GENETICS
HSP90 affects the expression of genetic variation and developmental stability in quantitative traits
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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;
||Department of Systems Biology, Harvard Medical School, Boston, MA 02115; and
FAS Center for Systems Biology, Harvard University, Cambridge, MA 02138
Contributed by Susan Lindquist, December 24, 2007 (sent for review December 2, 2007)
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.
cryptic variation | morphological evolution
Author contributions: T.A.S., N.S., S.L., and C.Q. designed research; T.A.S., N.S., S.U., K.S., and C.Q. performed research; R.M. contributed new analytic tools; T.A.S., N.S., R.M., and C.Q. analyzed data; and T.A.S., S.L., and C.Q. wrote the paper.
Present address: Genomics Institute of the Novartis Research Foundation, San Diego, CA 92121.
¶Present address: The Arnold Arboretum, Harvard University, Cambridge, MA 02138.
**Present address: 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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