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Origins of lineage-specific elements via gene duplication, relocation, and regional rearrangement in Neurospora crassa
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  • Zheng Wang,
  • Yen-Wen Wang,
  • Takao Kasuga,
  • Hayley Hassler,
  • Francesc Lopez-Giraldez,
  • Caihong Dong,
  • Oded Yarden,
  • Jeffrey Townsend
Zheng Wang
Yale University School of Public Health
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Yen-Wen Wang
Yale University School of Public Health
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Takao Kasuga
University of California Davis
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Hayley Hassler
Yale University School of Public Health
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Francesc Lopez-Giraldez
Yale School of Medicine
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Caihong Dong
Institute of Microbiology Chinese Academy of Sciences
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Oded Yarden
Hebrew University of Jerusalem Robert H Smith Faculty of Agriculture Food and Environment
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Jeffrey Townsend
Yale University

Corresponding Author:[email protected]

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The origin of new genes has long been a central interest of evolutionary biologists. However, their novelty evades reconstruction by the classical tools of evolutionary modeling. This evasion of insight from 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, yet harbor clusters of lineage-specific genes (LSGs) adjacent to the telomeres. Several Neurospora species are comprehensively characterized organisms apt for studying the evolution of LSGs. Using gene synteny, we documented that 78% of Neurospora LSGs clusters are located in chromosomal regions 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 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 mas-1 and its neighbors was investigated in detail, suggesting that it arose from an ancient lysophospholipase precursor that is ubiquitous in lineages of the Sordariomycetes; mas-1 plays a role in cell-wall integrity and cellular sensitivity to antifungal toxins. Our discoveries illuminate a “rummage region” in the N. crassa genome that enables formation of new genes and functions to arise via gene duplication and relocation, followed by fast mutation and recombination facilitated by tandem repeats and deconstrained non-coding sequences.
13 Jul 2023Submitted to Molecular Ecology
14 Jul 2023Review(s) Completed, Editorial Evaluation Pending
14 Jul 2023Submission Checks Completed
14 Jul 2023Assigned to Editor
19 Jul 2023Reviewer(s) Assigned
31 Aug 2023Editorial Decision: Revise Minor
19 Sep 20231st Revision Received
21 Sep 2023Submission Checks Completed
21 Sep 2023Assigned to Editor
21 Sep 2023Review(s) Completed, Editorial Evaluation Pending
27 Sep 2023Editorial Decision: Accept