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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).
Cited by
Sorted by citations
Ghalambor, C. K., McKay, J., Carroll, S. P., & Reznick, D. N. (2007) · Functional Ecology · doi:10.1111/j.1365-2435.2007.01283.x · Cited by 3,752
Molecular chaperones in protein folding and proteostasis
Hartl, F. U., Bracher, A., & Hayer-Hartl, M. (2011) · Nature · doi:10.1038/nature10317 · Cited by 3,381
Proliferation, cell cycle and apoptosis in cancer
Evan, G. I., & Vousden, K. H. (2001) · Nature · doi:10.1038/35077213 · Cited by 3,417
Hsp70 chaperones: Cellular functions and molecular mechanism
Mayer, M. P., & Bukau, B. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-004-4464-6 · Cited by 2,857
Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response
Wang, W., Vinocur, B. J., Shoseyov, O., & Altman, A. (2004) · Trends in Plant Science · doi:10.1016/j.tplants.2004.03.006 · Cited by 2,759
HSP90 and the chaperoning of cancer
Whitesell, L., & Lindquist, S. L. (2005) · Nature Reviews Cancer · doi:10.1038/nrc1716 · Cited by 2,502
Self-citationKitano, H. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1471 · Cited by 2,278
EGF–ERBB signalling: towards the systems level
Citri, A., & Yarden, Y. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1962 · Cited by 2,056
The epigenetic progenitor origin of human cancer
Feinberg, A. P., OHLSSON, R. I., & Henikoff, S. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1748 · Cited by 1,885
HSP90 at the hub of protein homeostasis: emerging mechanistic insights
Taipale, M., Jarosz, D. F., & Lindquist, S. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2918 · Cited by 1,818
Self-citationStefani, M., & Dobson, C. M. (2003) · Journal of Molecular Medicine · doi:10.1007/s00109-003-0464-5 · Cited by 1,670
Phenotypic plasticity and the epigenetics of human disease
Feinberg, A. P. (2007) · Nature · doi:10.1038/nature05919 · Cited by 1,613
Roles for MicroRNAs in Conferring Robustness to Biological Processes
Ebert, M. S., & Sharp, P. A. (2012) · Cell · doi:10.1016/j.cell.2012.04.005 · Cited by 1,564
Schopf, F. H., Biebl, M. M., & Buchner, J. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.20 · Cited by 1,540
Foundations for engineering biology
Endy, D. (2005) · Nature · doi:10.1038/nature04342 · Cited by 1,511
Engineering stability in gene networks by autoregulation
Becskei, A., & Serrano, L. G. (2000) · Nature · doi:10.1038/35014651 · Cited by 1,493
The evolutionary and ecological role of heat shock proteins
Sørensen, J. G., Kristensen, T. N., & Loeschcke, V. (2003) · Ecology Letters · doi:10.1046/j.1461-0248.2003.00528.x · Cited by 1,398
A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors
Kamal, A., Thao, L., Sensintaffar, J., Zhang, L., Boehm, M. F., Fritz, L. C., & Burrows, F. J. (2003) · Nature · doi:10.1038/nature01913 · Cited by 1,380
Hsp90 as a capacitor of phenotypic variation
Queitsch, C., Sangster, T. A., & Lindquist, S. (2002) · Nature · doi:10.1038/nature749 · Cited by 1,372
Self-citationThe Concept of Synthetic Lethality in the Context of Anticancer Therapy
Kaelin, W. G. (2005) · Nature reviews. Cancer · doi:10.1038/nrc1691 · Cited by 1,405
Remodeling of Yeast Genome Expression in Response to Environmental Changes
Causton, H. C., Ren, B., Koh, S. S., Harbison, C. T., Kanin, E. I., Jennings, E. G., Lee, T. I., True, H. L., Lander, E. S., & Young, R. A. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.2.323 · Cited by 1,382
Converging concepts of protein folding in vitro and in vivo
Hartl, F. U., & Hayer-Hartl, M. K. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1591 · Cited by 1,235
Folding of Newly Translated Proteins In Vivo: The Role of Molecular Chaperones
Frydman, J. (2001) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.70.1.603 · Cited by 1,184
The Genetic Architecture of Quantitative Traits
Mackay, T. F. C. (2001) · Annual Review of Genetics · doi:10.1146/annurev.genet.35.102401.090633 · Cited by 1,106
Pathways of chaperone-mediated protein folding in the cytosol
Young, J. C., Agashe, V. R., Siegers, K., & Hartl, F. U. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1492 · Cited by 1,121
Roles of heat-shock proteins in innate and adaptive immunity.
Srivastava, P. (2002) · Nature reviews. Immunology · doi:10.1038/nri749 · Cited by 1,069
Language as shaped by the brain
Christiansen, M. H., & Chater, N. (2008) · Behavioral and Brain Sciences · doi:10.1017/s0140525x08004998 · Cited by 1,102
Lande, R. (2009) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2009.01754.x · Cited by 1,101
Evolution, the Extended Synthesis
Pigliucci, M., & Müller, G. (2010) · The MIT Press eBooks · doi:10.7551/mitpress/9780262513678.001.0001 · Cited by 976
Heat shock proteins in cancer: chaperones of tumorigenesis
Calderwood, S. K., Khaleque, A., Sawyer, D. B., & Ciocca, D. R. (2006) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2006.01.006 · Cited by 972
Quantitative Analysis of Hsp90-Client Interactions Reveals Principles of Substrate Recognition
Taipale, M., Krykbaeva, I., Koeva, M., Kayatekin, C., Westover, K. D., Karras, G. I., & Lindquist, S. (2012) · Cell · doi:10.1016/j.cell.2012.06.047 · Cited by 879
Self-citationProteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging
Morimoto, R. I. (2008) · Genes & Development · doi:10.1101/gad.1657108 · Cited by 872
Organization of cell assemblies in the hippocampus
Harris, K. D., Csicsvari, J., Hirase, H., Dragoi, G., & Buzsáki, G. (2003) · Nature · doi:10.1038/nature01834 · Cited by 901
Morphological integration and developmental modularity
Klingenberg, C. P. (2008) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.37.091305.110054 · Cited by 863
Srivastava, P. K. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.100301.064801 · Cited by 846
Young, J. C., Moarefi, I., & Hartl, F. U. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200104079 · Cited by 838
Epistasis and quantitative traits: using model organisms to study gene–gene interactions
Mackay, T. F. C. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3627 · Cited by 854
Principles for the buffering of genetic variation
Hartman, J. L., Garvik, B., & Hartwell, L. (2001) · Science · doi:10.1126/science.1056072 · Cited by 808
The frailty of adaptive hypotheses for the origins of organismal complexity
Lynch, M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702207104 · Cited by 829
Heat-shock protein 90, a chaperone for folding and regulation
Picard, D. (2002) · Cellular and Molecular Life Sciences · doi:10.1007/pl00012491 · Cited by 812
GHKL, an emergent ATPase/kinase superfamily
DUTTA, R., & Inouye, M. (2000) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01503-0 · Cited by 767
Hsp90 Potentiates the Rapid Evolution of New Traits: Drug Resistance in Diverse Fungi
Cowen, L. E., & Lindquist, S. (2005) · Science · doi:10.1126/science.1118370 · Cited by 698
Self-citationPERSPECTIVE: EVOLUTION AND DETECTION OF GENETIC ROBUSTNESS
de Visser, J. A. G. M., Hermisson, J., Wagner, G. P., Ancel, L. W., Bagheri, H. C., Blanchard, J. L., Chao, L., Cheverud, J. M., Elena, S. F., Fontana, W., et al. (2003) · Evolution · doi:10.1111/j.0014-3820.2003.tb00377.x · Cited by 707
Upper thermal limits in terrestrial ectotherms: how constrained are they?
Hoffmann, A. A., Chown, S. L., & Clusella‐Trullas, S. (2012) · Functional Ecology · doi:10.1111/j.1365-2435.2012.02036.x · Cited by 701
Hsp90 inhibitors as novel cancer chemotherapeutic agents
Neckers, L. (2002) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(02)02316-x · Cited by 677
A yeast prion provides a mechanism for genetic variation and phenotypic diversity
True, H. L., & Lindquist, S. L. (2000) · Nature · doi:10.1038/35035005 · Cited by 672
Self-citationRobustness and evolvability: a paradox resolved
Wagner, A. (2008) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2007.1137 · Cited by 669
Chaperoning signaling pathways: molecular chaperones as stress-sensing`heat shock' proteins
Nollen, E. A. A., & Morimoto, R. I. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.14.2809 · Cited by 644
Progressive disruption of cellular protein folding in models of polyglutamine diseases
Gidalevitz, T., Ben-Zvi, A., Ho, K. H., Brignull, H. R., & Morimoto, R. I. (2006) · Science · doi:10.1126/science.1124514 · Cited by 643
Variability in gene expression underlies incomplete penetrance
Raj, A., Rifkin, S. A., Andersen, E. C., & van Oudenaarden, A. (2010) · Nature · doi:10.1038/nature08781 · Cited by 642
Waddington's canalization revisited: Developmental stability and evolution
Siegal, M. L., & Bergman, A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.102303999 · Cited by 661
Adaptive Radiation, Ecological Opportunity, and Evolutionary Determinism
Losos, J. B. (2010) · The American Naturalist · doi:10.1086/652433 · Cited by 651
Discovering susceptibility genes for asthma and allergy
Vercelli, D. (2008) · Nature Reviews Immunology · doi:10.1038/nri2257 · Cited by 635
Hsp90 & Co. – a holding for folding
Büchner, J. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01373-0 · Cited by 625
Lahti, D. C., Johnson, N., Ajie, B. C., Otto, S. P., Hendry, A. P., Blumstein, D. T., Coss, R. G., Donohue, K., & Foster, S. A. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2009.03.010 · Cited by 615
Mapping phenotypes: canalization, plasticity and developmental stability
Debat, V., & David, P. (2001) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(01)02266-2 · Cited by 614
Hsp70 and Hsp90—a relay team for protein folding
Wegele, H., Müller, L., & Büchner, J. (2004) · Springer eBooks · doi:10.1007/s10254-003-0021-1 · Cited by 609
The role of developmental plasticity in evolutionary innovation
Moczek, A. P., Sultan, S. E., Foster, S. A., Ledón‐Rettig, C. C., Dworkin, I. M., Nijhout, H. F., Abouheif, E., & Pfennig, D. W. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.0971 · Cited by 609
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Brehme, M., Voisine, C., Rolland, T., Wachi, S., Soper, J. H., Zhu, Y., Orton, K., Villella, A., Garza, D., Vidal, M., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.09.042 · Cited by 584
Pigliucci, M. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2278 · Cited by 601
Regulatory circuitry governing fungal development, drug resistance, and disease.
Shapiro, R. S., Robbins, N., & Cowen, L. E. (2011) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00045-10 · Cited by 576
Roberts, R. J., Agius, C., Saliba, C., Bossier, P., & Sung, Y. Y. (2010) · Journal of Fish Diseases · doi:10.1111/j.1365-2761.2010.01183.x · Cited by 589
Transgenerational Epigenetic Effects
Youngson, N. A., & Whitelaw, E. (2008) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.9.081307.164445 · Cited by 594
Physiological Diversity in Insects: Ecological and Evolutionary Contexts
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Hsp90: Chaperoning signal transduction
Richter, K., & Büchner, J. (2001) · Journal of Cellular Physiology · doi:10.1002/jcp.1131 · Cited by 579
Canalization of development by microRNAs
Hornstein, E., & Shomron, N. (2006) · Nature Genetics · doi:10.1038/ng1803 · Cited by 578
Lou, X., Chen, G., Yan, L., Ma, J. Z., Zhu, J., Elston, R. C., & Li, M. D. (2007) · The American Journal of Human Genetics · doi:10.1086/518312 · Cited by 564
Dongen, S. V. (2006) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2006.01175.x · Cited by 560
Ecological Opportunity and Adaptive Radiation
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Uncovering cryptic genetic variation
Gibson, G., & Dworkin, I. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1426 · Cited by 546
Explaining intraspecific diversity in plant secondary metabolites in an ecological context
Moore, B. D., Andrew, R. L., Külheim, C., & Foley, W. J. (2013) · New Phytologist · doi:10.1111/nph.12526 · Cited by 536
DO WE NEED AN EXTENDED EVOLUTIONARY SYNTHESIS?
Pigliucci, M. (2007) · Evolution · doi:10.1111/j.1558-5646.2007.00246.x · Cited by 534
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Maloney, A., & Workman, P. (2002) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2.1.3 · Cited by 531
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Microbial Cell Individuality and the Underlying Sources of Heterogeneity
Avery, S. V. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1460 · Cited by 521
Evolutionary capacitance as a general feature of complex gene networks
Bergman, A., & Siegal, M. L. (2003) · Nature · doi:10.1038/nature01765 · Cited by 523
Functions and mechanisms of epigenetic inheritance in animals
Skvortsova, K., Iovino, N., & Bogdanović, O. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0074-2 · Cited by 533
Crispo, E. (2007) · Evolution · doi:10.1111/j.1558-5646.2007.00203.x · Cited by 532
Stationary phase in gram-negative bacteria
Lloréns, J. M. N., Tormo, A., & Martínez‐García, E. (2010) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2010.00213.x · Cited by 508
Heat shock genes — integrating cell survival and death
Arya, R., Mallik, M., & Lakhotia, S. C. (2007) · Journal of Biosciences · doi:10.1007/s12038-007-0059-3 · Cited by 503
Lehner, B., Crombie, C., Tischler, J., Fortunato, A., & Fraser, A. G. (2006) · Nature Genetics · doi:10.1038/ng1844 · Cited by 502
Molecular chaperones and the stress of oncogenesis
Mosser, D. D., & Morimoto, R. I. (2004) · Oncogene · doi:10.1038/sj.onc.1207529 · Cited by 512
Cryptic genetic variation: evolution's hidden substrate
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The Hsp90 chaperone machinery: Conformational dynamics and regulation by co-chaperones
Li, J., Soroka, J., & Buchner, J. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.09.003 · Cited by 498
Stress and transposable elements: co-evolution or useful parasites?
Capy, P., Gasperi, G., Biémont, C., & Bazin, C. (2000) · Heredity · doi:10.1046/j.1365-2540.2000.00751.x · Cited by 497
Locust Phase Polyphenism: An Update
Pener, M. P., & Simpson, S. J. (2009) · Advances in insect physiology · doi:10.1016/s0065-2806(08)36001-9 · Cited by 495
Ecological Developmental Biology: Developmental Biology Meets the Real World
Gilbert, S. F. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0210 · Cited by 468
Timescales of Genetic and Epigenetic Inheritance
Rando, O. J., & Verstrepen, K. J. (2007) · Cell · doi:10.1016/j.cell.2007.01.023 · Cited by 472
The Evolutionary Genetics of Canalization
Flatt, T. (2005) · The Quarterly Review of Biology · doi:10.1086/432265 · Cited by 473
Mutation rate variation in multicellular eukaryotes: causes and consequences
Baer, C. F., Miyamoto, M. M., & Denver, D. R. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2158 · Cited by 475
An integrated epigenetic and genetic approach to common human disease
BJORNSSON, H. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.06.009 · Cited by 448
Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents
Gilbert, S. F., Bosch, T. C. G., & Ledón‐Rettig, C. C. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3982 · Cited by 461
Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation
Badyaev, A. V. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.3045 · Cited by 453
Sloan, J., Grosvenor, S. J., Friedrichs, S., Kirkland, A. I., HUTCHISON, J. L., & Green, M. L. H. (2002) · Angewandte Chemie International Edition · doi:10.1002/1521-3773(20020402)41:7 · Cited by 90
Protein Folding in the Cytoplasm and the Heat Shock ResponsePreprint
Vabulas, R. M., Raychaudhuri, S., Hayer-Hartl, M. K., & Hartl, F. U. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a004390 · Cited by 450
PIWI proteins and PIWI-interacting RNAs in the soma
Ross, R. J., Weiner, M. M., & Lin, H. (2014) · Nature · doi:10.1038/nature12987 · Cited by 436
The Evolution of Genetic Architecture
Hansen, T. F. (2006) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.37.091305.110224 · Cited by 438
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Sreedhar, A. S., & Csermely, P. (2004) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2003.11.004 · Cited by 419
Epigenetics at the Epicenter of Modern Medicine
Feinberg, A. P. (2008) · JAMA · doi:10.1001/jama.299.11.1345 · Cited by 424
Evolution of a Polyphenism by Genetic Accommodation
Suzuki, Y., & Nijhout, H. F. (2006) · Science · doi:10.1126/science.1118888 · Cited by 411
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
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