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

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

doi:10.1073/pnas.0712200105

Cited by 166 publications

(195 citation statements)

References 42 publications

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“…This HSP90-responsive QTL is in a very similar position-Ϸ10 cM distal to the erecta locus-to a QTL observed in previous experiments using GDA to inhibit HSP90 (17). A colocalizing QTL has also been found in the CVI ϫ Ler RIL set (17).…”

Section: Hsp90-responsive Qtl Affecting Hypocotyl Length In the Darkmentioning

confidence: 50%

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HSP90-buffered genetic variation is common in Arabidopsis thaliana

Sangster

Salathia

Lee

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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132

118

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HSP90 is a protein chaperone particularly important in the maturation of a diverse set of proteins that regulate key steps in a multitude of biological processes. Alterations in HSP90 function produce altered phenotypes at low penetrance in natural populations. Previous work has shown that at least some of these phenotypes are due to genetic variation that remains phenotypically cryptic until it is revealed by the impairment of HSP90 function. Exposure of such ''buffered'' genetic polymorphisms can also be accomplished by environmental stress, linking the appearance of new phenotypes to defects in protein homeostasis. Should such polymorphisms be widespread, natural selection may be more effective at producing phenotypic change in suboptimal environments. In evaluating this hypothesis, a key unknown factor is the frequency with which HSP90-buffered polymorphisms occur in natural populations. Here, we present Arabidopsis thaliana populations suitable for genetic mapping that have constitutively reduced HSP90 levels. We employ quantitative genetic techniques to examine the HSP90-dependent polymorphisms affecting a host of plastic plant life-history traits. Our results demonstrate that HSP90-dependent natural variation is present at high frequencies in A. thaliana, with an expectation that at least one HSP90-dependent polymorphism will affect nearly every quantitative trait in progeny of two different wild lines. Hence, HSP90 is likely to occupy a central position in the translation of genotypic variation into phenotypic differences.cryptic variation ͉ molecular chaperone ͉ morphological evolution

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Section: Hsp90-responsive Qtl Affecting Hypocotyl Length In the Darkmentioning

confidence: 50%

“…A previously created Col ϫ Ler RIL population (19) has been demonstrated to harbor several HSP90-dependent QTL affecting the hypocotyl length of dark-grown seedlings (17). These experiments used geldanamycin (GDA), a highly specific HSP90 inhibitor (20).…”

Section: Hsp90-responsive Qtl Affecting Hypocotyl Length In the Darkmentioning

confidence: 99%

HSP90-buffered genetic variation is common in Arabidopsis thaliana

Sangster

Salathia

Lee

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

132

118

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“…Useful results taking that approach are likely with exceedingly low probability and little of mechanistic interest will likely emerge as a byproduct. An alternative approach based on modulating expression of multiple aquaporins using RNAi may be possible; Sangster et al (2004Sangster et al ( , 2008aSangster et al ( , 2008b, for example, used this approach successfully to determine the function of the HSP90s in A. thaliana. Figure 2 illustrates a basic schematic model for response of a plant to any environmental stimulus.…”

Section: Water and Transpirationmentioning

confidence: 99%

The integration of activity in saline environments: problems and perspectives

Cheeseman

2013

Functional Plant Biol.

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Abstract. The successful integration of activity in saline environments requires flexibility of responses at all levels, from genes to life cycles. Because plants are complex systems, there is no 'best' or 'optimal' solution and with respect to salt, glycophytes and halophytes are only the ends of a continuum of responses and possibilities. In this review, I briefly examine seven major aspects of plant function and their responses to salinity including transporters, secondary stresses, carbon acquisition and allocation, water and transpiration, growth and development, reproduction, and cytosolic function and 'integrity'. I conclude that new approaches are needed to move towards understanding either organismal integration or 'salt tolerance', especially cessation of protocols dependent on sudden, often lethal, shock treatments and the embracing of systems level resources. Some of the tools needed to understand the integration of activity and even 'salt stress' are already in hand, such as those for whole-transcriptome analysis. Others, ranging from discovery studies of the nature of the cytosol to expanded tool kits for proteomic, metabolomic and epigenomic studies, still need to be further developed. After resurrecting the distinction between applied stress and the resultant strain and noting that with respect to salinity, the strain is manifest in changes at all -omic levels, I conclude that it should be possible to model and quantify stress responses.

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“…One of the more intriguing observations is that wild-type phenotypes are robust to much environmental and genetic variation (Sangster et al 2008a;McGuigan & Sgrò 2009). Waddington (1942) coined the term canalization to describe this phenotypic robustness; individuals with different genotypes have the same phenotype (or a limited set of phenotypes), which is expressed despite variation in the environment.…”

Section: Introductionmentioning

confidence: 99%

“…Mutations derived by laboratory mutagenesis are expected to have more dramatic phenotypic effects than naturally segregating variation (van der Straten et al 1997), and RNAi disruption of Hsp90 (Sangster et al 2008a) likewise may have effects on Hsp90 expression and functioning much larger than those found in nature. It is not known if natural variants in Hsp90 or genes involved in its regulation might exert effects on phenotypic variability in wild populations.…”

Section: Introductionmentioning

confidence: 99%

A naturally occurring variant of Hsp90 that is associated with decanalization

2010

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The heat shock protein Hsp90 has been the focus of many studies since it was suggested that it acts to mediate the buffering of phenotypic variation. Hsp90-mediated buffering may result in the accumulation of cryptic genetic variation that, when released either as a consequence of environmental or genetic stress, increases the evolvability of a population. Recent studies using laboratory-induced mutations of Hsp90 and/or chemical inhibition to disrupt Hsp90 function confirm that Hsp90 can buffer cryptic genetic variation. We have previously identified a naturally occurring variant in the charged linker region of the Hsp90 gene, and now examine whether this variant is associated with altered levels of trait variability. The variant is associated with the release of cryptic genetic variation for canalized morphological (bristle) traits, but not for uncanalized morphological (wing and bristle) traits, and the effect on canalized traits depends on culture temperature. This suggests that natural genetic variation in Hsp90 may mediate the evolution of canalized morphological traits even if it does not influence the expression of variation for uncanalized traits.

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

Cited by 166 publications

References 42 publications

HSP90-buffered genetic variation is common in Arabidopsis thaliana

HSP90-buffered genetic variation is common in Arabidopsis thaliana

The integration of activity in saline environments: problems and perspectives

A naturally occurring variant of Hsp90 that is associated with decanalization

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