Abstract
We have studied the process of post-embryonic segmentation in the anostracan crustacean Artemia franciscana using a specific antibody raised against the engrailed protein of this organism. Three cephalic segments are specified during embryonic development, before larval hatching, whilst trunk (thoracic) segmentation begins after the first stage free-swimming nauplius larva has emerged from the dormant cyst. Thus, cephalic and trunk segmentation seem to be at least in part independent and superimposed processes. Trunk stripes of engrailed expression are added one at a time as segments are generated from the posterior growth zone. The first detectable decision in engrailed expression is the establishment of a line of engrailed-expressing cells, interpretable as delineating the parasegmental boundary. The subsequent widening of engrailed stripes is not correlated with cell lineage events but is probably mediated by the combination of inheritance of the active state and recruitment of new cells into the engrailed-expressing stripe.
Similar content being viewed by others
References
Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101:1–22
Akam M, Dawes R (1992) More than one way to splice an egg. Curr Biol 2:395–398
Anderson DT (1967) Larval development and segment formation in the branchiopod crustaceans Limnadia stanleyana King (Conchostraca) and Artemia salina (L.) (Anostraca). Aust J Zool 15:47–91
Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon Press, Oxford
Basler K, Struhl G (1994) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368:208–214
Benesch R (1969) Zur Ontogenie und Morphologie von Artemia salina L. Zool Jahrb Abt Anat Ontog Tiere 86:307–458
Bressan GM, Stanley KK (1987) pUEX, a bacterial expression vector related to pEX with universal host specificity. Nucl Acids Res 15:10056
Campbell GL, Caveney S (1989) engrailed gene expression in the abdominal segment of Oncopeltus: gradients and cell states in the insect segment. Development 106:727–737
Cohen S, Jürgens G (1991) Drosophila headlines. Trends Genet 7:267–271
Dawes R, Dawson I, Falciani F, Tear G, Akam M (1994) Dax, a locust Hox gene related to fushi-tarazu but showing no pairrule expression. Development 120:1561–1572
DiNardo S, O'Farrell PH (1987) Establishment and refinement of segmental pattern in the Drosophila embryo: spatial control of engrailed expression by pair-rule genes. Genes Dev 1:1212–1225
DiNardo S, Kuner JM, Theis J, O'Farrell PH (1985) Development of embryonic pattern in Drosophila melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell 43:59–69
Dohle W, Scholtz G (1988) Clonal analysis of the crustacean segment: the discordance between genealogical and segmental borders. Development 104 (Suppl):147–160
Fleig R (1990) Engrailed expression and body segmentation in the honeybee Apis mellifera. Roux's Arch Dev Biol 198:467–473
Fleig R (1994) Head segmentation in the embryo of the Colorado beetle Leptinotarsa decemlineata as seen with anti-en immunostaining. Roux's Arch Dev Biol 203:227–229
Freeman JA (1986) Epidermal cell proliferation during thoracic development in larvae of Artemia. J Crust Biol 6:37–48
Freeman JA (1989) Segment morphogenesis in Artemia larvae. In: ] Warner AH, Macrae TH, Bagshaw JC (eds) Cell and molecular biology of Artemia development. Plenum Press, New York, pp 77–90
Hertzler PL, Clark WH Jr (1992) Cleavage and gastrulation in the shrimp Sicyonia ingentis: invagination is accompanied by oriented cell division. Development 116:127–140
Ingham PW, Martinez-Arias A, Lawrence PA, Howard K (1985) Expression of engrailed in the parasegment of Drosophila. Nature 317:634–636
Karr TL, Weir MD, Ali Z, Kornberg T (1989) Patterns of engrailed protein in early Drosophila embryos. Development 105:605–612
Klinger M (1994) Segmentation in insects: how singular is Drosophila? Bio Essays 16:391–392
Kraft R, Jäckle H (1994) Drosophila mode of metamerization in the embryogenesis of the lepidopteran insect Manduca sexta. Proc Nat Acad Sci USA 91:6634–6638
Manzanares M, Marco R, Garesse R (1993) Genomic organization and developmental pattern of expression of the engrailed gene from the brine shrimp Artemia. Development 118:1209–1219
Martinez-Arias A, Lawrence PA (1985) Parasegments and compartments in the Drosophila embryo. Nature 313:639–642
Mitchison TJ, Sedat J (1983) Localization of antigenic determinants in whole Drosophila embryos. Dev Biol 99:261–264
Morata G, Lawrence PA (1975) Control of compartment development by the engrailed gene in Drosophila. Nature 255:614–617
Nagy LM (1994) A glance posterior. Curr Biol 4:811–814
Nagy LM, Carroll S (1994) Conservation of wingless patterning functions in short-germ embryos of Tribolium castaneum. Nature 367:460–464
Olson CS, Clegg JS (1978) Cell division during the development of Artemia salina. Roux's Arch Dev Biol 184:1–13
Patel NH (1994) Developmental evolution: insights from studies of insect segmentation. Science 266:581–590
Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB, Goodman CS (1989a) Expression of engrailed proteins in arthropods, annelids and chordates. Cell 58:955–968
Patel NH, Kornberg TB, Goodman CS (1989b) Expression of engrailed during segmentation in grasshopper and crayfish. Development 107:201–212
Patel NH, Ball EE, Goodman CS (1992) Changing role of even-skipped during the evolution of insect pattern formation. Nature 357:339–342
Patel NH, Condron BG, Zinn K (1994) Pair-rule expression of even-skipped is found in both short- and long-germ beetles. Nature 367:429–434
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Press, New York
Sander K (1976) Specification of the basic body pattern in insect embryogenesis. Adv Insect Physiol 12:125–238
Scholtz G (1992) Cell lineage studies in the crayfish Cherax destructor (Crustacea, Decapoda): germ band formation, segmentation, and early neurogenesis. Roux's Arch Dev Biol 202:36–48
Scholtz G (1995) Head segmentation in Crustacea- and immunoytochemical study. J Zool 98:36–48
Scholtz G, Dohle W, Sandeman RE, Richter S (1993) Expression of engrailed can be lost and regained in cells of one clone in crustacean embryos. Int J Dev Biol 37:299–304
Scholtz G, Patel NH, Dohle W (1994) Serially homologous engrailed stripes are generated via different cell lineages in the germ band of amphipod crustaceans (Malacostraca, Peracarida). Int J Dev Biol 38:471–478
Schram FR (1986) Crustacea. Oxford University Press, Oxford New York
Schrehardt A (1987) A scanning electron-microscope study of the post-embryonic development of Artemia. In: Sorgeloos P, Bengston DA, Dedeir W, Jaspers E (eds). Artemia research and its applications, vol 1. Universa Press, Wetteren, pp 532
Sommer RJ, Tautz D (1993) Involvement of an orthologue of the Drosophila pair-rule gene hairy in segment formation of the short germ-band embryo of Tribolium (Coleoptera). Nature 361:448–450
Stern CD (1990) Two distinct mechanisms for segmentation? Sem Dev Biol 1:109–116
Thomas JB, Bastiani MJ, Bate M, Goodman CS (1984) From grasshopper to Drosophila: a common plan for neuronal development. Nature 310:203–207
Turquin MJ (1969) Le développement du systeme nerveux de Niphargus virei (Crustacée, Amphipode, Hypogé) Bull Soc Zool France 94:649–656
Tyson GE, Sullivan ML (1980) Scanning electron microscopy of cuticular sensilla of Artemia; setae of the adult trunk segments. In: Persoone G, Sorgeloos P, Roels O, Jaspers E (eds). The Brine shrimp Artemia, vol 1. Universa Press, Wetteren, pp 99–106
Vincent JP, O'Farrell PH (1992) The state of engrailed expression is not clonally transmitted during early Drosophila development. Cell 68:923–931
Weygoldt P (1958) Die Embryonalentwicklung des Amphipoden Gammarus pulex pulex (L.) Zool Jahrb Abt Anat Ontog Tiere 77:51–110
Williams JA, Paddock SW, Vorwerk K, Carroll SB (1994) Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary. Nature 368:299–305
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Manzanares, M., Williams, T.A., Marco, R. et al. Segmentation in the crustacean Artemia: engrailed staining studied with an antibody raised against the Artemia protein. Roux's Arch Dev Biol 205, 424–431 (1996). https://doi.org/10.1007/BF00377222
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00377222