Urochordate betagamma-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. The vertebrate betagamma-crystallin genes encode abundant structural proteins critical for the function of the lens. 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 betagamma-crystallin. The crystal structure of Ciona betagamma-crystallin is very similar to that of a vertebrate betagamma-crystallin domain, except for paired, occupied calcium binding sites. The Ciona betagamma-crystallin is only expressed in the palps and in the otolith, the pigmented sister cell of the light-sensing ocellus. The Ciona betagamma-crystallin promoter region targeted expression to the visual system, including lens, in transgenic Xenopus tadpoles. We conclude that the vertebrate betagamma-crystallins evolved from a single domain protein already expressed in the neuroectoderm of the prevertebrate ancestor. The conservation of the regulatory hierarchy controlling betagamma-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.
Shimeld
Sebastian M
SM
Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford OX1 3PS, United Kingdom. sebastian.shimeld@zoo.ox.ac.uk
Purkiss
Andrew G
AG
Dirks
Ron P H
RP
Bateman
Orval A
OA
Slingsby
Christine
C
Lubsen
Nicolette H
NH
D000595:Amino Acid Sequence; D000818:Animals; D002938:Ciona intestinalis / Q000033:anatomy & histology / Q000235:genetics*; D003001:Cloning, Molecular; D003460:Crystallization; D019143:Evolution, Molecular; D005786:Gene Expression Regulation / Q000235:genetics; D049452:Green Fluorescent Proteins; D007908:Lens, Crystalline / Q000033:anatomy & histology*; D016013:Likelihood Functions; D008957:Models, Genetic; D008958:Models, Molecular; D008969:Molecular Sequence Data; D010802:Phylogeny; D016415:Sequence Alignment; D014961:X-Ray Diffraction; D014981:Xenopus; D038204:beta-Crystallins / Q000737:chemistry / Q000235:genetics*; D038222:gamma-Crystallins / Q000737:chemistry / Q000235:genetics*
D038204:beta-Crystallins; D038222:gamma-Crystallins; D049452:Green Fluorescent Proteins