Abstract
Two forkhead family transcription factors, HeFoxA1 and HeFoxA2, were isolated from the serpulid annelid Hydroides elegans and their transcript distribution were characterized during embryogenesis. HeFoxA1 is first detected in second quartet blastomeres soon after their formation, and later in all vegetal half blastomeres, which comprise ectoderm, endoderm, and mesoderm precursors. HeFoxA1 expression declines first in subtrochal ectoderm and presumptive midgut precursors, as well as apparently in D quadrant blastomeres in advance of any known signaling events. Later, during gastrulation, HeFoxA1 declines in hindgut precursors, and by the end of gastrulation the expression remains active only in foregut precursors. HeFoxA1 is apparently expressed in ectomesoderm cells involved in forming the larva-specific protonephridium (the so-called head kidney). The other ortholog, HeFoxA2, is expressed in a subset of the cells in which HeFoxA1 is expressed during early stages, but later it is largely restricted to the endoderm–ectoderm boundary of the proctodaeum. In addition, HeFoxA2 has a unique expression in two hindgut cells and abutting ectoderm cells located by the imminent anal opening. The combined expression of HeFoxA1 and HeFoxA2 correlates with mesoderm and endoderm expression of their orthologs in other bilaterians.
References
Anderson DT (1966) The comparative embryology of the Polychaeta. Acta Zool (Stockh) 47:1–42
Arenas-Mena C, Cameron AR, Davidson EH (2000) Spatial expression of hox cluster genes in the ontogeny of a sea urchin. Development 127:4631–4643
Arenas-Mena C, Cameron RA, Davidson EH (2006) Hindgut specification and cell-adhesion functions of Sphox11/13b in the endoderm of the sea urchin embryo. Dev Growth Differ 48(7):463–472
Boyer BC, Henry JQ (1998) Evolutionary modifications of the Spiralian developmental program. Am Zool 38:621–633
Finnerty JR, Pang K, Burton P, Paulson D, Martindale MQ (2004) Origins of bilateral symmetry: hox and dpp expression in a sea anemone. Science 304:1335–1337
Fritzenwanker JH, Saina M, Technau U (2004) Analysis of forkhead and snail expression reveals epithelial–mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev Biol 275:389–402
Gerrier P (1970) Les caractères de la segmentation et la détermination de la polarité dorsoventrale dans le développement de quelques Spiralia. J Embryol Exp Morph 23:611–637
Hatschek B (1885) Entwicklung der trochophora von Eupomatus uncinatus, Philippi (Serpula uncinata). Arbeiten aus dem Zoologischen Institut Wien 6:121
Kaestner KH, Knochel W, Martinez DE (2000) Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev 14:142–146
Kraus Y, Technau U (2006) Gastrulation in the sea anemone Nematostella vectensis occurs by invagination and immigration: an ultrastructural study. Dev Genes Evol 216:119–132
Kusch T, Reuter R (1999) Functions for Drosophila brachyenteron and forkhead in mesoderm specification and cell signalling. Development 126:3991–4003
Lambert JD, Nagy LM (2003) The MAPK cascade in equally cleaving spiralian embryos. Dev Biol 263:231–241
Lartillot N, Le Gouar M, Adoutte A (2002) Expression patterns of fork headand goosecoid homologues in the mollusc Patella vulgata supports the ancestry of the anterior mesendoderm across Bilateria. Dev Genes Evol 212:551–561
Luetjens CM, Dorresteijn AWC (1995) Multiple, alternative cleavage patterns precede uniform larval morphology during normal development of Dreissena polymorpha (Mollusca Lamellibranchia). Roux’s Archives of Developmental Biology 205:138–149
Luetjens C, Dorresteijn A (1998) The site of fertilisation determines dorsoventral polarity but not chirality in the zebra mussel embryo. Zygote 6:239–248
Martindale MQ, Doe CQ, Morrill JB (1985) The role of animal-vegetal interaction with respect to the determination of dorsoventral polarity in the equal-cleaving spiralian, Lymnaea palustris. Dev Genes Evol 194:281–295
Segrove F (1941) The development of the serpulid Pomatoceros triqueter L. Q J Microsc Sci 82:467–540
Shearer CMA (1911) On the development and structure of the trochophore of Hydroides (Eupomatus) uncinatus. Q J Microsc Sci 56:543–590
Shimeld SM (1997) Characterisation of amphioxus HNF-3 genes: conserved expression in the notochord and floor plate. Dev Biol 183:74–85
Taguchi S, Tagawa K, Humphreys T, Nishino A, Satoh N, Harada Y (2000) Characterization of a hemichordate fork head/HNF-3 gene expression. Dev Genes Evol 210:11–17
Treadwell AL (1901) The cytogeny of Podarke obscura. J Morphol 17:399–486
Wilson EB (1892) The cell lineage of Nereis. J Morphol 6:361–480
Wisely B (1958) The development and settling of a serpulid worm Hydroides norvegica Gunnerus (Polychaeta). Aust J Mar Freshw Res 9:351–361
Acknowledgements
I would like to thank Dr. Bruno Pernet for his thoughtful comments on the manuscript and Mr. Lee Davis for facilitating our access to his marina for worm collection.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by D.A. Weisblat
Rights and permissions
About this article
Cite this article
Arenas-Mena, C. Embryonic expression of HeFoxA1 and HeFoxA2 in an indirectly developing polychaete. Dev Genes Evol 216, 727–736 (2006). https://doi.org/10.1007/s00427-006-0099-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-006-0099-y