Unique trajectory of gene family evolution from genomic analysis of nearly all known species in an ancient yeast lineage
Gene gains and losses are a major driver of genome evolution; their precise characterization can provide insights into the origin and diversification of major lineages. Here, we examined gene family evolution of 1154 genomes from nearly all known species in the medically and technologically important yeast subphylum Saccharomycotina. We found that yeast gene family evolution differs from that of plants, animals, and filamentous ascomycetes, and is characterized by smaller overall gene numbers yet larger gene family sizes for a given gene number. Faster-evolving lineages (FELs) in yeasts experienced significantly higher rates of gene losses-commensurate with a narrowing of metabolic niche breadth-but higher speciation rates than their slower-evolving sister lineages (SELs). Gene families most often lost are those involved in mRNA splicing, carbohydrate metabolism, and cell division and are likely associated with intron loss, metabolic breadth, and non-canonical cell cycle processes. Our results highlight the significant role of gene family contractions in the evolution of yeast metabolism, genome function, and speciation, and suggest that gene family evolutionary trajectories have differed markedly across major eukaryotic lineages.
Authors
- Marizeth Groenewald (ORCID: https://orcid.org/0000-0003-0835-5925)
- Kyle T. David (ORCID: https://orcid.org/0000-0001-9907-789X)
- Carla Gonçalves (ORCID: https://orcid.org/0000-0002-0420-4970)
- Kaitlin J. Fisher (ORCID: https://orcid.org/0000-0002-7536-0508)
- Dana A. Opulente (ORCID: https://orcid.org/0000-0003-3224-7510)
- John F. Wolters (ORCID: https://orcid.org/0000-0002-5477-4250)
- Hongyue Liu (ORCID: https://orcid.org/0000-0002-4058-4990)
- Biyang Xu
- Marie‐Claire Harrison (ORCID: https://orcid.org/0000-0002-3013-9906)
- Antonis Rokas (ORCID: https://orcid.org/0000-0002-7248-6551)
- Shengyuan Shao
- Chris Todd Hittinger (ORCID: https://orcid.org/0000-0001-5088-7461)
- Jacob L. Steenwyk (ORCID: https://orcid.org/0000-0002-8436-595X)
- Shengying Li (ORCID: https://orcid.org/0000-0002-5244-870X)
- Abigail L. LaBella (ORCID: https://orcid.org/0000-0003-0068-6703)
- Xing‐Xing Shen (ORCID: https://orcid.org/0000-0001-5765-1419)
- Xiaofan Zhou (ORCID: https://orcid.org/0000-0002-2879-6317)
- Bo Feng
- Xiaolin Tian (ORCID: https://orcid.org/0009-0008-9529-3227)
- Zhaohao Chen
- Yonglin Li
Institutions
- South China Agricultural University (CN)
- University of North Carolina at Charlotte (US)
- Qingdao University (CN)
- Howard Hughes Medical Institute (US)
- Shandong University (CN)
- Vanderbilt University (US)
- Great Lakes Bioenergy Research Center (US)
- Key Laboratory of Guangdong Province (CN)
- Westerdijk Fungal Biodiversity Institute (NL)
- Qingdao National Laboratory for Marine Science and Technology (CN)
- State University of New York at Oswego (US)
- State Key Laboratory of Microbial Technology
- Zhejiang University (CN)
- Villanova University (US)
- Shandong University of Science and Technology (CN)
- Universidade Nova de Lisboa (PT)
- University of California, Berkeley (US)
Publication Details
- Journal
- Molecular Systems Biology
- Published
- 2025-05-27
- DOI
- https://doi.org/10.1038/s44320-025-00118-0
- Citations
- 6
- Primary Topic
- Fungal and yeast genetics research
- Type
- article
- Field-Weighted Citation Impact
- 4.84
Funders
- National Science Foundation
- Burroughs Wellcome Fund
- Life Sciences Research Foundation
- National Natural Science Foundation of China
- National Institute of Food and Agriculture
- National Key Research and Development Program of China
- Basic and Applied Basic Research Foundation of Guangdong Province
- National Institute of Allergy and Infectious Diseases