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Hsp90 as a capacitor for morphological evolution
Abstract
The heat-shock protein Hsp90 supports diverse but specific signal transducers and lies at the interface of several developmental pathways. We report here that when Drosophila Hsp90 is mutant or pharmacologically impaired, phenotypic variation affecting nearly any adult structure is produced, with specific variants depending on the genetic background and occurring both in laboratory strains and in wild populations. Multiple, previously silent, genetic determinants produced these variants and, when enriched by selection, they rapidly became independent of the Hsp90 mutation. Therefore, widespread variation affecting morphogenic pathways exists in nature, but is usually silent; Hsp90 buffers this variation, allowing it to accumulate under neutral conditions. When Hsp90 buffering is compromised, for example by temperature, cryptic variants are expressed and selection can lead to the continued expression of these traits, even when Hsp90 function is restored. This provides a plausible mechanism for promoting evolutionary change in otherwise entrenched developmental processes.
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“Hence Hsp90 has acted as an evolutionary capacitor during eukaryotic evolution19-21.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [19]
In the citing paper
“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 [19]
In the citing paper
“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 [19]
Citations
Cites
Introduction to Quantitative Genetics.
Edwards, A. W. F., & Falconer, D. S. (1982) · Biometrics · doi:10.2307/2529912 · Cited by 21,447
The Neutral Theory of Molecular Evolution
Kimura, M. (1979) · Scientific American · doi:10.1038/scientificamerican1179-98 · Cited by 7,687
The origins of order; self organization and selection in evolution
Kauffman, S. A. (1994) · International Journal of Biochemistry · doi:10.1016/0020-711x(94)90119-8 · Cited by 6,753
The Neutral Theory of Molecular Evolution
Kimura, M. (1983) · Cambridge University Press eBooks · doi:10.1017/cbo9780511623486 · Cited by 6,300
CANALIZATION OF DEVELOPMENT AND THE INHERITANCE OF ACQUIRED CHARACTERS
WADDINGTON, C. H. (1942) · Nature · doi:10.1038/150563a0 · Cited by 3,255
The Genome of Drosophila Melanogaster
Lindsley, D. L., & Zimm, G. G. (1992) · Cited by 3,098
GENETIC ASSIMILATION OF AN ACQUIRED CHARACTER
Waddington, C. H. (1953) · Evolution · doi:10.1111/j.1558-5646.1953.tb00070.x · Cited by 1,494
Whitesell, L., Mimnaugh, E. G., De Costa, B., Myers, C. E., & Neckers, L. M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.18.8324 · Cited by 1,444
Raff, R. A. (1996) · University of Chicago Press eBooks · doi:10.7208/chicago/9780226256573.001.0001 · Cited by 1,262
Zou, J., Guo, Y., Guettouche, T., Smith, D. F., & Voellmy, R. W. (1998) · Cell · doi:10.1016/s0092-8674(00)81588-3 · Cited by 1,232
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- Xu, Y., Singer, M. & Lindquist, S. Maturation of c-src as a kinase and as a substrate is dependent on Hsp90. Proc. Natl Acad. Sci. USA (in the press).
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Hummel, B., Hansen, E. C., Yoveva, A., Aprile-Garcia, F., Hussong, R., & Sawarkar, R. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3368 · Cited by 72
Canalization, Cryptic Variation, and Developmental Buffering
Dworkin, I. M. (2005) · Elsevier eBooks · doi:10.1016/b978-012088777-4/50010-7 · Cited by 72
Gutiérrez, J. P., Nieto, B., Piqueras, P., Ibáñez‐Escriche, N., & Salgado, C. (2006) · Genetics Selection Evolution · doi:10.1051/gse:2006014 · Cited by 72
Characterization of a Plant Homolog of Hop, a Cochaperone of Hsp90
Zhang, Z., Quick, M. K., Kanelakis, K. C., Gijzen, M., & Krishna, P. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.011940 · Cited by 72
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Minelli, A., & Fusco, G. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0268 · Cited by 71
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Qin, H., & Panek, J. S. (2008) · Organic Letters · doi:10.1021/ol800749w · Cited by 71
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Hochbaum, D., Zhang, Y., Stuckenholz, C., Labhart, P., Alexiadis, V., Martin, R., Knölker, H., & Fisher, A. L. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002179 · Cited by 74
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Shrestha, L., Patel, H. J., & Chiosis, G. (2016) · Cell chemical biology · doi:10.1016/j.chembiol.2015.12.006 · Cited by 71
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Simpson, P. (2002) · Nature Reviews Genetics · doi:10.1038/nrg947 · Cited by 72
Willmund, F., & Schroda, M. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.063578 · Cited by 71
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Cross signaling, cell specificity, and physiology
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Bagdány, M., Veit, G., Fukuda, R., Avramescu, R. G., Okiyoneda, T., Baaklini, I., Singh, J., Sovak, G., Xu, H., Apaja, P. M., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00444-4 · Cited by 71
Geller, R., Pechmann, S., Acevedo, A., Andino, R., & Frydman, J. (2018) · Nature Communications · doi:10.1038/s41467-018-04203-x · Cited by 74
Stefánsson, T. S., McDonald, B. A., & Willi, Y. (2013) · Evolutionary Applications · doi:10.1111/eva.12039 · Cited by 69
Sonnenschein, C., Soto, A. M., Rangarajan, A., & Kulkarni, P. (2014) · Journal of Biosciences · doi:10.1007/s12038-013-9403-y · Cited by 72
Ricketson, D., Hostick, U., Fang, L., Yamamoto, K. R., & Darimont, B. D. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.02.057 · Cited by 69
Guerrero‐Bosagna, C., Sabat, P., & Valladares, L. (2005) · Evolution & Development · doi:10.1111/j.1525-142x.2005.05033.x · Cited by 70
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Schawaroch, V. (2002) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2002.tb01711.x · Cited by 69
Li, W., Meng, R., Liu, Y., Chen, S., Jiang, J., Wang, L., Zhao, S., Wang, Z., Fang, W., Chen, F., et al. (2022) · Horticulture Research · doi:10.1093/hr/uhac073 · Cited by 68
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Proteome analysis of nuclear matrix proteins during apoptotic chromatin condensation
Gerner, C., Gotzmann, J., Fröhwein, U., Schamberger, C. J., Ellinger, A., & Sauermann, G. (2002) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401010 · Cited by 68
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Wang, K., Zhang, X., Goatley, M., & Ervin, E. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102914 · Cited by 67
Canella, A., Welker, A. M., Yoo, J. Y., Xu, J., Abas, F. S., Kesanakurti, D., Nagarajan, P., Beattie, C. E., Sulman, E. P., Liu, J., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-3151 · Cited by 66
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Will, T., Schmidtberg, H., Škaljac, M., & Vilcinskas, A. (2016) · Development Genes and Evolution · doi:10.1007/s00427-016-0564-1 · Cited by 63
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Jaeger, A. M., Stopfer, L. E., Lee, S., Gaglia, G., Sandel, D. A., Santagata, S., Lin, N., Trepel, J. B., White, F. M., Jacks, T., et al. (2019) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-0596 · Cited by 61
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Shang, L., & Tomasi, T. B. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m509901200 · Cited by 63
Fluctuating asymmetry-indicator of what?
Rasmuson, M. (2002) · Hereditas · doi:10.1034/j.1601-5223.2002.1360301.x · Cited by 61
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Calabrese, V., Scapagnini, G., Ravagna, A., Stella, A. M. G., & Butterfield, D. A. (2002) · Developmental Neuroscience · doi:10.1159/000064941 · Cited by 61
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Aviner, R., & Frydman, J. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a034090 · Cited by 61
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Berger, D., Bauerfeind, S. S., Blanckenhorn, W. U., & Schäfer, M. A. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01392.x · Cited by 60
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Fares, M. A. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.04.008 · Cited by 64
Kukuczka, B., Magneschi, L., Petroutsos, D., Steinbeck, J., Bald, T., Powikrowska, M., Fufezan, C., Finazzi, G., & Hippler, M. (2014) · PLANT PHYSIOLOGY · doi:10.1104/pp.114.240648 · Cited by 60
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Ikegami, K., de March, C. A., Nagai, M. H., Ghosh, S., Do, M., Sharma, R., Bruguera, E. S., Lu, Y., Fukutani, Y., Vaidehi, N., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1915520117 · Cited by 60
Genotype by environment interaction for gene expression in Drosophila melanogaster
Huang, W., Carbone, M. A., Lyman, R. F., Anholt, R. R. H., & Mackay, T. F. C. (2020) · Nature Communications · doi:10.1038/s41467-020-19131-y · Cited by 63
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Walser, J., Chen, B., & Feder, M. E. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0020165 · Cited by 60
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Ofria, C., Adami, C., & Collier, T. C. (2003) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(03)00062-6 · Cited by 60
Rank, N. E., Bruce, D. A., McMillan, D. M., Barclay, C., & Dahlhoff, E. P. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.02695 · Cited by 59
New MicroRNAs in Drosophila—Birth, Death and Cycles of Adaptive Evolution
Lyu, Y., Shen, Y., Li, H., Chen, Y., Guo, L., Zhao, Y., Hungate, E. A., Shi, S., Wu, C., & Tang, T. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004096 · Cited by 59
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Tichá, T., Samakovli, D., Kuchařová, A., Vavrdová, T., & Šamaj, J. (2020) · Journal of Experimental Botany · doi:10.1093/jxb/eraa177 · Cited by 60
Larreta, R., Soto, M., Quijada, L., Folgueira, C., Abánades, D. R., Alonso‐Moreno, C., & Requena, J. M. (2004) · BMC Molecular Biology · doi:10.1186/1471-2199-5-3 · Cited by 59
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Kitamura, Y., & Nomura, Y. (2002) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(02)00301-7 · Cited by 59
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Zhong, W., & Priest, N. K. (2010) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-010-1117-7 · Cited by 58
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Castonguay, E., & Angers, B. (2012) · Genetics Research International · doi:10.1155/2012/534289 · Cited by 58
Dworkin, I. M., Kennerly, E., Tack, D. C., Hutchinson, J., Brown, J., Mahaffey, J. W., & Gibson, G. C. (2008) · Genetics · doi:10.1534/genetics.108.096453 · Cited by 62
The developmental genetics of biological robustness
Mestek, L., & Barkoulas, M. (2015) · Annals of Botany · doi:10.1093/aob/mcv128 · Cited by 61
Roy, A. L., Loughland, I., & Seebacher, F. (2017) · Scientific Reports · doi:10.1038/s41598-017-03300-z · Cited by 58
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Bagheri, H. C., & Wagner, G. P. (2004) · Genetics · doi:10.1534/genetics.104.028696 · Cited by 58
Kirschner, M. W. (1999) · Trends in Cell Biology · doi:10.1016/s0962-8924(99)01666-9 · Cited by 58
Workman, P. (2003) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-003-0593-0 · Cited by 59
Dickinson, W. J., & Seger, J. (1999) · Nature · doi:10.1038/19894 · Cited by 58
Bogan, S. N., & Yi, S. V. (2024) · Genome Biology and Evolution · doi:10.1093/gbe/evae022 · Cited by 60
The Stress of Misfolded Proteins
Brignull, H. R., Morley, J. F., & Morimoto, R. I. (2007) · Springer eBooks · doi:10.1007/978-0-387-39975-1_15 · Cited by 59
Genomic neighbourhood and the regulation of gene expression
De, S., & Babu, M. M. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2010.04.004 · Cited by 59
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Goldfish morphology as a model for evolutionary developmental biology
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Metadata
- Authors
- Rutherford, S. L., & Lindquist, S.
- Affiliations
- Howard Hughes Medical Institute (US)
- Venue
- Nature
- Published
- 1998-11
- Volume
- 396
- Issue
- 6709
- Pages
- 336-342
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1554180547
- Cited by
- 2,270
- References
- 38
- Citations by year
- 2026: 45 · 2025: 57 · 2024: 53 · 2023: 58 · 2022: 60 · 2021: 54 · 2020: 56 · 2019: 86 · 2018: 95 · 2017: 77 · 2016: 84 · 2015: 93 · 2014: 104 · 2013: 108 · 2012: 93
- FWCI
- 18.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- 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 › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Morphological variations and asymmetry
- Keywords
- HSP90, morphological evolution, cryptic genetic variation, Drosophila, developmental pathways, signal transduction, genetic background effects, temperature effects, morphological variation
- MeSH terms
- Animals, Drosophila, Heat-Shock Proteins, Models, Genetic, Mutation, Phenotype, Temperature, Genetic Variation, HSP90 Heat-Shock Proteins, Directed Molecular Evolution, Drosophila Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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