Engrailed in Cephalopods: a Key Gene Related to the Emergence of Morphological Novelties

Overview

Journal Dev Genes Evol

Specialty Biology

Date 2007 Mar 31

PMID 17394016

Citations 10

Authors

S Baratte

A Andouche

L Bonnaud

Affiliations

Soon will be listed here.

Abstract

The engrailed gene is a transcription factor required in numerous species for major developmental steps (neurogenesis, limb development, boundary establishment), and its evolution is known to be closely related to the evolution of the metazoan body plan. Cephalopods exhibit numerous morphological peculiarities among molluscs, such as a direct development, a complex sensory and nervous system (eyes, brain, giant axons), a reduced shell, a funnel, and a brachial crown. We assessed a potential recruitment of engrailed in the development of these derived traits and examined the expression pattern of engrailed during the organogenesis of the cuttlefish Sepia officinalis, by immunostaining. Engrailed was detected at the margin of the prospective internal shell, which is consistent with studies on molluscs having an external shell and confirms a conserved role of engrailed in delimitating the molluscan shell compartment. Interestingly, unexpected patterns were early detected in the emerging arms, funnel and optic vesicles and latter in tentacles and eye lids. We also identified an engrailed cognate in the squid Loligo, which provides new evidence that engrailed in molluscs is not restricted to a 'shell function' and has been recruited in the mollusc lineage for the emergence of morphological novelties in cephalopods.

Citing Articles

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References

Joyner A . Engrailed, Wnt and Pax genes regulate midbrain--hindbrain development. Trends Genet. 1996; 12(1):15-20. DOI: 10.1016/0168-9525(96)81383-7. View

Raftery L, Sanicola M, Blackman R, Gelbart W . The relationship of decapentaplegic and engrailed expression in Drosophila imaginal disks: do these genes mark the anterior-posterior compartment boundary?. Development. 1991; 113(1):27-33. DOI: 10.1242/dev.113.1.27. View

Force A, Lynch M, Pickett F, Amores A, Yan Y, Postlethwait J . Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999; 151(4):1531-45. PMC: 1460548. DOI: 10.1093/genetics/151.4.1531. View

Plaza S, Langlois M, Turque N, LeCornet S, Bailly M, Begue A . The homeobox-containing Engrailed (En-1) product down-regulates the expression of Pax-6 through a DNA binding-independent mechanism. Cell Growth Differ. 1997; 8(10):1115-25. View

Yaguchi S, Nakajima Y, Wang D, Burke R . Embryonic expression of engrailed in sea urchins. Gene Expr Patterns. 2006; 6(5):566-71. DOI: 10.1016/j.modgep.2005.10.004. View

Quiring R, Walldorf U, Kloter U, Gehring W . Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science. 1994; 265(5173):785-9. DOI: 10.1126/science.7914031. View

Seaver E, Kaneshige L . Expression of 'segmentation' genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans. Dev Biol. 2005; 289(1):179-94. DOI: 10.1016/j.ydbio.2005.10.025. View

Moshel S, Levine M, Collier J . Shell differentiation and engrailed expression in the Ilyanassa embryo. Dev Genes Evol. 1998; 208(3):135-41. DOI: 10.1007/s004270050164. View

Nederbragt A, van Loon A, Dictus W . Expression of Patella vulgata orthologs of engrailed and dpp-BMP2/4 in adjacent domains during molluscan shell development suggests a conserved compartment boundary mechanism. Dev Biol. 2002; 246(2):341-55. DOI: 10.1006/dbio.2002.0653. View

10.

Hartmann B, Lee P, Kang Y, Tomarev S, DE Couet H, Callaerts P . Pax6 in the sepiolid squid Euprymna scolopes: evidence for a role in eye, sensory organ and brain development. Mech Dev. 2003; 120(2):177-83. DOI: 10.1016/s0925-4773(02)00456-2. View

11.

Gritzan U, Hatini V, DiNardo S . Mutual antagonism between signals secreted by adjacent wingless and engrailed cells leads to specification of complementary regions of the Drosophila parasegment. Development. 1999; 126(18):4107-15. DOI: 10.1242/dev.126.18.4107. View

12.

Seaver E, Paulson D, Irvine S, Martindale M . The spatial and temporal expression of Ch-en, the engrailed gene in the polychaete Chaetopterus, does not support a role in body axis segmentation. Dev Biol. 2001; 236(1):195-209. DOI: 10.1006/dbio.2001.0309. View

13.

Hidalgo A . Growth and patterning from the engrailed interface. Int J Dev Biol. 1998; 42(3):317-24. View

14.

Holland L, Kene M, Williams N, Holland N . Sequence and embryonic expression of the amphioxus engrailed gene (AmphiEn): the metameric pattern of transcription resembles that of its segment-polarity homolog in Drosophila. Development. 1997; 124(9):1723-32. DOI: 10.1242/dev.124.9.1723. View

15.

Brunet I, Weinl C, Piper M, Trembleau A, Volovitch M, Harris W . The transcription factor Engrailed-2 guides retinal axons. Nature. 2005; 438(7064):94-8. PMC: 3785142. DOI: 10.1038/nature04110. View

16.

Kornberg T . Engrailed: a gene controlling compartment and segment formation in Drosophila. Proc Natl Acad Sci U S A. 1981; 78(2):1095-9. PMC: 319953. DOI: 10.1073/pnas.78.2.1095. View

17.

Logan C, Wizenmann A, Drescher U, Monschau B, BONHOEFFER F, Lumsden A . Rostral optic tectum acquires caudal characteristics following ectopic engrailed expression. Curr Biol. 1996; 6(8):1006-14. DOI: 10.1016/s0960-9822(02)00645-0. View

18.

Jacobs D, Wray C, Wedeen C, Kostriken R, DeSalle R, Staton J . Molluscan engrailed expression, serial organization, and shell evolution. Evol Dev. 2001; 2(6):340-7. DOI: 10.1046/j.1525-142x.2000.00077.x. View

19.

Gibert J . The evolution of engrailed genes after duplication and speciation events. Dev Genes Evol. 2002; 212(7):307-18. DOI: 10.1007/s00427-002-0243-2. View

20.

Patel N, Coleman K, Poole S, ELLIS M, Kornberg T, Goodman C . Expression of engrailed proteins in arthropods, annelids, and chordates. Cell. 1989; 58(5):955-68. DOI: 10.1016/0092-8674(89)90947-1. View