent gene duplications. SeveralNeurosporaspecies are comprehensively characterized organisms apt for studying the evolution of lineage‐specific genes (LSGs). Using gene synteny, we documented that 78% ofNeurosporaLSG clusters are located adjacent to the telomeres featuring extensive tracts of non‐coding DNA and duplicated genes. Here, we report several instances of LSGs that are likely from regional rearrangements and potentially from gene rebirth. To broadly investigate the functions of LSGs, we assembled transcriptomics data from 68 experimental data points and identified co‐regulatory modules using Weighted Gene Correlation Network Analysis, revealing that LSGs are widely but peripherally involved in known regulatory machinery for diverse functions. The ancestral status of the LSGmas‐1, a gene with roles in cell‐wall integrity and cellular sensitivity to antifungal toxins, was investigated in detail alongside its genomic neighbours, indicating that it arose from an ancient lysophospholipase precursor that is ubiquitous in lineages of the Sordariomycetes. Our discoveries illuminate a “rummage region” in theN. crassagenome that enables the formation of new genes and functions to arise via gene duplication and relocation, followed by fast mutation and recombination facilitated by sequence repeats and unconstrained non‐coding sequences.
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- PAR ID:
- 10559425
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 33
- Issue:
- 24
- ISSN:
- 0962-1083
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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