F-actin bundles in Drosophila bristles are assembled from modules composed of short filaments.
The actin bundles in Drosophila bristles run the length of the bristle cell and are accordingly 65 microns (microchaetes) or 400 microns (macrochaetes) in length, depending on the bristle type. Shortly after completion of bristle elongation in pupae, the actin bundles break down as the bristle surface becomes chitinized. The bundles break down in a bizarre way; it is as if each bundle is sawed transversely into pieces that average 3 microns in length. Disassembly of the actin filaments proceeds at the "sawed" surfaces. In all cases, the cuts in adjacent bundles appear in transverse register. From these images, we suspected that each actin bundle is made up of a series of shorter bundles or modules that are attached end-to-end. With fluorescent phalloidin staining and serial thin sections, we show that the modular design is present in nondegenerating bundles. Decoration of the actin filaments in adjacent bundles in the same bristle with subfragment 1 of myosin reveals that the actin filaments in every module have the same polarity. To study how modules form developmentally, we sectioned newly formed and elongating bristles. At the bristle tip are numerous tiny clusters of 6-10 filaments. These clusters become connected together more basally to form filament bundles that are poorly organized, initially, but with time become maximally cross-linked. Additional filaments are then added to the periphery of these organized bundle modules. All these observations make us aware of a new mechanism for the formation and elongation of actin filament bundles, one in which short bundles are assembled and attached end-to-end to other short bundles, as are the vertical girders between the floors of a skyscraper.
Tilney
L G
LG
Department of Biology, University of Pennsylvania, Philadelphia 19104, USA.
Connelly
P
P
Smith
S
S
Guild
G M
GM
D008841:Actin Cytoskeleton / Q000737:chemistry / Q000648:ultrastructure*; D000199:Actins / Q000032:analysis* / Q000648:ultrastructure; D000818:Animals; D002352:Carrier Proteins / Q000235:genetics; D016764:Cell Polarity; D029721:Drosophila Proteins; D004331:Drosophila melanogaster / Q000235:genetics / Q000254:growth & development / Q000648:ultrastructure; D007301:Insect Hormones / Q000235:genetics; D008840:Microfilament Proteins; D008854:Microscopy, Electron; D008855:Microscopy, Electron, Scanning; D008870:Microtubules / Q000648:ultrastructure; D009024:Morphogenesis; D009154:Mutation; D011679:Pupa; D011984:Sensory Receptor Cells / Q000254:growth & development / Q000648:ultrastructure*
D000199:Actins; D002352:Carrier Proteins; D029721:Drosophila Proteins; D007301:Insect Hormones; D008840:Microfilament Proteins; C084628:f protein, Drosophila; C020324:fascin