Literature DB >> 18287065

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

Todd A Sangster1, Neeraj Salathia, Soledad Undurraga, Ron Milo, Kurt Schellenberg, Susan Lindquist, Christine Queitsch.   

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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Year:  2008        PMID: 18287065      PMCID: PMC2268568          DOI: 10.1073/pnas.0712200105

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  29 in total

Review 1.  Between genotype and phenotype: protein chaperones and evolvability.

Authors:  Suzanne L Rutherford
Journal:  Nat Rev Genet       Date:  2003-04       Impact factor: 53.242

2.  Bay-0 x Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis.

Authors:  O. Loudet; S. Chaillou; C. Camilleri; D. Bouchez; F. Daniel-Vedele
Journal:  Theor Appl Genet       Date:  2002-02-13       Impact factor: 5.699

3.  Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability.

Authors:  Claire C Milton; Brandon Huynh; Philip Batterham; Suzanne L Rutherford; Ary A Hoffmann
Journal:  Proc Natl Acad Sci U S A       Date:  2003-10-31       Impact factor: 11.205

4.  A study of canalization and developmental stability in the sternopleural bristle system of Drosophila melanogaster.

Authors:  Ian Dworkin
Journal:  Evolution       Date:  2005-07       Impact factor: 3.694

5.  Hsp90 as a capacitor for morphological evolution.

Authors:  S L Rutherford; S Lindquist
Journal:  Nature       Date:  1998-11-26       Impact factor: 49.962

Review 6.  Heat-shock protein 90, a chaperone for folding and regulation.

Authors:  D Picard
Journal:  Cell Mol Life Sci       Date:  2002-10       Impact factor: 9.261

7.  Natural variation in light sensitivity of Arabidopsis.

Authors:  J N Maloof; J O Borevitz; T Dabi; J Lutes; R B Nehring; J L Redfern; G T Trainer; J M Wilson; T Asami; C C Berry; D Weigel; J Chory
Journal:  Nat Genet       Date:  2001-12       Impact factor: 38.330

8.  STAIRS: a new genetic resource for functional genomic studies of Arabidopsis.

Authors:  Rachil Koumproglou; Tim M Wilkes; Paul Townson; Xiao Y Wang; Jim Beynon; Harpal S Pooni; H John Newbury; Mike J Kearsey
Journal:  Plant J       Date:  2002-08       Impact factor: 6.417

9.  Maturation of the tyrosine kinase c-src as a kinase and as a substrate depends on the molecular chaperone Hsp90.

Authors:  Y Xu; M A Singer; S Lindquist
Journal:  Proc Natl Acad Sci U S A       Date:  1999-01-05       Impact factor: 11.205

10.  Hsp90 selectively modulates phenotype in vertebrate development.

Authors:  Patricia L Yeyati; Ruth M Bancewicz; John Maule; Veronica van Heyningen
Journal:  PLoS Genet       Date:  2007-02-08       Impact factor: 5.917

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  72 in total

Review 1.  HSP90 at the hub of protein homeostasis: emerging mechanistic insights.

Authors:  Mikko Taipale; Daniel F Jarosz; Susan Lindquist
Journal:  Nat Rev Mol Cell Biol       Date:  2010-06-09       Impact factor: 94.444

2.  HSP90 functions in the circadian clock through stabilization of the client F-box protein ZEITLUPE.

Authors:  Tae-sung Kim; Woe Yeon Kim; Sumire Fujiwara; Jeongsik Kim; Joon-Yung Cha; Jin Ho Park; Sang Yeol Lee; David E Somers
Journal:  Proc Natl Acad Sci U S A       Date:  2011-09-26       Impact factor: 11.205

3.  Detection of a gravitropism phenotype in glutamate receptor-like 3.3 mutants of Arabidopsis thaliana using machine vision and computation.

Authors:  Nathan D Miller; Tessa L Durham Brooks; Amir H Assadi; Edgar P Spalding
Journal:  Genetics       Date:  2010-07-20       Impact factor: 4.562

4.  Stress, genomes, and evolution.

Authors:  David Mittelman; John H Wilson
Journal:  Cell Stress Chaperones       Date:  2010-06-04       Impact factor: 3.667

5.  Heritability and adaptive phenotypic plasticity of adult body size in the mosquito Aedes aegypti with implications for dengue vector competence.

Authors:  Jennifer R Schneider; Dave D Chadee; Akio Mori; Jeanne Romero-Severson; David W Severson
Journal:  Infect Genet Evol       Date:  2010-11-09       Impact factor: 3.342

6.  Epigenetic variation contributes to environmental adaptation of Arabidopsis thaliana.

Authors:  Rik Kooke; Joost J B Keurentjes
Journal:  Plant Signal Behav       Date:  2015

Review 7.  Genetic assimilation: a review of its potential proximate causes and evolutionary consequences.

Authors:  Ian M Ehrenreich; David W Pfennig
Journal:  Ann Bot       Date:  2015-09-10       Impact factor: 4.357

Review 8.  Decanalizing thinking on genetic canalization.

Authors:  Kerry Geiler-Samerotte; Federica M O Sartori; Mark L Siegal
Journal:  Semin Cell Dev Biol       Date:  2018-05-24       Impact factor: 7.727

9.  Trithorax requires Hsp90 for maintenance of active chromatin at sites of gene expression.

Authors:  Muhammad Tariq; Ute Nussbaumer; Yujie Chen; Christian Beisel; Renato Paro
Journal:  Proc Natl Acad Sci U S A       Date:  2009-01-14       Impact factor: 11.205

10.  HSP90-buffered genetic variation is common in Arabidopsis thaliana.

Authors:  Todd A Sangster; Neeraj Salathia; Hana N Lee; Etsuko Watanabe; Kurt Schellenberg; Keith Morneau; Hui Wang; Soledad Undurraga; Christine Queitsch; Susan Lindquist
Journal:  Proc Natl Acad Sci U S A       Date:  2008-02-19       Impact factor: 11.205

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