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© The Rockefeller University Press, 0021-9525/1998//1135 $5.00
The Journal of Cell Biology, Volume 141, Number 5, , 1998 1135-1145


Articles

Patterning Muscles Using Organizers: Larval Muscle Templates and Adult Myoblasts Actively Interact to Pattern the Dorsal Longitudinal Flight Muscles of Drosophila



Sudipto Roy and K. VijayRaghavan

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore 560012, India

Pattern formation in muscle development is often mediated by special cells called muscle organizers. During metamorphosis in Drosophila, a set of larval muscles function as organizers and provide scaffolding for the development of the dorsal longitudinal flight muscles. These organizers undergo defined morphological changes and dramatically split into templates as adult fibers differentiate during pupation. We have investigated the cellular mechanisms involved in the use of larval fibers as templates. Using molecular markers that label myoblasts and the larval muscles themselves, we show that splitting of the larval muscles is concomitant with invasion by imaginal myoblasts and the onset of differentiation. We show that the Erect wing protein, an early marker of muscle differentiation, is not only expressed in myoblasts just before and after fusion, but also in remnant larval nuclei during muscle differentiation. We also show that interaction between imaginal myoblasts and larval muscles is necessary for transformation of the larval fibers. In the absence of imaginal myoblasts, the earliest steps in metamorphosis, such as the escape of larval muscles from histolysis and changes in their innervation, are normal. However, subsequent events, such as the splitting of these muscles, fail to progress. Finally, we show that in a mutant combination, null for Erect wing function in the mesoderm, the splitting of the larval muscles is aborted. These studies provide a genetic and molecular handle for the understanding of mechanisms underlying the use of muscle organizers in muscle patterning. Since the use of such organizers is a common theme in myogenesis in several organisms, it is likely that many of the processes that we describe are conserved.


Abbreviations used in this paper: APF, after puparium formation; DLM, dorsal longitudinal muscle; DVM, dorso-ventral muscle; ewg, erect wing, IFM, indirect flight muscle; MHC, myosin heavy chain; UAS, upstream activating sequence.

S. Roy's visit to K. White's laboratory as a special graduate student was supported by a traveling fellowship from the Company of Biologists Ltd., (Cambridge, England) and Brandeis University. This work was supported by grants from the National Centre for Biological Sciences (NP1) and from the Human Frontier Science Programme (HFSP/KVR/95) to K. VijayRaghavan.

Address all correspondence to K. VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, IISc Campus, P.O. Box 1234, Bangalore 560012, India. Tel.: (91) 80-33-430-35. Fax: (91) 80-33-438-51. E-mail: vijay{at}ncbs.tifrbng.res.in



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