Evolutionary capacitance as a general feature of complex gene networks

Aviv Bergman, Mark Siegal

Research output: Contribution to journalArticle

Abstract

An evolutionary capacitor buffers genotypic variation under normal conditions, thereby promoting the accumulation of hidden polymorphism. But it occasionally fails, thereby revealing this variation phenotypically. The principal example of an evolutionary capacitor is Hsp90, a molecular chaperone that targets an important set of signal transduction proteins. Experiments in Drosophila and Arabidopsis have demonstrated three key properties of Hsp90: (1) it suppresses phenotypic variation under normal conditions and releases this variation when functionally compromised; (2) its function is overwhelmed by environmental stress; and (3) it exerts pleiotropic effects on key developmental processes. But whether these properties necessarily make Hsp90 a significant and unique facilitator of adaptation is unclear. Here we use numerical simulations of complex gene networks, as well as genome-scale expression data from yeast single-gene deletion strains, to present a mechanism that extends the scope of evolutionary capacitance beyond the action of Hsp90 alone. We illustrate that most, and perhaps all, genes reveal phenotypic variation when functionally compromised, and that the availability of loss-of-function mutations accelerates adaptation to a new optimum phenotype. However, this effect does not require the mutations to be conditional on the environment. Thus, there might exist a large class of evolutionary capacitors whose effects on phenotypic variation complement the systemic, environment-induced effects of Hsp90.

Original languageEnglish (US)
Pages (from-to)549-552
Number of pages4
JournalNature
Volume424
Issue number6948
DOIs
StatePublished - Jul 31 2003

Fingerprint

Gene Regulatory Networks
Mutation
Molecular Chaperones
Gene Deletion
Arabidopsis
Drosophila
Signal Transduction
Buffers
Yeasts
Genome
Phenotype
Genes
Proteins

ASJC Scopus subject areas

  • General

Cite this

Evolutionary capacitance as a general feature of complex gene networks. / Bergman, Aviv; Siegal, Mark.

In: Nature, Vol. 424, No. 6948, 31.07.2003, p. 549-552.

Research output: Contribution to journalArticle

Bergman, Aviv ; Siegal, Mark. / Evolutionary capacitance as a general feature of complex gene networks. In: Nature. 2003 ; Vol. 424, No. 6948. pp. 549-552.
@article{c645b38b82514810b706db26eaac915f,
title = "Evolutionary capacitance as a general feature of complex gene networks",
abstract = "An evolutionary capacitor buffers genotypic variation under normal conditions, thereby promoting the accumulation of hidden polymorphism. But it occasionally fails, thereby revealing this variation phenotypically. The principal example of an evolutionary capacitor is Hsp90, a molecular chaperone that targets an important set of signal transduction proteins. Experiments in Drosophila and Arabidopsis have demonstrated three key properties of Hsp90: (1) it suppresses phenotypic variation under normal conditions and releases this variation when functionally compromised; (2) its function is overwhelmed by environmental stress; and (3) it exerts pleiotropic effects on key developmental processes. But whether these properties necessarily make Hsp90 a significant and unique facilitator of adaptation is unclear. Here we use numerical simulations of complex gene networks, as well as genome-scale expression data from yeast single-gene deletion strains, to present a mechanism that extends the scope of evolutionary capacitance beyond the action of Hsp90 alone. We illustrate that most, and perhaps all, genes reveal phenotypic variation when functionally compromised, and that the availability of loss-of-function mutations accelerates adaptation to a new optimum phenotype. However, this effect does not require the mutations to be conditional on the environment. Thus, there might exist a large class of evolutionary capacitors whose effects on phenotypic variation complement the systemic, environment-induced effects of Hsp90.",
author = "Aviv Bergman and Mark Siegal",
year = "2003",
month = "7",
day = "31",
doi = "10.1038/nature01765",
language = "English (US)",
volume = "424",
pages = "549--552",
journal = "Nature Cell Biology",
issn = "1465-7392",
publisher = "Nature Publishing Group",
number = "6948",

}

TY - JOUR

T1 - Evolutionary capacitance as a general feature of complex gene networks

AU - Bergman, Aviv

AU - Siegal, Mark

PY - 2003/7/31

Y1 - 2003/7/31

N2 - An evolutionary capacitor buffers genotypic variation under normal conditions, thereby promoting the accumulation of hidden polymorphism. But it occasionally fails, thereby revealing this variation phenotypically. The principal example of an evolutionary capacitor is Hsp90, a molecular chaperone that targets an important set of signal transduction proteins. Experiments in Drosophila and Arabidopsis have demonstrated three key properties of Hsp90: (1) it suppresses phenotypic variation under normal conditions and releases this variation when functionally compromised; (2) its function is overwhelmed by environmental stress; and (3) it exerts pleiotropic effects on key developmental processes. But whether these properties necessarily make Hsp90 a significant and unique facilitator of adaptation is unclear. Here we use numerical simulations of complex gene networks, as well as genome-scale expression data from yeast single-gene deletion strains, to present a mechanism that extends the scope of evolutionary capacitance beyond the action of Hsp90 alone. We illustrate that most, and perhaps all, genes reveal phenotypic variation when functionally compromised, and that the availability of loss-of-function mutations accelerates adaptation to a new optimum phenotype. However, this effect does not require the mutations to be conditional on the environment. Thus, there might exist a large class of evolutionary capacitors whose effects on phenotypic variation complement the systemic, environment-induced effects of Hsp90.

AB - An evolutionary capacitor buffers genotypic variation under normal conditions, thereby promoting the accumulation of hidden polymorphism. But it occasionally fails, thereby revealing this variation phenotypically. The principal example of an evolutionary capacitor is Hsp90, a molecular chaperone that targets an important set of signal transduction proteins. Experiments in Drosophila and Arabidopsis have demonstrated three key properties of Hsp90: (1) it suppresses phenotypic variation under normal conditions and releases this variation when functionally compromised; (2) its function is overwhelmed by environmental stress; and (3) it exerts pleiotropic effects on key developmental processes. But whether these properties necessarily make Hsp90 a significant and unique facilitator of adaptation is unclear. Here we use numerical simulations of complex gene networks, as well as genome-scale expression data from yeast single-gene deletion strains, to present a mechanism that extends the scope of evolutionary capacitance beyond the action of Hsp90 alone. We illustrate that most, and perhaps all, genes reveal phenotypic variation when functionally compromised, and that the availability of loss-of-function mutations accelerates adaptation to a new optimum phenotype. However, this effect does not require the mutations to be conditional on the environment. Thus, there might exist a large class of evolutionary capacitors whose effects on phenotypic variation complement the systemic, environment-induced effects of Hsp90.

UR - http://www.scopus.com/inward/record.url?scp=0042154192&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0042154192&partnerID=8YFLogxK

U2 - 10.1038/nature01765

DO - 10.1038/nature01765

M3 - Article

VL - 424

SP - 549

EP - 552

JO - Nature Cell Biology

JF - Nature Cell Biology

SN - 1465-7392

IS - 6948

ER -