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Pleiotropic developmental expression of HasPOU-III, a class III POU gene, in the gastropod Haliotis asinina
Mechanisms of Development 114 (2002) 129–132 www.elsevier.com/locate/modo
Gene expression pattern
Pleiotropic developmental expression of HasPOU-III, a class III POU gene, in the gastropod Haliotis asinina Elizabeth K. O’Brien, Bernard M. Degnan* Department of Zoology and Entomology, University of Queensland, Brisbane, Queensland 4072, Australia Received 2 November 2001; received in revised form 14 December 2001; accepted 30 January 2002
Abstract HasPOU-III is expressed in multiple cell types during the first 3 days of development of the gastropod Haliotis asinina. HasPOU-III expression begins in two bilaterally symmetrical sets of cells on the ventral ectodermal surface of the trochophore larva; one set are putative foot mucous cells. After torsion, HasPOU-III transcripts transiently appear in the developing ganglia of the central nervous system. At the end of larval morphogenesis, HasPOU-III expression is initiated in dorsoposterior cells of the visceral mass, in the posterior cells of the statocyst and in the developing radular sac. These expression patterns in Haliotis, a spiralian lophotrochozoan, are similar to POU Class III genes in other bilaterians where expression occurs in secretory cells and the developing nervous system. q 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Central nervous system; Spiralian; Trochophore; Veliger; Lophotrochozoa; Mollusc; Secretory; Transcription factor; Larva; Marine invertebrate; Abalone; Gastropod; POU; Bilateria
1. Results and discussion POU genes encode transcription factors that are characterised by the presence of highly conserved POU and homeodomains (Herr et al., 1988). Expression in the nervous systems of vertebrates, Drosophila and Caenorhabditis elegans suggests POU genes play a central role in nerve cell differentiation and function (Veenstra et al., 1997). POU is also expressed in a range secretory cells in these organisms and other ecdysozoans and deuterostomes (Bu¨rglin and Ruvkun, 2001). Herein we describe the expression pattern of a member of the class III POU genes in the gastropod Haliotis asinina. Haliotis develops in manner similar to other spiralian lophotrochozoans (van den Biggelaar and Haszprunar, 1996; van den Biggelaar et al., 1997), which includes spiral cleavage, mesentoblast formation and a trochophore-like larval stage. Later in the development of Haliotis and other gastropods, the taxon-specific veliger larva forms which is an amalgamation of adult and larval structures (Giusti et al., 2000). Reverse transcription-polymerase chain reaction (RTPCR) analysis of HasPOU-III transcript prevalence indicates that this gene is first expressed at the newly hatched trochophore larval stage (Fig. 1). HasPOU-III transcripts * Corresponding author. Tel.: 161-7-3365-2467; fax: 161-7-3365-1655. E-mail address: [email protected] (B.M. Degnan).
are detected throughout larval development (Fig. 1) and in a range of adult tissues (O’Brien and Degnan, 2000). HasPOU-III transcripts are first detected in two bilaterally symmetrical sets of cells in the ventral ectoderm of the trochophore, 8 h post-fertilisation (hpf): two large cells in the centroposterior region of the presumptive foot field and two smaller cells are located in more lateroanterior positions within the field (Fig. 2A–D). The central cells correspond to the presumptive mucous cells of the foot. HasPOU-III transcripts remain localised to these cells during and after ontogenetic torsion (,16–20 hpf), where the cephalopedal (head–foot) region twists 1808 relative to the visceropallial (digestive gland–mantle) region (Figs. 2E–G and 3A,B). The mucous cells eventually localise to the dorsoposterior epidermis of the foot in the vicinity of the posterior of the operculum (Fig. 3A). Prior to torsion, HasPOU-III is expressed transiently in two additional cells in the foot field, posterior to the stomodaeum and prototroch (Fig. 2E,F). After torsion, HasPOU-III transcripts are detected in the developing adult central nervous system (CNS), specifically in pleuropedal, cerebral and oesophageal ganglia (Fig. 3A,B). After 4 h, expression is also detected in the branchial ganglion (Fig. 3B). During these early post-torsional stages, HasPOU-III expression is maintained in the presumptive foot mucous cells.
0925-4773/02/$ - see front matter q 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0925-477 3(02)00037-0
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E.K. O’Brien, B.M. Degnan / Mechanisms of Development 114 (2002) 129–132
0.2 mm filtered sea water with 8 mg/ml rifampicin (Sigma). Total RNAs were isolated from embryonic and larval stages, and RT-PCR amplified using gene-specific primers designed to amplify either 660 bp of a portion of the open reading frame (ORF) and the 3 0 -UTR of HasPOU-III
Fig. 1. RT-PCR analysis of the developmental expression of HasPOU-III and HasSox-B in Haliotis asinina. HasSox-B transcripts are present in all developmental stages while HasPOU-III expression is restricted to larval stages. PCR amplification of equivalent amounts of RNA not reverse transcribed into cDNA did not produce detectable bands in any stage (not shown). hpf, hours post-fertilisation.
Additional localised expression occurs in older Haliotis veliger larvae. In the later veliger, HasPOU-III expression is restricted to an entirely new set of cell types (Fig. 3C–G). Transcripts are localised in cells located in the dorsoposterior region of the visceral mass (Fig. 3C–G). This region of the visceral mass forms the caudal part of the juvenile intestine where chymotrypsin gene expression occurs (Degnan et al., 1995). Expression also occurs in the periodic acid schiff (PAS) reactive cells (Fig. 3D) of the statocysts (Fig. 3C,E– G) and in the presumptive developing radular sac (Fig. 3C,G), which is the site of radular tooth formation. This study is the first analysis of developmental expression of a POU gene in a representative lophotrochozoan. The ten distinct patterns of HasPOU-III expression that occurred in Haliotis over the first 3 days of development are predominantly in the CNS and a variety of secretory cell types. Comparison with POU-III expression patterns in ecdysozoans (e.g. insects and nematodes) and deuterostomes (e.g. vertebrates) (Treacy and Rosenfeld, 1992), suggests that this class of POU genes plays a conserved role in the development of bilaterian nervous system. In addition, POU-III genes appear to be expressed in a range of bilaterian secretory and excretory cells, including the silk gland and other secretory tissues in the insect Bombyx mori (Kokubo et al., 1997), the larval salt gland of the crustacean Artemia franciscana (Chavez et al., 1999), and the excretory systems of C. elegans and vertebrates (e.g. Mathis et al., 1992; Spaniol et al., 1996; Bu¨ rglin and Ruvkun, 2001). In addition to ganglionic expression, HasPOU-III is expressed developmentally in the foot mucous cells (Fretter and Graham, 1962), in the secretory region of the statocysts and in the vicinity of the radula-secreting sac.
2. Materials and methods 2.1. RT-PCR Gametes of H. asinina were collected from natural spawning events (Counihan et al., 2001) and artificially fertilised. Embryos and larvae were maintained at 258C in
Fig. 2. Expression of HasPOU-III during early larval development of H. asinina. All panels whole mount stained larvae presented with anterior to the top. Blue numbers designate different HasPOU-III expression patterns. (A–D) 8 h post-fertilisation (hpf) trochophore. (A, B) Ventral view; (A) staining allowed to develop longer than (B). (C, D) Lateral view, ventral right; (C) staining allowed to develop longer than (D). HasPOU-III expression restricted to two mucous gland cells (#1) and two putative sensory cells (#2) in the foot field. (E, F) 16 hpf pre-torsional veliger. (E), lateral view, ventral right; (F) ventroanterior view. New localised expression in two cells in the anterior of the foot field (#3). (G) 18 hpf veliger undergoing torsion, side view. f, foot field; m, mantle; o, operculum; p, prototroch; st, stomodaeum; vm, visceral mass. Scale bar, 50 mm.
E.K. O’Brien, B.M. Degnan / Mechanisms of Development 114 (2002) 129–132
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(GenBank accession no. AF231942; nt 438–1098; primer sequences: 5 0 -GCTAATGATGTGTGGTGAAGACGGC; 5 0 -CGGCAAGAGTTAAAGCACGAG) or part of the ORF of the HasSox-B gene as described in O’Brien and Degnan (2000). Equivalent amounts of staged RNA, that were not reverse transcribed into cDNA, acted as control templates to account for DNA contamination. 2.2. Whole mount in situ hybridisation A digoxygenin (DIG)-labelled RNA probe was transcribed from a linearised pBKS 1 plasmid containing a 660 bp insert of a portion of the ORF and the 3 0 -UTR of HasPOU-III (as described above). Whole mount in situ hybridisation (WMISH) was performed on fixed H. asinina larvae using this probe as described in Giusti et al. (2000). 2.3. PAS staining The PAS method (Culling, 1975) was used to identify structures rich in mucopolysaccharides or glycoproteins. Larvae were fixed as per WMISH and PAS staining was observed in whole mount larvae. Acknowledgements We thank the staff at Heron Island Research Station for valued assistance with broodstock collection. This research was supported by grants to B.M.D. from the Australian Research Council. References
Fig. 3. Expression of HasPOU-III during later larval (post-torsional) development. All panels whole mount stained larvae presented with anterior to the right. Blue numbers designate different HasPOU-III expression patterns, continued from Fig. 2. (A) 21 hpf veliger, lateral view, dorsal top. four concurrent expression patterns: mucous gland cells (#1), and pleuropedal (#4), cerebral (#5) and oesophageal (#6) ganglia. (B) 26 hpf veliger, lateral view, dorsal top with new HasPOU-III expression in the branchial ganglion (#7). (C–G) 66 hpf veliger. (C, D) Lateral view, dorsal top; (E) ventral view, plane of focus through the centre of the larva; (F) anterior view; (G) dorsal view. At this stage HasPOU-III expression detected in three new cell types (#8–10). Earlier expression patterns (#1– 7) are no longer detected. Expression is in bilaterally symmetrical set of cells located on the posterior edge of the statocyst (#8). This staining apparently overlaps with PAS staining in the posterior cells of the statocyst (D). (D) is enlarged 1.5 £ with respect to the other micrographs. Expression also is in 3–4 cells located at the right side of dorsoposterior edge of the visceral mass (#9). HasPOU-III transcripts also detected at this stage in cells in the vicinity of the radula sac (#10) which pushes against the ventral side of the mantle cavity. e, eye; f, foot; m, mantle; mo, mouth; o, operculum; pc, pallial cavity; s, statocyst; v, velum; vm, visceral mass. Scale bar 50 mm.
van den Biggelaar, J.A.M., Haszprunar, G., 1996. Cleavage patterns and mesentoblast formation in the gastropoda: an evolutionary perspective. Evolution 50, 1520–1540. van den Biggelaar, J.A.M., Dictus, W.J.A.G., van Loon, A.E., 1997. Cleavage patterns, cell-lineages and cell specification are clues to phyletic lineages in Spiralia. Sem. Cell Dev. Biol. 18, 367–378. Bu¨ rglin, T.R., Ruvkun, G., 2001. Regulation of ectodermal and excretory function by the C. elegans POU homeobox gene ceh-6. Development 128, 779–790. Chavez, M., Landry, C., Loret, S., Muller, M., Figueroa, J., Peers, B., Rentier-Delrue, F., Rousseau, G.G., Krauskopf, M., Martial, J.A., 1999. APH-1, a POU homeobox gene expressed in the salt gland of the crustacean Artemia franciscana. Mech. Dev. 87, 207–212. Counihan, R.T., McNamara, D.C., Souter, D.C., Jebreen, E.J., Preston, N.P., Johnson, C.R., Degnan, B.M., 2001. Pattern, synchrony and predictability of spawning of the tropical abalone, Haliotis asinina, from Heron Reef, Australia. Mar. Ecol. Prog. Ser. 213, 193–202. Culling, C.F.A., 1975. Handbook of Histopathological and Histochemical Techniques, 3rd ed., Butterworths, London pp. 267–268. Degnan, B.M., Groppe, J.C., Morse, D.E., 1995. Chymotrypsin mRNA expression in digestive gland amoebocytes: cell specification occurs prior to metamorphosis and gut morphogenesis in the gastropod, Haliotis rufescens. Roux’s Arch. Dev. Biol. 205, 97–101. Fretter, V., Graham, A., 1962. British Prosobranch Molluscs. Their Functional Anatomy and Ecology, Ray Society, London. Giusti, A.F., Hinman, V.F., Degnan, S.M., Degnan, B.M., Morse, D.E., 2000. Expression of a Scr/Hox5 gene in the larval central nervous
132
E.K. O’Brien, B.M. Degnan / Mechanisms of Development 114 (2002) 129–132
system of the gastropod Haliotis, a non-segmented spiralian lophotrocozoan. Evol. Dev. 2, 294–302. Herr, W., Sturm, R.A., Clerc, R.G., Corcoran, L.M., Baltimore, D., Sharp, P.A., Ingraham, H.A., Rosenfeld, M.G., Finney, M., Ruvkun, G., Horvitz, H.R., 1988. The POU domain: a large conserved region in the mammalian pit-1, oct-1, oct-2 and Caenorhabditis elegans unc-86 gene products. Genes Dev. 2, 1513–1516. Kokubo, H., Xu, P-X., Xu, X., Matsunami, K., Suzuki, Y., 1997. Spatial and temporal expression pattern of POU-M1/SGF-3 in Bombyx mori embryogenesis. Dev. Genes Evol. 206, 494–502. Mathis, J.M., Simmons, D.M., He, X., Swanson, L.W., Rosenfeld, M.G., 1992. Brain 4: a novel mammalian POU domain transcription factor exhibiting restricted brain-specific expression. EMBO J. 11, 2551– 2561.
O’Brien, E.K., Degnan, B.M., 2000. Expression of POU, Sox and Pax genes in the brain of the tropical abalone, Haliotis asinina. Mar. Biotech. 2, 545–557. Spaniol, P., Bornmann, C., Hauptmann, G., Gerster, T., 1996. Class III POU genes of zebrafish are predominantly expressed in the central nervous system. Nucleic Acids Res. 24, 4874–4881. Treacy, M.N., Rosenfeld, M.G., 1992. Expression of a family of POUdomain protein regulatory genes during development of the central nervous system. Annu. Rev. Neurosci. 15, 139–165. Veenstra, G.J.C., Van Der Vliet, P.C., Destree, O.H.J., 1997. POU domain transcription factors in embryonic development. Mol. Biol. Rep. 24, 139–155.
Gene expression pattern
Pleiotropic developmental expression of HasPOU-III, a class III POU gene, in the gastropod Haliotis asinina Elizabeth K. O’Brien, Bernard M. Degnan* Department of Zoology and Entomology, University of Queensland, Brisbane, Queensland 4072, Australia Received 2 November 2001; received in revised form 14 December 2001; accepted 30 January 2002
Abstract HasPOU-III is expressed in multiple cell types during the first 3 days of development of the gastropod Haliotis asinina. HasPOU-III expression begins in two bilaterally symmetrical sets of cells on the ventral ectodermal surface of the trochophore larva; one set are putative foot mucous cells. After torsion, HasPOU-III transcripts transiently appear in the developing ganglia of the central nervous system. At the end of larval morphogenesis, HasPOU-III expression is initiated in dorsoposterior cells of the visceral mass, in the posterior cells of the statocyst and in the developing radular sac. These expression patterns in Haliotis, a spiralian lophotrochozoan, are similar to POU Class III genes in other bilaterians where expression occurs in secretory cells and the developing nervous system. q 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Central nervous system; Spiralian; Trochophore; Veliger; Lophotrochozoa; Mollusc; Secretory; Transcription factor; Larva; Marine invertebrate; Abalone; Gastropod; POU; Bilateria
1. Results and discussion POU genes encode transcription factors that are characterised by the presence of highly conserved POU and homeodomains (Herr et al., 1988). Expression in the nervous systems of vertebrates, Drosophila and Caenorhabditis elegans suggests POU genes play a central role in nerve cell differentiation and function (Veenstra et al., 1997). POU is also expressed in a range secretory cells in these organisms and other ecdysozoans and deuterostomes (Bu¨rglin and Ruvkun, 2001). Herein we describe the expression pattern of a member of the class III POU genes in the gastropod Haliotis asinina. Haliotis develops in manner similar to other spiralian lophotrochozoans (van den Biggelaar and Haszprunar, 1996; van den Biggelaar et al., 1997), which includes spiral cleavage, mesentoblast formation and a trochophore-like larval stage. Later in the development of Haliotis and other gastropods, the taxon-specific veliger larva forms which is an amalgamation of adult and larval structures (Giusti et al., 2000). Reverse transcription-polymerase chain reaction (RTPCR) analysis of HasPOU-III transcript prevalence indicates that this gene is first expressed at the newly hatched trochophore larval stage (Fig. 1). HasPOU-III transcripts * Corresponding author. Tel.: 161-7-3365-2467; fax: 161-7-3365-1655. E-mail address: [email protected] (B.M. Degnan).
are detected throughout larval development (Fig. 1) and in a range of adult tissues (O’Brien and Degnan, 2000). HasPOU-III transcripts are first detected in two bilaterally symmetrical sets of cells in the ventral ectoderm of the trochophore, 8 h post-fertilisation (hpf): two large cells in the centroposterior region of the presumptive foot field and two smaller cells are located in more lateroanterior positions within the field (Fig. 2A–D). The central cells correspond to the presumptive mucous cells of the foot. HasPOU-III transcripts remain localised to these cells during and after ontogenetic torsion (,16–20 hpf), where the cephalopedal (head–foot) region twists 1808 relative to the visceropallial (digestive gland–mantle) region (Figs. 2E–G and 3A,B). The mucous cells eventually localise to the dorsoposterior epidermis of the foot in the vicinity of the posterior of the operculum (Fig. 3A). Prior to torsion, HasPOU-III is expressed transiently in two additional cells in the foot field, posterior to the stomodaeum and prototroch (Fig. 2E,F). After torsion, HasPOU-III transcripts are detected in the developing adult central nervous system (CNS), specifically in pleuropedal, cerebral and oesophageal ganglia (Fig. 3A,B). After 4 h, expression is also detected in the branchial ganglion (Fig. 3B). During these early post-torsional stages, HasPOU-III expression is maintained in the presumptive foot mucous cells.
0925-4773/02/$ - see front matter q 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0925-477 3(02)00037-0
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E.K. O’Brien, B.M. Degnan / Mechanisms of Development 114 (2002) 129–132
0.2 mm filtered sea water with 8 mg/ml rifampicin (Sigma). Total RNAs were isolated from embryonic and larval stages, and RT-PCR amplified using gene-specific primers designed to amplify either 660 bp of a portion of the open reading frame (ORF) and the 3 0 -UTR of HasPOU-III
Fig. 1. RT-PCR analysis of the developmental expression of HasPOU-III and HasSox-B in Haliotis asinina. HasSox-B transcripts are present in all developmental stages while HasPOU-III expression is restricted to larval stages. PCR amplification of equivalent amounts of RNA not reverse transcribed into cDNA did not produce detectable bands in any stage (not shown). hpf, hours post-fertilisation.
Additional localised expression occurs in older Haliotis veliger larvae. In the later veliger, HasPOU-III expression is restricted to an entirely new set of cell types (Fig. 3C–G). Transcripts are localised in cells located in the dorsoposterior region of the visceral mass (Fig. 3C–G). This region of the visceral mass forms the caudal part of the juvenile intestine where chymotrypsin gene expression occurs (Degnan et al., 1995). Expression also occurs in the periodic acid schiff (PAS) reactive cells (Fig. 3D) of the statocysts (Fig. 3C,E– G) and in the presumptive developing radular sac (Fig. 3C,G), which is the site of radular tooth formation. This study is the first analysis of developmental expression of a POU gene in a representative lophotrochozoan. The ten distinct patterns of HasPOU-III expression that occurred in Haliotis over the first 3 days of development are predominantly in the CNS and a variety of secretory cell types. Comparison with POU-III expression patterns in ecdysozoans (e.g. insects and nematodes) and deuterostomes (e.g. vertebrates) (Treacy and Rosenfeld, 1992), suggests that this class of POU genes plays a conserved role in the development of bilaterian nervous system. In addition, POU-III genes appear to be expressed in a range of bilaterian secretory and excretory cells, including the silk gland and other secretory tissues in the insect Bombyx mori (Kokubo et al., 1997), the larval salt gland of the crustacean Artemia franciscana (Chavez et al., 1999), and the excretory systems of C. elegans and vertebrates (e.g. Mathis et al., 1992; Spaniol et al., 1996; Bu¨ rglin and Ruvkun, 2001). In addition to ganglionic expression, HasPOU-III is expressed developmentally in the foot mucous cells (Fretter and Graham, 1962), in the secretory region of the statocysts and in the vicinity of the radula-secreting sac.
2. Materials and methods 2.1. RT-PCR Gametes of H. asinina were collected from natural spawning events (Counihan et al., 2001) and artificially fertilised. Embryos and larvae were maintained at 258C in
Fig. 2. Expression of HasPOU-III during early larval development of H. asinina. All panels whole mount stained larvae presented with anterior to the top. Blue numbers designate different HasPOU-III expression patterns. (A–D) 8 h post-fertilisation (hpf) trochophore. (A, B) Ventral view; (A) staining allowed to develop longer than (B). (C, D) Lateral view, ventral right; (C) staining allowed to develop longer than (D). HasPOU-III expression restricted to two mucous gland cells (#1) and two putative sensory cells (#2) in the foot field. (E, F) 16 hpf pre-torsional veliger. (E), lateral view, ventral right; (F) ventroanterior view. New localised expression in two cells in the anterior of the foot field (#3). (G) 18 hpf veliger undergoing torsion, side view. f, foot field; m, mantle; o, operculum; p, prototroch; st, stomodaeum; vm, visceral mass. Scale bar, 50 mm.
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(GenBank accession no. AF231942; nt 438–1098; primer sequences: 5 0 -GCTAATGATGTGTGGTGAAGACGGC; 5 0 -CGGCAAGAGTTAAAGCACGAG) or part of the ORF of the HasSox-B gene as described in O’Brien and Degnan (2000). Equivalent amounts of staged RNA, that were not reverse transcribed into cDNA, acted as control templates to account for DNA contamination. 2.2. Whole mount in situ hybridisation A digoxygenin (DIG)-labelled RNA probe was transcribed from a linearised pBKS 1 plasmid containing a 660 bp insert of a portion of the ORF and the 3 0 -UTR of HasPOU-III (as described above). Whole mount in situ hybridisation (WMISH) was performed on fixed H. asinina larvae using this probe as described in Giusti et al. (2000). 2.3. PAS staining The PAS method (Culling, 1975) was used to identify structures rich in mucopolysaccharides or glycoproteins. Larvae were fixed as per WMISH and PAS staining was observed in whole mount larvae. Acknowledgements We thank the staff at Heron Island Research Station for valued assistance with broodstock collection. This research was supported by grants to B.M.D. from the Australian Research Council. References
Fig. 3. Expression of HasPOU-III during later larval (post-torsional) development. All panels whole mount stained larvae presented with anterior to the right. Blue numbers designate different HasPOU-III expression patterns, continued from Fig. 2. (A) 21 hpf veliger, lateral view, dorsal top. four concurrent expression patterns: mucous gland cells (#1), and pleuropedal (#4), cerebral (#5) and oesophageal (#6) ganglia. (B) 26 hpf veliger, lateral view, dorsal top with new HasPOU-III expression in the branchial ganglion (#7). (C–G) 66 hpf veliger. (C, D) Lateral view, dorsal top; (E) ventral view, plane of focus through the centre of the larva; (F) anterior view; (G) dorsal view. At this stage HasPOU-III expression detected in three new cell types (#8–10). Earlier expression patterns (#1– 7) are no longer detected. Expression is in bilaterally symmetrical set of cells located on the posterior edge of the statocyst (#8). This staining apparently overlaps with PAS staining in the posterior cells of the statocyst (D). (D) is enlarged 1.5 £ with respect to the other micrographs. Expression also is in 3–4 cells located at the right side of dorsoposterior edge of the visceral mass (#9). HasPOU-III transcripts also detected at this stage in cells in the vicinity of the radula sac (#10) which pushes against the ventral side of the mantle cavity. e, eye; f, foot; m, mantle; mo, mouth; o, operculum; pc, pallial cavity; s, statocyst; v, velum; vm, visceral mass. Scale bar 50 mm.
van den Biggelaar, J.A.M., Haszprunar, G., 1996. Cleavage patterns and mesentoblast formation in the gastropoda: an evolutionary perspective. Evolution 50, 1520–1540. van den Biggelaar, J.A.M., Dictus, W.J.A.G., van Loon, A.E., 1997. Cleavage patterns, cell-lineages and cell specification are clues to phyletic lineages in Spiralia. Sem. Cell Dev. Biol. 18, 367–378. Bu¨ rglin, T.R., Ruvkun, G., 2001. Regulation of ectodermal and excretory function by the C. elegans POU homeobox gene ceh-6. Development 128, 779–790. Chavez, M., Landry, C., Loret, S., Muller, M., Figueroa, J., Peers, B., Rentier-Delrue, F., Rousseau, G.G., Krauskopf, M., Martial, J.A., 1999. APH-1, a POU homeobox gene expressed in the salt gland of the crustacean Artemia franciscana. Mech. Dev. 87, 207–212. Counihan, R.T., McNamara, D.C., Souter, D.C., Jebreen, E.J., Preston, N.P., Johnson, C.R., Degnan, B.M., 2001. Pattern, synchrony and predictability of spawning of the tropical abalone, Haliotis asinina, from Heron Reef, Australia. Mar. Ecol. Prog. Ser. 213, 193–202. Culling, C.F.A., 1975. Handbook of Histopathological and Histochemical Techniques, 3rd ed., Butterworths, London pp. 267–268. Degnan, B.M., Groppe, J.C., Morse, D.E., 1995. Chymotrypsin mRNA expression in digestive gland amoebocytes: cell specification occurs prior to metamorphosis and gut morphogenesis in the gastropod, Haliotis rufescens. Roux’s Arch. Dev. Biol. 205, 97–101. Fretter, V., Graham, A., 1962. British Prosobranch Molluscs. Their Functional Anatomy and Ecology, Ray Society, London. Giusti, A.F., Hinman, V.F., Degnan, S.M., Degnan, B.M., Morse, D.E., 2000. Expression of a Scr/Hox5 gene in the larval central nervous
132
E.K. O’Brien, B.M. Degnan / Mechanisms of Development 114 (2002) 129–132
system of the gastropod Haliotis, a non-segmented spiralian lophotrocozoan. Evol. Dev. 2, 294–302. Herr, W., Sturm, R.A., Clerc, R.G., Corcoran, L.M., Baltimore, D., Sharp, P.A., Ingraham, H.A., Rosenfeld, M.G., Finney, M., Ruvkun, G., Horvitz, H.R., 1988. The POU domain: a large conserved region in the mammalian pit-1, oct-1, oct-2 and Caenorhabditis elegans unc-86 gene products. Genes Dev. 2, 1513–1516. Kokubo, H., Xu, P-X., Xu, X., Matsunami, K., Suzuki, Y., 1997. Spatial and temporal expression pattern of POU-M1/SGF-3 in Bombyx mori embryogenesis. Dev. Genes Evol. 206, 494–502. Mathis, J.M., Simmons, D.M., He, X., Swanson, L.W., Rosenfeld, M.G., 1992. Brain 4: a novel mammalian POU domain transcription factor exhibiting restricted brain-specific expression. EMBO J. 11, 2551– 2561.
O’Brien, E.K., Degnan, B.M., 2000. Expression of POU, Sox and Pax genes in the brain of the tropical abalone, Haliotis asinina. Mar. Biotech. 2, 545–557. Spaniol, P., Bornmann, C., Hauptmann, G., Gerster, T., 1996. Class III POU genes of zebrafish are predominantly expressed in the central nervous system. Nucleic Acids Res. 24, 4874–4881. Treacy, M.N., Rosenfeld, M.G., 1992. Expression of a family of POUdomain protein regulatory genes during development of the central nervous system. Annu. Rev. Neurosci. 15, 139–165. Veenstra, G.J.C., Van Der Vliet, P.C., Destree, O.H.J., 1997. POU domain transcription factors in embryonic development. Mol. Biol. Rep. 24, 139–155.