HSP90-buffered genetic variation is common in Arabidopsis thaliana

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.

Fig. 1.

QTL affecting dark hypocotyl length. Red, HSP90-reduced set; green, control set. QTL significance (interval map) is in LOD; a horizontal line of the appropriate color denotes a genome-wide α = 0.05 significance threshold.

Fig. 2.

Significant QTL for chromosomes 2–4. Red, HSP90-RNAi set; green, control set. Stars denote significantly HSP90-responsive QTL. Black bar, most significant location for QTL; box, 2-LOD interval. QTL significance is in shades of gray. Additive effect by direction of arrow, up signifies that Col-0 allele increases the trait mean. Trait variance explained by QTL by size of arrow. Traits: 1, days from germination to flowering; 2, rosette leaf number; 3, cauline leaf number; 4, total leaf number; 5, longest leaf length; 6, longest leaf width; 7, longest leaf depth; 8, longest leaf petiole length; 9, longest leaf petiole length:longest leaf length; 10, longest leaf surface area; 11, longest leaf volume; 12, internode mean; 13, plant height; 14, days actively flowering; 15, growth per day; 16, primary stem fertile siliques; 17, primary stem infertile siliques; 18, primary stem total siliques; 19, secondary stems from rosette; 20, secondary stems from primary stem; 21, dry mass of aerial tissue; 22, total seed weight; 23, total seed weight:dry mass.