The three-dimensional genome drives the evolution of asymmetric gene duplicates via enhancer capture-divergence
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 on <i>Drosophila melanogaster</i> tissue 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 gene <i>HP6</i>/<i>Umbrea</i> as an example of the ECD process. By assaying genome-wide chromosomal conformations in multiple <i>Drosophila</i> species, we show that <i>HP6/Umbrea</i> was inserted near a preexisting, long-distance three-dimensional genomic interaction. We then use this data to identify a newly found enhancer (<i>FLEE1</i>), buried within the coding region of the highly conserved, essential gene <i>MFS18</i>, that likely neofunctionalized <i>HP6/Umbrea</i>. Last, we demonstrate ancestral transcriptional coregulation of <i>HP6/Umbrea</i>'s future insertion site, illustrating how enhancer capture provides a highly evolvable, one-step solution to Ohno's dilemma.
Authors
- Alexander Guzzetta (ORCID: https://orcid.org/0000-0002-8809-7438)
- J. J. Emerson (ORCID: https://orcid.org/0000-0001-9474-0891)
- Peter Andolfatto (ORCID: https://orcid.org/0000-0003-3393-4574)
- Ittai Eres (ORCID: https://orcid.org/0000-0002-0265-8194)
- UnJin Lee (ORCID: https://orcid.org/0000-0003-2424-650X)
- Jianhai Chen (ORCID: https://orcid.org/0000-0003-0093-2003)
- Manyuan Long (ORCID: https://orcid.org/0000-0002-6755-197X)
- Débora R. Sobreira (ORCID: https://orcid.org/0000-0002-2232-3922)
- Nicolas Svetec (ORCID: https://orcid.org/0000-0001-9617-2752)
- Dylan Sosa (ORCID: https://orcid.org/0000-0003-3162-0643)
- Qi Zhou (ORCID: https://orcid.org/0000-0002-7419-2047)
- Shengqian Xia (ORCID: https://orcid.org/0000-0002-9264-3649)
- Christopher B. Langer (ORCID: https://orcid.org/0000-0002-4119-2606)
- Patrick Reilly (ORCID: https://orcid.org/0000-0003-3468-9769)
- Mujahid Ali (ORCID: https://orcid.org/0000-0003-3583-493X)
- Deanna Arsala (ORCID: https://orcid.org/0000-0001-8950-9572)
- Cong Li (ORCID: https://orcid.org/0009-0008-5255-5215)
- Li Zhang (ORCID: https://orcid.org/0000-0002-0698-0754)
- Li Zhao (ORCID: https://orcid.org/0000-0001-6776-1996)
Institutions
- University of Vienna (AT)
- University of California, Irvine (US)
- Yale University (US)
- University of Chicago (US)
- Chinese Institute for Brain Research (CN)
- Zhejiang University (CN)
- Columbia University (US)
- Rockefeller University (US)
Publication Details
- Journal
- Science Advances
- Published
- 2024-12-18
- DOI
- https://doi.org/10.1126/sciadv.adn6625
- Citations
- 6
- Primary Topic
- Genomics and Chromatin Dynamics
- Type
- article
- Field-Weighted Citation Impact
- 1.40