Cited by 174Heat shock proteins researchEvolution and Genetic DynamicsMorphological variations and asymmetry

HSP90 affects the expression of genetic variation and developmental stability in quantitative traits

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Sangster, Todd A., Salathia, Neeraj, Undurraga, Soledad, Milo, Ron, Schellenberg, Kurt, Lindquist, Susan, Queitsch, Christine·2008·Proceedings of the National Academy of Sciences

Abstract

Modulation of the activity of the molecular chaperone HSP90 has been extensively discussed as a means to alter phenotype in many traits and organisms. Such changes can be due to the exposure of cryptic genetic variation, which in some instances may also be accomplished by mild environmental alteration. Should such polymorphisms be widespread, natural selection may be more effective at producing phenotypic change in suboptimal environments. However, the frequency and identity of buffered polymorphisms in natural populations are unknown. Here, we employ quantitative genetic dissection of an Arabidopsis thaliana developmental response, hypocotyl elongation in the dark, to detail the underpinnings of genetic variation responsive to HSP90 modulation. We demonstrate that HSP90-dependent alleles occur in continuously distributed, environmentally responsive traits and are amenable to quantitative genetic mapping techniques. Furthermore, such alleles are frequent in natural populations and can have significant effects on natural phenotypic variation. We also find that HSP90 modulation has both general and allele-specific effects on developmental stability; that is, developmental stability is a phenotypic trait that can be affected by natural variation. However, effects of revealed variation on trait means outweigh effects of decreased developmental stability, and the HSP90-dependent trait alterations could be acted on by natural selection. Thus, HSP90 may centrally influence canalization, assimilation, and the rapid evolutionary alteration of phenotype through the concealment and exposure of cryptic genetic variation.

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  • Hsp90 can buffer the effects of genetic or epigenetic variation, keeping it silent until released when the chaperone reservoir is compromised in response to stress.

    “First, Hsp90 can buffer the effects of genetic or epigenetic variation, keeping it silent until released when the chaperone reservoir is compromised in response to stress.”
  • Hsp90's role as a capacitor for variation has been observed in diverse eukaryotes including flies, plants, and fungi.

    “This role as a capacitor for variation has been observed in diverse eukaryotes including flies, plants, and fungi18,19,129-134.”

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  1. [3]Waddington CH. Genetic assimilation of the bithorax phenotype. Evolution (Lawrence, Kans) 1956;10:1–13. [Google Scholar]

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Authors
Sangster, T. A., Salathia, N., Undurraga, S., Milo, R., Schellenberg, K., Lindquist, S., & Queitsch, C.
Affiliations
  • Howard Hughes Medical Institute (US)
  • Harvard University (US)
Venue
Proceedings of the National Academy of Sciences
Published
2008-02-26
Volume
105
Issue
8
Pages
2963-2968
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2029741513
Cited by
174
References
41
Citations by year
2026: 2 · 2025: 8 · 2024: 3 · 2023: 7 · 2022: 4 · 2021: 3 · 2020: 4 · 2019: 6 · 2018: 16 · 2017: 9 · 2016: 9 · 2015: 17 · 2014: 7 · 2013: 12 · 2012: 13
FWCI
7.40
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
National Institute of General Medical Sciences (P50GM068763, GM-068763)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
Keywords
HSP90, molecular chaperones, cryptic genetic variation, developmental stability, canalization, assimilation, hypocotyl elongation, Arabidopsis thaliana, natural selection, phenotypic plasticity, allele-specific effects
MeSH terms
Phenotype, Genetic Variation, Arabidopsis, Plant Roots, Hypocotyl, HSP90 Heat-Shock Proteins, Quantitative Trait Loci

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