GENETICS
HSP90-buffered genetic variation is common in Arabidopsis thaliana
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*Committee on Genetics, University of Chicago, Chicago, IL 60637;
Whitehead Institute for Biomedical Research, Howard Hughes Medical Institute, Cambridge, MA 02142; and
FAS Center for Systems Biology, Harvard University, Cambridge, MA 02138
Contributed by Susan Lindquist, December 25, 2007 (sent for review December 16, 2007)
Abstract
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
Author contributions: T.A.S., N.S., C.Q., and S.L. designed research; T.A.S., N.S., H.N.L., E.W., K.S., K.M., H.W., S.U., and C.Q. performed research; T.A.S., N.S., H.N.L., E.W., and C.Q. analyzed data; and T.A.S., C.Q., and S.L. wrote the paper.
Present addresses: Genomics Institute of the Novartis Research Foundation, San Diego, CA 92121.
¶Present addresses: Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720.
||Present addresses: Department of Genome Sciences, University of Washington, Seattle, WA 98195.
**Present addresses: The Arnold Arboretum, Harvard University, Cambridge, MA 02138.
The authors declare no conflict of interest.
To whom correspondence may be addressed. E-mail: lindquist_admin{at}wi.mit.edu or queitsch{at}u.washington.edu
© 2008 by The National Academy of Sciences of the USA
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