Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution
Abstract
Morphological alterations have been shown to occur in Drosophila melanogaster when function of Hsp90 (heat shock 90-kDa protein 1alpha, encoded by Hsp83) is compromised during development. Genetic selection maintains the altered phenotypes in subsequent generations. Recent experiments have shown, however, that phenotypic variation still occurs in nearly isogenic recombinant inbred strains of Arabidopsis thaliana. Using a sensitized isogenic D. melanogaster strain, iso-Kr(If-1), we confirm this finding and present evidence supporting an epigenetic mechanism for Hsp90's capacitor function, whereby reduced activity of Hsp90 induces a heritably altered chromatin state. The altered chromatin state is evidenced by ectopic expression of the morphogen wingless in eye imaginal discs and a corresponding abnormal eye phenotype, both of which are epigenetically heritable in subsequent generations, even when function of Hsp90 is restored. Mutations in nine different genes of the trithorax group that encode chromatin-remodeling proteins also induce the abnormal phenotype. These findings suggest that Hsp90 acts as a capacitor for morphological evolution through epigenetic and genetic mechanisms.
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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.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [134]
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.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [134]
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- Authors
- Sollars, V., Lu, X., Xiao, L., Wang, X., Garfinkel, M. D., & Ruden, D. M.
- Affiliations
- Thomas Jefferson University (US)
- University of Alabama at Birmingham (US)
- Columbia University (US)
- Corresponding author
- Ruden, Douglas M.
- Venue
- Nature Genetics
- Published
- 2002-12-16
- Volume
- 33
- Issue
- 1
- Pages
- 70-74
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- OpenAlex
- W2057056702
- Cited by
- 409
- References
- 25
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 9 · 2023: 3 · 2022: 6 · 2021: 7 · 2020: 4 · 2019: 11 · 2018: 13 · 2017: 13 · 2016: 11 · 2015: 18 · 2014: 22 · 2013: 20 · 2012: 28
- FWCI
- 8.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Alcohol Abuse and Alcoholism (R01AA012276)
- National Cancer Institute (R01CA105349)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- HSP90, epigenetic inheritance, morphological evolution, morphological plasticity, chromatin state, trithorax group genes, chromatin remodeling, wingless, eye imaginal disc, eye phenotype, Drosophila melanogaster, Arabidopsis thaliana
- MeSH terms
- Animals, Chromatin, Drosophila melanogaster, Biological Evolution, Eye Abnormalities, Female, Heat-Shock Proteins, Male, Mutation, Phenotype, Proto-Oncogene Proteins, Selection, Genetic, Genetic Variation, Wings, Animal, Gene Expression Regulation, Developmental, HSP90 Heat-Shock Proteins, Drosophila Proteins, Wnt1 Protein
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