Urochordate βγ-crystallin and the evolutionary origin of the vertebrate eye lens

A refracting lens is a key component of our image-forming camera eye; however, its evolutionary origin is unknown because precursor structures appear absent in nonvertebrates [1]. The vertebrate beta gamma-crystallin genes encode abundant structural proteins critical for the function of the lens [2]. We show that the urochordate Ciona intestinalis, which split from the vertebrate lineage before the evolution of the lens, has a single gene coding for a single domain monomeric beta gamma-crystallin. The crystal structure of Ciona beta gamma-crystallin is very similar to that of a vertebrate beta gamma-crystallin domain, except for paired, occupied calcium binding sites. The Ciona beta gamma-crystallin is only expressed in the palps and in the otolith, the pigmented sister cell of the light-sensing ocellus. The Ciona beta gamma-crystallin promoter region targeted expression to the visual system, including lens, in transgenic Xenopus tadpoles. We conclude that the vertebrate beta gamma-crystallins evolved from a single domain protein already expressed in the neuroectoderm of the prevertebrate ancestor. The conservation of the regulatory hierarchy controlling beta gamma-crystallin expression between organisms with and without a lens shows that the evolutionary origin of the lens was based on co-option of pre-existing regulatory circuits controlling the expression of a key structural gene in a primitive light-sensing system.