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Dosage sensitivity and the evolution of gene families in yeast

Author

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  • Balázs Papp

    (University of Bath
    Department of Plant Taxonomy and Ecology, Eötvös Loránd University)

  • Csaba Pál

    (University of Bath
    Department of Plant Taxonomy and Ecology, Eötvös Loránd University)

  • Laurence D. Hurst

    (University of Bath)

Abstract

According to what we term the balance hypothesis, an imbalance in the concentration of the subcomponents of a protein–protein complex can be deleterious1. If so, there are two consequences: first, both underexpression and overexpression of protein complex subunits should lower fitness, and second, the accuracy of transcriptional co-regulation of subunits should reflect the deleterious consequences of imbalance. Here we show that all these predictions are upheld in yeast (Saccharomyces cerevisiae). This supports the hypothesis2,3 that dominance is a by-product of physiology and metabolism rather than the result of selection to mask the deleterious effects of mutations. Beyond this, single-gene duplication of protein subunits is expected to be harmful, as this, too, leads to imbalance. As then expected, we find that members of large gene families are rarely involved in complexes. The balance hypothesis therefore provides a single theoretical framework for understanding components both of dominance and of gene family size.

Suggested Citation

  • Balázs Papp & Csaba Pál & Laurence D. Hurst, 2003. "Dosage sensitivity and the evolution of gene families in yeast," Nature, Nature, vol. 424(6945), pages 194-197, July.
    • Handle: RePEc:nat:nature:v:424:y:2003:i:6945:d:10.1038_nature01771
    DOI: 10.1038/nature01771
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    Cited by:

    1. Xiaowen Shi & Hua Yang & Chen Chen & Jie Hou & Tieming Ji & Jianlin Cheng & James A. Birchler, 2022. "Dosage-sensitive miRNAs trigger modulation of gene expression during genomic imbalance in maize," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Fridtjof Brauns & Leila Iñigo de la Cruz & Werner K.-G. Daalman & Ilse Bruin & Jacob Halatek & Liedewij Laan & Erwin Frey, 2023. "Redundancy and the role of protein copy numbers in the cell polarization machinery of budding yeast," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Thuy N. Nguyen & Christine Ingle & Samuel Thompson & Kimberly A. Reynolds, 2024. "The genetic landscape of a metabolic interaction," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Shinsuke Ohnuki & Yoshikazu Ohya, 2018. "High-dimensional single-cell phenotyping reveals extensive haploinsufficiency," PLOS Biology, Public Library of Science, vol. 16(5), pages 1-23, May.

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