Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution.
Morphological alterations have been shown to occur in Drosophila melanogaster when function of Hsp90 (heat shock 90-kDa protein 1alpha, encoded by Hsp83) is compromised during development. Genetic selection maintains the altered phenotypes in subsequent generations. Recent experiments have shown, however, that phenotypic variation still occurs in nearly isogenic recombinant inbred strains of Arabidopsis thaliana. Using a sensitized isogenic D. melanogaster strain, iso-Kr(If-1), we confirm this finding and present evidence supporting an epigenetic mechanism for Hsp90's capacitor function, whereby reduced activity of Hsp90 induces a heritably altered chromatin state. The altered chromatin state is evidenced by ectopic expression of the morphogen wingless in eye imaginal discs and a corresponding abnormal eye phenotype, both of which are epigenetically heritable in subsequent generations, even when function of Hsp90 is restored. Mutations in nine different genes of the trithorax group that encode chromatin-remodeling proteins also induce the abnormal phenotype. These findings suggest that Hsp90 acts as a capacitor for morphological evolution through epigenetic and genetic mechanisms.
Sollars
Vincent
V
Kimmel Cancer Institute, Thomas Jefferson University, Philadelphia, Pennsylvania 19107, USA.
Lu
Xiangyi
X
Xiao
Li
L
Wang
Xiaoyan
X
Garfinkel
Mark D
MD
Ruden
Douglas M
DM
D000818:Animals; D005075:Biological Evolution; D002843:Chromatin / Q000235:genetics / Q000378:metabolism; D029721:Drosophila Proteins / Q000032:analysis / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000033:anatomy & histology / Q000187:drug effects / Q000235:genetics* / Q000254:growth & development*; D005124:Eye Abnormalities / Q000235:genetics; D005260:Female; D018507:Gene Expression Regulation, Developmental; D014644:Genetic Variation; D018841:HSP90 Heat-Shock Proteins / Q000235:genetics*; D006360:Heat-Shock Proteins / Q000235:genetics / Q000378:metabolism; D008297:Male; D009154:Mutation; D010641:Phenotype; D011518:Proto-Oncogene Proteins / Q000032:analysis / Q000235:genetics; D012641:Selection, Genetic; D014921:Wings, Animal / Q000254:growth & development; D051155:Wnt1 Protein
D002843:Chromatin; D029721:Drosophila Proteins; D018841:HSP90 Heat-Shock Proteins; D006360:Heat-Shock Proteins; C089272:Hsp83 protein, Drosophila; D011518:Proto-Oncogene Proteins; D051155:Wnt1 Protein; C074622:wg protein, Drosophila