Compartments and the control of growth in the Drosophila wing imaginal disc

The mechanisms that control organ growth are among the least known in development. This is particularly the case for the process in which growth is arrested once final size is reached. We have studied this problem in the wing disc of Drosophila, the developmental and growth parameters of which are well known. We have devised a method to generate entire fast-growing Minute+ (M+) discs or compartments in slow developing Minute/+ (M/+) larvae. Under these conditions, a M+ wing disc gains at least 20 hours of additional development time. Yet it grows to the same size of Minute/+ discs developing in M/+ larvae. We have also generated wing discs in which all the cells in either the anterior (A) or the posterior (P) compartment are transformed from M/+ to M+. We find that the difference in the cell division rate of their cells is reflected in autonomous differences in the developmental progression of these compartments: each grows at its own rate and manifests autonomous regulation in the expression of the developmental genes wingless and vestigial. In spite of these differences, `mosaic' discs comprising fast and slow compartments differentiate into adult wings of the correct size and shape. Our results demonstrate that imaginal discs possess an autonomous mechanism with which to arrest growth in anterior and posterior compartments, which behave as independent developmental units. We propose that this mechanism does not act by preventing cell divisions, but by lengthening the division cycle.

[1]  S. Goto,et al.  Proximal to distal cell communication in the Drosophila leg provides a basis for an intercalary mechanism of limb patterning. , 1999, Development.

[2]  G. Morata,et al.  Minutes: mutants of drosophila autonomously affecting cell division rate. , 1975, Developmental biology.

[3]  G. Campbell,et al.  Transducing the Dpp Morphogen Gradient in the Wing of Drosophila Regulation of Dpp Targets by brinker , 1999, Cell.

[4]  S. Leevers,et al.  Controlling the size of organs and organisms. , 2005, Current opinion in cell biology.

[5]  G M Rubin,et al.  Expression of baculovirus P35 prevents cell death in Drosophila. , 1994, Development.

[6]  Sean B. Carroll,et al.  Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene , 1996, Nature.

[7]  P. Lawrence,et al.  The early development of mesothoracic compartments in Drosophila. An analysis of cell lineage and fate mapping and an assessment of methods. , 1977, Developmental biology.

[8]  E. Hafen,et al.  Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. , 2003, Trends in cell biology.

[9]  P. Bryant,et al.  Intrinsic and Extrinsic Control of Growth in Developing Organs , 1984, The Quarterly Review of Biology.

[10]  S. Blair,et al.  Engrailed expression in the anterior lineage compartment of the developing wing blade of Drosophila. , 1992, Development.

[11]  T. P. Neufeld,et al.  Coordination of Growth and Cell Division in the Drosophila Wing , 1998, Cell.

[12]  B. Charroux,et al.  Grunge, related to human Atrophin-like proteins, has multiple functions in Drosophila development. , 2002, Development.

[13]  A. Teleman,et al.  Dpp Gradient Formation in the Drosophila Wing Imaginal Disc , 2000, Cell.

[14]  S. Carroll,et al.  Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary , 1994, Nature.

[15]  P J Bryant,et al.  Intrinsic growth control in the imaginal primordia of Drosophila, and the autonomous action of a lethal mutation causing overgrowth. , 1985, Developmental biology.

[16]  N. Fuse,et al.  Diploidy of Drosophila imaginal cells is maintained by a transcriptional repressor encoded by escargot. , 1994, Genes & development.

[17]  A. Ferrús Parameters of mitotic recombination in minute mutants of Drosophila melanogaster. , 1975, Genetics.

[18]  A. Whitworth,et al.  Temporally dynamic response to Wingless directs the sequential elaboration of the proximodistal axis of the Drosophila wing. , 2003, Developmental biology.

[19]  G. Rubin,et al.  Analysis of genetic mosaics in developing and adult Drosophila tissues. , 1993, Development.

[20]  G. Morata,et al.  The Pax-homeobox gene eyegone is involved in the subdivision of the thorax of Drosophila , 2003, Development.

[21]  P. Simpson Analysis of the compartments of the wing of Drosophila melanogaster mosaic for a temperature-sensitive mutation that reduces mitotic rate. , 1976, Developmental biology.

[22]  A. Garcı́a-Bellido,et al.  Cell cycling and patterned cell proliferation in the Drosophila wing during metamorphosis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[23]  H. Müller,et al.  The Drosophila Caspase Inhibitor DIAP1 Is Essential for Cell Survival and Is Negatively Regulated by HID , 1999, Cell.

[24]  S. Cohen,et al.  Specification of the wing by localized expression of wingless protein , 1996, Nature.

[25]  B. Edgar,et al.  A characterization of the effects of Dpp signaling on cell growth and proliferation in the Drosophila wing. , 2002, Development.

[26]  G. Struhl,et al.  Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. , 1995, Development.

[27]  G. Morata,et al.  Visualization of Gene Expression in Living Adult Drosophila , 1996, Science.

[28]  Ginés Morata,et al.  The brinker gradient controls wing growth in Drosophila , 2004, Development.

[29]  Ryan S. Udan,et al.  Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway , 2003, Nature Cell Biology.

[30]  William M. Gelbart,et al.  Decapentaplegic: A gene complex affecting morphogenesis in Drosophila melanogaster , 1982, Cell.

[31]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

[32]  P. Lawrence,et al.  Measuring dimensions: the regulation of size and shape. , 2000, Development.

[33]  A. Lambertsson The minute genes in Drosophila and their molecular functions. , 1998, Advances in genetics.

[34]  A. Garcı́a-Bellido,et al.  Parameters of the wing imaginal disc development of Drosophila melanogaster. , 1971, Developmental biology.