Summary
The effects ofpolyhomeotic (ph) mutants in imaginal cells have been studied in a clonal analysis. Clones of cells, homozygous forph, sort-out after a few divisions, probably as a consequence of modified cell affinities. The dorso-ventral margin of the wing has special characteristics that retard this phenomenon. The formation and exclusion of a clone of 8–16 cells affect the polarity of the wild-type neighbour cells and can provoke pattern triplications. The results suggest that a defect in intercellular communication prevents the wild-type cells from maintaining coordinated positional information. The cells react by regenerative growth, and reorganize into a new pattern. The pleiotropic phenotypes ofph mutants are explained according to a common hypothesis aboutph + function.
Similar content being viewed by others
References
Akam M (1986) Developmental genes. Mediators of cell communication? Nature 319:447–448
Arking R (1975) Temperature sensitive cell lethal mutants ofDrosophila: isolation and characterization. Genetics 80:519–537
Baker NE (1988) Embryonic and imaginal requirements forwingless, a segment-polarity gene inDrosophila. Dev Biol 125:96–108
Bodenstein D (1962) Regeneration in insects. Symp Genet Biol Ital 9:1–19
Botas J, Cabrera CV, Garcia-Bellido A (1988) The reinforcement-extinction process of selector gene activity: a positive feed-back loop and cell-cell interactions in Ultrabithorax patterning. Roux's Arch Dev Biol 197:424–434
Bryant PJ (1971) Regeneration and duplication following operationsin situ on the imaginal discs ofDrosophila melanogaster. Dev Biol 26:637–651
Bryant PJ (1974) Determination and pattern formation in the imaginal discs ofDrosophila. Curr Top Dev Biol 8:41–80
Bryant PJ (1987) Experimental and genetic analysis of growth and cell proliferation inDrosophila imaginal discs. In: Genetic regulation of development, vol 17. Alan R. Liss, New York, pp 339–372
Busturia A Morata G (1988) Ectopic expression of homeotic genes caused by the elimination of thePolycomb gene inDrosophila imaginal epidermis. Development 104:713–720
Cabrera CV, Botas J, Garcia-Bellido, A (1985) Distribution of Ultrabithorax proteins in mutants ofDrosophila Bithorax complex and its regulatory genes. Nature 318:569–571
Capdevila MP, Botas J, Garcia-Bellido A (1986) Genetic interactions between thePolycomb locus and theAntennapedia andbithorax complexes ofDrosophila. Wilhelm Roux's Arch 195:417–432
Doe CQ, Goodman CS (1985) Early events in insect neurogenesis. II. The role of cell interactions and cell lineage in the determination of neuronal precursor cells. Dev Biol 111:206–219
Doe CQ, Smouse D, Goodman CS (1988) Control of neuronal fate by theDrosophila segmentation gene even-skipped. Nature 333:376–378
Dübendorfer K, Nöthiger R (1982) A clonal analysis of cell lineage and growth in the male and female genital disc ofDrosophila melanogaster. Wilhelm Roux's Arch 191:42–55
Duncan I (1982)Polycomblike: a gene that appears to be required for the normal expression of the bithorax and Antennapedia gene complexes ofDrosophila melanogaster. Genetics 102:49–70
Duncan I, Lewis EB (1982) Genetic control of body segment differentiation inDrosophila. In: Subtelny S (ed) Developmental order: its origin and regulation. Alan R. Liss, New York, pp 533–554
Dura JM, Ingham P (1988) Tissue and stage specific control of homeotic and segmentation gene expression inDrosophila embryos by thepolyhomeotic gene. Development 103:733–741
Dura JM, Brock HW, Santamaria P (1985)polyhomeotic: a gene ofDrosophila melanogaster required for correct expression of segmental identity. Mol Gen Gener 198:213–220
Dura JM, Randsholt NB, Deatrick J, Erk I, Santamaria P, Freeman JD, Freeman SJ, Weddell D, Brock HW (1987) A complex genetic locus,polyhomeotic, is required for segmental specification and epidermal development inD. melanogaster. Cell 51:829–839
Dura JM, Deatrick J, Randsholt NB, Brock HW, Santamaria P (1988) Maternal and zygotic requirement for thepolyhomeotic complex genetic locus inDrosophila. Roux's Arch Dev Biol 197:239–246
French V, Bryant PJ, Bryant SV (1976) Pattern regulation in epimorphic fields. Science 193:969–981
Garcia-Bellido A (1972) Some parameters of mitotic recombination inDrosophila melanogaster. Mol Gen Genet 115:54–72
Garcia-Bellido A, Dapena J (1974) Induction, detection and characterization of cell differentiation mutants inDrosophila. Mol Gen Genet 128:117–130
Garcia-Bellido A, Lewis EB (1976) Autonomous differentiation of homeotic bithorax mutants ofDrosophila melanogaster. Dev Biol 48:400–410
Garcia-Bellido A, Merriam JR (1971a) Parameters of the wing imaginal disc development ofDrosophila melanogaster. Dev Biol 24:61–87
Garcia-Bellido A, Merriam JR (1971b) Genetic analysis of cell heredity in imaginal discs ofDrosophila melanogaster. Proc Natl Acad Sci USA 68:2222–2226
Garcia-Bellido A, Santamaria P (1972) Developmental analysis of the wing disc in the mutantengrailed ofDrosophila melanogaster. Genetics 72:87–104
Garcia-Bellido A, Ripoll P, Morata G (1973) Developmental compartalization of the wing disc ofDrosophila melanogaster. Nat New Biol 245:251–253
Garcia-Bellido A, Ripoll P, Morata G (1976) Developmental segregations in the dorsal mesothoracic disc ofDrosophila. Dev Biol 48:132–147
Girton JR (1981) Pattern triplications produced by a cell-lethal mutation inDrosophila. Dev Biol 84:164–172
Girton JR and Bryant PJ (1980) The use of cell-lethal mutations in the study ofDrosophila development. Dev Biol 77:233–243
Girton JR, Russell MA (1980) A clonal analysis of pattern duplication in a temperature-sensitive cell-lethal mutant ofDrosophila melanogaster. Dev Biol 77:1–21
Ingham PW (1984) A gene that regulates the bithorax complex differentially in the larval and adult cells ofDrosophila. Cell 37:815–823
James AA, Bryant PJ (1981) Mutations causing pattern deficiencies and duplications in the imaginal wing disc ofDrosophila melanogaster. Dev Biol 85:39–54
Jürgens G, Gateff E (1979) Pattern specification in imaginal discs ofDrosophila melanogaster developmental analysis of a temperature-sensitive mutant producing duplicated legs. Wilhelm Roux's Archiv 186:1–25
Kauffmann SA (1984) Pattern generation and regeneration. In: Pattern formation: a Primer in developmental biology Malacinski G, Bryant SV (eds). Macmillan, New York, pp 73–162
Kimble J (1981) Alterations in cell lineage following laser ablation of cells in the somatic gonad ofCenorhabditis elegans. Dev Biol 87:286–300
Kirby BS, Bryant PJ, Schneiderman HA (1982) Regeneration following duplication in imaginal wing disc fragments ofDrosophila melanogaster. Dev Biol 90:259–271
Lawrence PA and Morata G (1976) Compartments in the wing ofDrosophila: a study of theengrailed gene. Dev Biol 50:321–337
Leptin M, Aebersold R, Wilcox M (1987)Drosophila position-antigens resemble the vertebrate fibronectin-receptor family. EMBO J 6:1037–1043
Lewis J (1981) Simpler rules for epimorphic regeneration: the polar coordinate model without polar co-ordinates. J Theor Biol 88:371–392
Meinhardt H, Gierer A (1974) Applications of a theory of biological pattern formation based on lateral inhibition. J Cell Sci 15:321–346
Meinhardt H, Gierer A (1980) Generation and regeneration of sequences of structures during morphogenesis. J Theor Biol 85:429–450
Mittenthal JE (1981) The rule of normal neighbors: a hypothesis for morphogenetic pattern regulation. Dev Biol 88:15–26
Morata G (1975) Analysis of gene expression during the development in the homeotic mutantContrabithorax ofDrosophila. J Embryol Exp Morphol 34:19–31
Morata G, Garcia-Bellido A (1976) Developmental analysis of some mutants of thebithorax system ofDrosophila. Wilhelm Roux' Arch 179:125–143
Morata G, Lawrence PA (1977) The development ofwingless, a homeotic mutation ofDrosophila. Dev Biol 56:227–250
Moscona AA (1956) Development of heterotypic combinations of dissociated embryonic chick cells. Proc Soc Exp Biol Med 92:410–416
O'Brochta DA, Bryant PJ (1985) A zone of non-proliferating cells at a lineage restriction boundary inDrosophila. Nature 313:138–141
Ripoll P, El Messal M, Laron E, Simpson P (1988) A gradient of affinities for sensory bristles across the wing blade ofDrosophila melanogaster. Development 103:757–767
Schubiger M and Palka J (1987) Changing spatial patterns of DNA replication in the developing wing ofDrosophila. Dev Biol 123:145–153
Simpson P (1976) Analysis of the compartments of the wing ofDrosophila melanogaster mosaic for a temperature-sensitive mutation that reduces mitotic rate. Dev Biol 54:100–115
Simpson P (1979) Parameters of cell competition in the compartments of the wing disc ofDrosophila. Dev Biol 69:182–193
Simpson P and Grau Y (1987) The segment polarity mutantcostal-2 inDrosophila II. The origin of imaginal pattern duplications. Dev Biol 122:201–209
Simpson P, Schneiderman HA (1975) Isolation of temperature-sensitive mutations blocking clone development inDrosophila melanogaster, and the effects of a temperature-sensitive cell lethal mutation on pattern formation in imaginal discs.
Simpson P, El Messal M, Moscoso del Prado and Ripoll P (1988) Stripes of positional homology across the wing blade ofDrosophila m. Development 103:391–401
Smouse D, Goodman C, Mahowald A, Perrimon N (1988)polyhomeotic: a gene required for the embryonic development of axon pathways in the central nervous system ofDrosophila. Genes Dev 2:830–840
Stern C (1954) Two or three bristles. Sci Am 42:213–247
Stern C (1956) The genetic control of developmental competence and morphogenetic tissue interactions in genetic mosaics. Wilhelm Roux' Arch Entwicklungsmech Org 149:1–25
Struhl G (1981) A gene product required for correct initiation of segmental determination inDrosophila. Nature 293:36–41
Szabad J, Simpson P, Nöthiger R (1979) Regeneration and compartments inDrosophila. J Embryol Exp Morphol 49:229–241
Wolpert L (1971) Positional information and pattern formation. Curr Top Dev Biol 6:183–224
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Santamaria, P., Deatrick, J. & Randsholt, N.B. Pattern triplications following genetic ablation on the wing ofDrosophila . Roux's Arch Dev Biol 198, 65–77 (1989). https://doi.org/10.1007/BF02447741
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02447741