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 genus Neurospora, members of which lack recent gene duplications. Several Neurospora species are comprehensively characterized organisms apt for studying the evolution of lineage-specific genes (LSGs). Using gene synteny, we documented that 78% of Neurospora LSG 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 LSG mas-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 the N. crassa genome 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.
Bibliographical noteFunding Information:
We appreciate the constructive and insightful comments from Dr. Ursula Oggenfuss and another anonymous reviewer. We also thank the Broad Institute, FungiDB, and JGI for making related fungal genomic data available. All authors have declared that no competing interests exist. This study was supported by funding to JPT from the National Institutes of Health R01 grant AI146584, National Science Foundation grant IOS 1457044 to JPT, and NSF‐BSF‐2018712 to OY. The funders had no role in the study design, data collection and interpretation, or the decision to submit the work for publication. Neurospora
© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.
- chromosomal rearrangement
- de novo origination
- molecular evolution
- orphan gene