Abstract
Hox genes encode a set of evolutionarily conserved transcription factors that regulate anterior–posterior patterning. Here we report the first developmental expression of a Hox gene from Chaetognatha. These metazoans have been shown recently to be part of the protostome group of bilaterians. We describe the analysis of the SceMed4 gene (a Spadella cephaloptera Median Hox gene) including its expression from late stages of egg development to 7 days after hatching. In all of these stages, SceMed4 is expressed in two lateral stripes in a restricted region of the developing ventral ganglion.
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Balavoine G, de Rosa R, Adoutte A (2002) Hox clusters and bilaterian phylogeny. Mol Phylogenet Evol 24:366–373
Bone Q, Pulsford A (1984) The sense organs and ventral ganglion of Sagitta (Chaetognatha). Acta Zool 65:209–220
Caroll SB, Grenier JK, Weatherbee SD (2001) From DNA to diversity, molecular genetics and the evolution of animal design. Blackwell, Oxford
Doncaster L (1902) On the development of Sagitta, with note on the anatomy of the adult. Q J Microsc Sci 46:351–398
Duvert M, Savineau JP, Campistron G, Onteniente B (1997) Distribution and role of aspartate in the nervous system of the chaetognath Sagitta. J Comp Neurol 380:485–494
Erber A, Riemer D, Bovenschulte M, Weber K (1998) Molecular phylogeny of metazoan intermediate filament proteins. J Mol Evol 47:751–762
Giribet G, Distel DL, Polz M, Sterrer W, Wheeler WC (2000) Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18s rDNA sequences and morphology. Syst Biol 49:539–562
Giusti AF, Hinman VF, Degnan SM, Degnan BM, Morse DE (2000) Expression of a Scr/Hox5 gene in the larval central nervous system of the gastropod Haliotis, a non-segmented spiralian lophotrochozoan. Evol Dev 2:294–302
Goto T, Katayama-Kumoi Y, Tohyama M, Yoshida M (1992) Distribution and development of the serotonin- and RFamide-like immunoreactive neurons in the arroworm, Paraspadella gotoi (Chaetognatha). Cell Tissue Res 267:215–222
Haase A, Stern M, Wachtler K, Bicker G (2001) A tissue-specific marker of Ecdysozoa. Dev Genes Evol 211:428–433
Halanych K (1996) Testing hypotheses of chaetognath origins: long branches revealed by 18S rDNA. Syst Biol 45:223–246
Helfenbein KG, Fourcade HM, Vanjani RG, Boore JL (2004) The mitochondrial genome of Paraspadella gotoi is highly reduced and reveals that chaetognaths are a sister group to protostomes. Proc Natl Acad Sci U S A 101:10639–10643
Hinman VF, O’Brien EK, Richards GS, Degnan BM (2003) Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina. Evol Dev 5:508–521
Hirth F, Hartmann B, Reichert H (1998) Homeotic gene action in embryonic brain development of Drosophila. Development 125:1579–1589
Hughes CL, Kaufman TC (2002) Hox genes and the evolution of the arthropod body plan. Evol Dev 4:459–499
Ikuta T, Yoshida N, Satoh N, Saiga H (2004) Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development. Proc Natl Acad Sci U S A 101:15118–15123
Irvine SQ, Martindale MQ (2000) Expression patterns of anterior Hox genes in the polychaete Chaetopterus: correlation with morphological boundaries. Dev Biol 217:333–351
John CC (1933) Habits, structure, and development of Spadella cephaloptera. Q J Microsc Sci 75:625–696
Keynes R, Krumlauf R (1994) Hox genes and regionalization of the nervous system. Annu Rev Neurosci 17:109–132
Kourakis MJ, Master VA, Lokhorst DK, Nardelli-Haefliger D, Wedeen CJ, Martindale MQ, Shankland M (1997) Conserved anterior boundaries of Hox gene expression in the central nervous system of the leech Helobdella. Dev Biol 190:284–300
Lawrence PA, Morata G (1994) Homeobox genes: their function in Drosophila segmentation and pattern formation. Cell 78:181–189
Lee PN, Callaerts P, De Couet HG, Martindale MQ (2003) Cephalopod Hox genes and the origin of morphological novelties. Nature 424:1061–1065
Littlewood DTJ, Telford MJ, Clough KA, Rohde K (1998) Gnathostomulida—an enigmatic metazoan phylum from both morphological and molecular perspective. Mol Phyl Evol 9:72–79
Mallatt J, Winchell CJ (2002) Testing the new animal phylogeny: first use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Mol Biol Evol 19:289–301
McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302
Nardelli-Haefliger D, Shankland M (1992) Lox2, a putative leech segment identity gene, is expressed in the same segmental domain in different stem cell lineages. Development 116:697–710
Nielsen C (2001) Animal evolution: relationships between invertebrate phyla, 2nd edn. Oxford University Press, Oxford
Papillon D, Perez Y, Fasano L, Le Parco Y, Caubit X (2003) Hox gene survey in the chaetognath Spadella cephaloptera: evolutionary implications. Dev Genes Evol 213:142–148
Papillon D, Perez Y, Caubit X, Le Parco Y (2004) Identification of chaetognaths as protostomes is supported by the analysis of their mitochondrial genome. Mol Biol Evol 21:2122–2129
Peterson KJ, Eernisse DJ (2001) Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18s rDNA gene sequences. Evol Dev 3:170–205
Rehkämper G, Welsch U (1985) On the fine structure of the cerebral ganglion of Sagitta (Chaetognatha). Zoomorphology 105:83–89
Seo HC, Edvardsen RB, Maeland AD, Bjordal M, Jensen MF, Hansen A, Flaat M, Weissenbach J, Lehrach H, Wincker P, Reinhardt R, Chourrout D (2004) Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431:67–71
Shimotori T, Goto T (2001) Developmental fates of the first four blastomeres of the chaetognath Paraspadella gotoi: relationship to protostomes. Dev Growth Differ 43:371–382
Takada N, Goto T, Satoh N (2002) Expression pattern of the Brachyury gene in the arrow worm Paraspadella gotoi (Chaetognatha). Genesis 32:240–245
Telford MJ, Holland PWH (1993) The phylogenetic affinities of the chaetognaths: a molecular analyses. Mol Biol Evol 10:660–676
Wada H, Garcia-Fernandez J, Holland PW (1999) Colinear and segmental expression of amphioxus Hox genes. Dev Biol 213:131–141
Wadah H, Satoh N (1994) Details of the evolutionary history from invertebrates to vertebrates; as deduced from the sequences of 18s rDNA. Proc Natl Acad Sci U S A 91:1801–1804
Zrzàvy J, Mihulka S, Kepka P, Bezdik A, Tietz D (1998) Phylogeny of the metazoa based on morphological and 18s ribosomal DNA evidence. Cladistics 14:249–285
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We wish to thank Kerridge S. and anonymous reviewers for helpful corrections.
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Papillon, D., Perez, Y., Fasano, L. et al. Restricted expression of a median Hox gene in the central nervous system of chaetognaths. Dev Genes Evol 215, 369–373 (2005). https://doi.org/10.1007/s00427-005-0483-z
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DOI: https://doi.org/10.1007/s00427-005-0483-z