Evolution of graded refractive index in squid lenses.
A lens with a graded refractive index is required for vision in aquatic animals with camera-type eyes. This optical design entails a radial gradient of protein density, with low density in external layers and high density in internal layers. To maintain the optical stability of the eye, different material properties are required for proteins in different regions of the lens. In low-density regions of the lens where slight protein aggregation causes significant light scattering, aggregation must be minimized. Squid lens S-crystallin proteins are evolutionarily derived from the glutathione S-transferase protein family. We used biochemistry, optical modelling and phylogenetics to study the evolution and material properties of S-crystallins. S-crystallins are differentially expressed in a radial gradient, suggesting a role in refractive index. This gradient in S-crystallin expression is correlated with their evolutionary history and biochemistry. S-crystallins have been under positive selection. This selection appears to have resulted in stabilization of derived S-crystallins via mutations in the dimer interface and extended electrostatic fields. These derived S-crystallins probably cause the glassy organization and stability of low refractive index lens layers. Our work elucidates the molecular and evolutionary mechanisms underlying the production and maintenance of camera-like optics in squid lenses.
Sweeney
Alison M
AM
Department of Biology, Duke University, Durham, NC 27708, USA. ams27@duke.edu
Des Marais
David L
DL
Ban
Yih-En Andrew
YE
Johnsen
Sönke
S
D000595:Amino Acid Sequence; D000818:Animals; D005075:Biological Evolution; D003459:Crystallins / Q000737:chemistry* / Q000235:genetics; D049832:Decapodiformes / Q000502:physiology*; D019281:Dimerization; D005982:Glutathione Transferase / Q000235:genetics; D007908:Lens, Crystalline / Q000502:physiology; D008969:Molecular Sequence Data; D010802:Phylogeny; D012031:Refractometry; D019032:Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization; D055672:Static Electricity
D003459:Crystallins; D005982:Glutathione Transferase