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Hsp90 as a capacitor for morphological evolution

Author

Listed:
  • Suzanne L. Rutherford

    (Howard Hughes Medical Institute, University of Chicago
    University of California at Irvine)

  • Susan Lindquist

    (Howard Hughes Medical Institute, University of Chicago)

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.

Suggested Citation

  • Suzanne L. Rutherford & Susan Lindquist, 1998. "Hsp90 as a capacitor for morphological evolution," Nature, Nature, vol. 396(6709), pages 336-342, November.
    • Handle: RePEc:nat:nature:v:396:y:1998:i:6709:d:10.1038_24550
    DOI: 10.1038/24550
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    Cited by:

    1. D. Blanco-Obregon & K. El Marzkioui & F. Brutscher & V. Kapoor & L. Valzania & D. S. Andersen & J. Colombani & S. Narasimha & D. McCusker & P. Léopold & L. Boulan, 2022. "A Dilp8-dependent time window ensures tissue size adjustment in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Sergey Vakulenko & Dmitry Grigoriev, 2021. "Deep Gene Networks and Response to Stress," Mathematics, MDPI, vol. 9(23), pages 1-19, November.
    3. Minhao Li & Dawn S. Chen & Ian P. Junker & Fabianna I. Szorenyi & Guan Hao Chen & Arnold J. Berger & Aaron A. Comeault & Daniel R. Matute & Yun Ding, 2024. "Ancestral neural circuits potentiate the origin of a female sexual behavior in Drosophila," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Zeina Shreif & Vipul Periwal, 2014. "A Network Characteristic That Correlates Environmental and Genetic Robustness," PLOS Computational Biology, Public Library of Science, vol. 10(2), pages 1-23, February.
    5. Joseph J. Hale & Takeshi Matsui & Ilan Goldstein & Martin N. Mullis & Kevin R. Roy & Christopher Ne Ville & Darach Miller & Charley Wang & Trevor Reynolds & Lars M. Steinmetz & Sasha F. Levy & Ian M. , 2024. "Genome-scale analysis of interactions between genetic perturbations and natural variation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. Pei Zhao & Chao Wang & Shuhong Sun & Xi Wang & William E. Balch, 2024. "Tracing genetic diversity captures the molecular basis of misfolding disease," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    7. Bryan Sands & Soo Yun & Alexander R. Mendenhall, 2021. "Introns control stochastic allele expression bias," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    8. Masel, Joanna & Lyttle, David N., 2011. "The consequences of rare sexual reproduction by means of selfing in an otherwise clonally reproducing species," Theoretical Population Biology, Elsevier, vol. 80(4), pages 317-322.
    9. Kaushik Bhattacharya & Samarpan Maiti & Szabolcs Zahoran & Lorenz Weidenauer & Dina Hany & Diana Wider & Lilia Bernasconi & Manfredo Quadroni & Martine Collart & Didier Picard, 2022. "Translational reprogramming in response to accumulating stressors ensures critical threshold levels of Hsp90 for mammalian life," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    10. Casper J Breuker & James S Patterson & Christian Peter Klingenberg, 2006. "A Single Basis for Developmental Buffering of Drosophila Wing Shape," PLOS ONE, Public Library of Science, vol. 1(1), pages 1-7, December.
    11. Tracy Chih-Ting Koubkova-Yu & Jung-Chi Chao & Jun-Yi Leu, 2018. "Heterologous Hsp90 promotes phenotypic diversity through network evolution," PLOS Biology, Public Library of Science, vol. 16(11), pages 1-29, November.

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