Sea Urchin Tube Feet Are Photosensory Organs That Express a Rhabdomeric-like Opsin and PAX6

Overview

Journal Proc Biol Sci

Specialty Biology

Date 2011 Apr 1

PMID 21450733

Citations 25

Authors

Michael P Lesser

Karen L Carleton

Stefanie A Bottger

Thomas M Barry

Charles W Walker

Affiliations

Soon will be listed here.

Abstract

All echinoderms have unique hydraulic structures called tube feet, known for their roles in light sensitivity, respiration, chemoreception and locomotion. In the green sea urchin, the most distal portion of these tube feet contain five ossicles arranged as a light collector with its concave surface facing towards the ambient light. These ossicles are perforated and lined with pigment cells that express a PAX6 protein that is universally involved in the development of eyes and sensory organs in other bilaterians. Polymerase chain reaction (PCR)-based sequencing and real time quantitative PCR (qPCR) also demonstrate the presence and differential expression of a rhabdomeric-like opsin within these tube feet. Morphologically, nerves that could serve to transmit information to the test innervate the tube feet, and the differential expression of opsin transcripts in the tube feet is inversely, and significantly, related to the amount of light that tube feet are exposed to depending on their location on the test. The expression of these genes, the differential expression of opsin based on light exposure and the unique morphological features at the distal portion of the tube foot strongly support the hypothesis that in addition to previously identified functional roles of tube feet they are also photosensory organs that detect and respond to changes in the underwater light field.

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References

Nathans J, Hogness D . Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell. 1983; 34(3):807-14. DOI: 10.1016/0092-8674(83)90537-8. View

Katoh K, Misawa K, Kuma K, Miyata T . MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30(14):3059-66. PMC: 135756. DOI: 10.1093/nar/gkf436. View

Arnheiter H . Evolutionary biology. Eyes viewed from the skin. Nature. 1998; 391(6668):632-3. DOI: 10.1038/35487. View

Moutsaki P, Bellingham J, Soni B, Foster R . Sequence, genomic structure and tissue expression of carp (Cyprinus carpio L.) vertebrate ancient (VA) opsin. FEBS Lett. 2000; 473(3):316-22. DOI: 10.1016/s0014-5793(00)01550-7. View

Santos R, Gorb S, Jamar V, Flammang P . Adhesion of echinoderm tube feet to rough surfaces. J Exp Biol. 2005; 208(Pt 13):2555-67. DOI: 10.1242/jeb.01683. View

Karnik S, Sakmar T, Chen H, Khorana H . Cysteine residues 110 and 187 are essential for the formation of correct structure in bovine rhodopsin. Proc Natl Acad Sci U S A. 1988; 85(22):8459-63. PMC: 282477. DOI: 10.1073/pnas.85.22.8459. View

Aizenberg J, Tkachenko A, Weiner S, Addadi L, HENDLER G . Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature. 2001; 412(6849):819-22. DOI: 10.1038/35090573. View

Tomarev S, Callaerts P, Kos L, Zinovieva R, Halder G, Gehring W . Squid Pax-6 and eye development. Proc Natl Acad Sci U S A. 1997; 94(6):2421-6. PMC: 20103. DOI: 10.1073/pnas.94.6.2421. View

Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn A, Wittbrodt J . Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science. 2004; 306(5697):869-71. DOI: 10.1126/science.1099955. View

10.

Halder G, Callaerts P, Gehring W . Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science. 1995; 267(5205):1788-92. DOI: 10.1126/science.7892602. View

11.

Johnsen S . Identification and localization of a possible rhodopsin in the echinoderms Asterias forbesi (Asteroidea) and Ophioderma brevispinum (Ophiuroidea). Biol Bull. 1997; 193(1):97-105. DOI: 10.2307/1542739. View

12.

Yerramilli D, Johnsen S . Spatial vision in the purple sea urchin Strongylocentrotus purpuratus (Echinoidea). J Exp Biol. 2009; 213(2):249-55. DOI: 10.1242/jeb.033159. View

13.

Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D . The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1998; 25(24):4876-82. PMC: 147148. DOI: 10.1093/nar/25.24.4876. View

14.

Wang J, McDowell J, HARGRAVE P . Site of attachment of 11-cis-retinal in bovine rhodopsin. Biochemistry. 1980; 19(22):5111-7. DOI: 10.1021/bi00563a027. View

15.

Kojima D, Terakita A, Ishikawa T, Tsukahara Y, Maeda A, Shichida Y . A novel Go-mediated phototransduction cascade in scallop visual cells. J Biol Chem. 1997; 272(37):22979-82. DOI: 10.1074/jbc.272.37.22979. View

16.

Ebnet E, Fischer M, DEININGER W, Hegemann P . Volvoxrhodopsin, a light-regulated sensory photoreceptor of the spheroidal green alga Volvox carteri. Plant Cell. 1999; 11(8):1473-84. PMC: 144291. DOI: 10.1105/tpc.11.8.1473. View

17.

Crawford B, Burke R . TEM and SEM methods. Methods Cell Biol. 2004; 74:411-41. DOI: 10.1016/s0091-679x(04)74017-0. View

18.

Florey E, Cahill M . Cholinergic motor control of sea urchin tube feet: evidence for chemical transmission without synapses. J Exp Biol. 1980; 88:281-92. DOI: 10.1242/jeb.88.1.281. View

19.

Czerny T, Busslinger M . DNA-binding and transactivation properties of Pax-6: three amino acids in the paired domain are responsible for the different sequence recognition of Pax-6 and BSAP (Pax-5). Mol Cell Biol. 1995; 15(5):2858-71. PMC: 230517. DOI: 10.1128/MCB.15.5.2858. View

20.

Arendt D . Evolution of eyes and photoreceptor cell types. Int J Dev Biol. 2004; 47(7-8):563-71. View