Correlations between developmental capacity and structure of tissue sublines derived from the eye-antennal imaginal disc ofDrosophila melanogaster

Abstract

Developmental capacities of imaginal disc tissue sublines were correlated with their growth rate, morphology, histology and fine structure. Tissue sublines were derived from half an eye-antennal disc ofDrosophila melanogaster and were serially subculturedin vivo in the abdomens of adult female flies for over 150 transfer generations (8 years and more than 1000 cell divisions). During this period the capacities for differentiation of the tissue sublines were repeatedly tested by implantations into larvae for metamorphosis. At the outset the tissues behaved autotypically and metamorphosed into eye and antennal structures. They then transformed in one of three ways: they underwent transdetermination to become allotypic and metamorphosed into structures belonging to another disc; they became anormotypic and metamorphosed into abnormal cuticular patterns; they became atelotypic and failed to make any cuticle when caused to metamorphose. All allotypic sublines gradually became anormotypic and finally atelotypic. The results show that atelotypic tissue sublines arise in two ways: directly from autotypic tissues or gradually from auto-, allo-, or anormotypic tissues.One gradually transformed atelotypic tissue line which had failed to make cuticle for four years and 59 transfer generations, although repeatedly tested, was enabled to regain the capacity to secrete cuticle by subculturing at low temperatures in abdomens of adultD. virilis where the implanted tissues grew slowly.Allo-, anormo-, and atelotypic changes were associated with a marked increase in rate of proliferation and with characteristic changes in tissue and cell structure. Auto- and allotypic tissues are composed mainly of columnar or cuboidal imaginal disc epithelial cells arranged in monolayers, with a regimented array of microvilli on their apical surface, a smooth basement membrane on their basal surface, and extensive intercellular junctional complexes. They form sac-like structures when subcultured in adult abdomens. Anormotypic tissue is a mosaic of regions with cells in monolayers and in compact masses. The cells in both arrangements resemble imaginal disc cells in their staining properties. However, the cells in these monolayers do not have well developed microvillar surfaces and their basement membranes are curled and detached from the cell surface. The cells in compact masses appear to be modified imaginal disc epithelial cells which possess neither a microvillar surface nor a basement membrane and have far fewer intercellular junctional complexes than do imaginal disc epithelial cells.Atelotypic tissue sublines are composed primarily of cells in a compact mass and form a solid ball when cultured in adult abdomens. These masses contain numerous lacunae and are comprised of three cell types with characteristic morphology and staining properties, designated as intensely staining cells, faintly staining cells, and elongated cells. The intensely staining cells resemble the modified imaginal disc epithelial cells in compact masses that occur in anormotypic tissues and, like them, they lack microvilli and a basement membrane. The faintly staining cells are spindle shaped and appear to have arisen from the intensely staining cells. The elongated cells are found exclusively in the lacunae and they resemble adepithelial cells which may be the precursors of muscles in normal imaginal discs. Developing muscle cells occur in both anormotypic and atelotypic implants.Correlations are drawn between the tissue and cell structure and the developmental capacities of different tissue sublines which permit predictions to be made of the developmental capacities of a tissue subline from an examination of its structure. Cells arranged in monolayers with a well-formed microvillar surface, continuous basement membrane, and extensive junctional complexes secrete a cuticle with a normal pattern. Cells arranged in monolayers, but with detached and curled basement membranes and defective microvillar surfaces secrete a cuticle with an abnormal pattern. Cells in compact masses lack microvilli, a basement membrane, and extensive intercellular junctions and do not secrete cuticle. The elongated cells found in some sublines probably form muscle.Possible mechanisms underlying the atelotypic transformation were discussed and the significance of the reversibility of atelotypic behavior was examined. The structure and behavior of atelotypic lines were compared with those of neoplasms derived from imaginal discs of theD. melanogaster mutant,l(2)gl ⁴.