Abstract
Hox and ParaHox genes are transcriptional regulators vital for many aspects of embryonic development in bilaterian animals and are considered to have originated from one ancestral proto-Hox/ParaHox cluster. Hox genes are clustered in the genome of both protostomes and deuterostomes, and there is a specific relationship between the position of a gene in the cluster and the position of its expression along the animal body axis (colinearity). It is not clear whether the ParaHox genes Gsx, Xlox, and, Cdx generally exhibit a similar phenomenon since developmental expression for all three ParaHox genes within a single species has not yet been described for any protostome animal. Here we show the spatial and temporal localization for all three ParaHox genes in the polychaete Capitella sp. I, a member of one of the morphologically most diverse and understudied groups within the Metazoa, the Lophotrochozoa. Our data demonstrate that although both CapI-Xlox and CapI-Cdx are regionally expressed in the gut, the three Capitella sp. I ParaHox genes as a group do not perfectly fit predictions of temporal or spatial colinearity. Instead, there is a conservation of expression across species associated with development of particular tissues, and the relative order of initiation of ParaHox gene expression likely reflects the relative order of species-specific tissue development during ontogenesis.
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References
Brooke NM, Garcia-Fernandez J, Holland PWH (1998) The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 392:920–922
Chawengsaksophak K, Beck F (1996) Chromosomal location of cdx2, a murine homologue of the Drosophila gene caudal, to mouse chromosome 5. Genomics 34:270–271
Copf T, Schroder R, Averof M (2004) Ancestral role of caudal genes in axis elongation and segmentation. PNAS 101:17711–17715
de Rosa R, Grenier JK, Andreeva T, Cook CE, Adoutte A, Akam M, Carroll S, Balavoine G (1999) Hox genes in brachiopods and priapulids and protostome evolution. Nature 399:772–776
de Rosa R, Prud’homme B, Balavoine G (2005) Caudal and even-skipped in the annelid Platynereis dumerilii and ancestry of posterior growth. Evol Dev 7:574–587
Duprey P, Chowdhury K, Dressler G, Balling R, Simon D, Guenet J, Gruss P (1988) A mouse gene homologous to the Drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev 12A:1647–1654
Eisig H (1899) Zur Entwicklungsgeschichte der Capitelliden. Mitt Zool Stn Neapel 13:1–292
Ferrier DEK, Holland PWH (2001) Sipunculan ParaHox genes. Evol Dev 3:263–270
Ferrier DEK, Holland PWH (2002) Ciona intestinalis ParaHox genes: evolution of Hox/ParaHox cluster integrity, developmental mode, and temporal colinearity. Mol Phylogenet Evol 24:412–417
Fiedorek F, Kay E (1995) Mapping of the insulin promoter factor 1 gene (IPF1) to distal mouse chromosome 5. Genomics 28:581–584
Gamer L, Wright C (1993) Murine Cdx-4 bears striking similarities to the Drosophila caudal gene in its homeodomain sequence and early expression pattern. Mech Dev 43:71–81
Garcia-Fernandez J (2005) Hox, ParaHox, ProtoHox: facts and guesses. Heredity 94:145–152
Gont L, Steinbeisser H, Blumberg B, de Robertis E (1993) Tail formation as a continuation of gastrulation: the multiple cell populations of the Xenopus tailbud derive from the late blastopore lip. Development 119:991–1004
Holland PWH (2001) Beyond the Hox: how widespread is homeobox gene clustering? J Anat 199:13–23
Hsieh-Li HM, Witte DP, Szucsk JC, Weinstein M, Li H, Potter S (1995) Gsh-2, a murine homeobox gene expressed in the developing brain. Mech Dev 50:177–186
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Hwang S, Wu J, Chen C, Hui C, Chen C (2003) Novel pattern of AtXlox gene expression in starfish Archaster typicus embryos. Dev Growth Differ 45:85–93
Inoue H, Riggs A, Tanizawa Y, Ueda K, Kuwano A, Liu L, Donis-Keller H, Permutt M (1996) Isolation, characterization, and chromosomal mapping of the human insulin promoter factor 1 (IPF-1) gene. Diabetes 45:789–794
Iwanoff PP (1928) Die Entwicklung der Larvalsegmente bei den Anneliden. Z Morphol Okol Tiere 10:62–161
Kourakis MJ, Martindale MQ (2000) Combined-method phylogenetic analysis of Hox and ParaHox genes of the Metazoa. J Exp Zool 288:175–191
Le Gouar M, Lartillot N, Adoutte A, Vervoort M (2003) The expression of a caudal homologue in a mollusc, Patella vulgata. Gene Expr Patterns 3:35–37
Macdonald P, Struhl G (1986) A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 324:537–545
Marom K, Shapira E, Fainsod A (1997) The chicken caudal genes establish an anterior–posterior gradient by partially overlapping temporal and spatial patterns of expression. Mech Dev 64:41–52
Matsuo K, Yoshida H, Shimizu T (2005) Differential expression of caudal and dorsal genes in the teloblast lineages of the oligochaete annelid Tubifex tubifex. Dev Genes Evol 215:238–247
McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302
Ohlsson H, Karlsson K, Edlund T (1993) IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J 12:4251–4259
Pillemer G, Epstein M, Blumberg B, Yisraeli J, De Robertis E, Steinbeisser H, Fainsod A (1998) Nested expression and sequential downregulation of the Xenopus caudal genes along the anterior–posterior axis. Mech Dev 71:193–196
Pollard S, Holland PWH (2000) Evidence for 14 homeobox clusters in human genome ancestry. Curr Biol 10:1059–1062
Reece-Hoyes J, Keenan I, Isaacs H (2002) Cloning and expression of the Cdx family from the frog Xenopus tropicalis. Dev Dyn 223:134–140
Ruvkun G, Hobert O (1998) The taxonomy of developmental control in Caenorhabditis elegans. Science 282:2033–2041
Seaver EC, Kaneshige LM (in press) Expression of ‘segmentation’ genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans. Dev Biol
Seaver EC, Thamm K, Hill SD (2005) Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages. Evol Dev 7:312–326
Subramanian V, Meyer B, Gruss P (1995) Disruption of the murine homeobox gene Cdx1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell 83:641–653
Swofford DL (2002) PAUP* 4.0: phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, MA
Urbach R, Technau G (2003) Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130:3621–3637
Wedeen CJ, Shankland M (1997) Mesoderm is required for the formation of a segmented endodermal cell layer in the leech Helobdella. Dev Biol 191:202–214
Weiss JB, Von Ohlen T, Mellerick DM, Dressler G, Doe CQ, Scott MP (1998) Dorsoventral patterning in the Drosophila central nervous system: the intermediate neuroblasts defective homeobox gene specifies intermediate column identity. Genes Dev 12:3591–3602
Wright C, Schnegelsberg P, De Roberts EM (1989) XlHbox 8: a novel Xenopus homeo protein restricted to a narrow band of endoderm. Development 105:787–794
Wu LH, Lengyel JA (1998) Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125:2433–2442
Wysocka-Diller JW, Aisemberg GO, Macagno ER (1995) A novel homeobox cluster expressed in repeated structures of the midgut. Dev Biol 171:439–447
Acknowledgements
This work was supported by NSF (IBN00-94925). We are grateful to members of Kewalo Marine Lab for discussions and comments on the preparation of this manuscript.
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Communicated by D.A. Weisblat
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Fröbius, A.C., Seaver, E.C. ParaHox gene expression in the polychaete annelid Capitella sp. I. Dev Genes Evol 216, 81–88 (2006). https://doi.org/10.1007/s00427-005-0049-0
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DOI: https://doi.org/10.1007/s00427-005-0049-0