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

• Published in: Proceedings of the National Academy of Sciences - PNAS 2008-02, Vol.105 (8), p.2963-2968
• Main Authors: Sangster, Todd A, Salathia, Neeraj, Undurraga, Soledad, Milo, Ron, Schellenberg, Kurt, Lindquist, Susan, Queitsch, Christine
• Format: Article
• Language: English
• Subjects: alleles; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis thaliana; Biological Sciences; Chromosomes; Evolution; Evolutionary genetics; Gene expression; Genetic diversity; Genetic Variation; Genetics; Genotype & phenotype; Genotypes; heat shock proteins; HSP90 Heat-Shock Proteins - genetics; Hypocotyl - growth & development; Hypocotyls; molecular chaperones; Phenotype; Phenotypes; Phenotypic traits; phenotypic variation; plant proteins; Plant Roots - growth & development; Polymorphism; Quantitative genetics; Quantitative Trait Loci; seedling growth
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.0712200105

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.