The fine structure of developing bristles in wild type and mutant Drosophila melanogaster

Abstract

In an attempt to understand the factors involved in morphogenesis of a complex cell like a scale or bristle, the fine structure of the normal development of bristle cells in Drosophila melanogaster (Oregon R ) has been studied and compared with that of the mutants sn3 and Sb. In the development of the normal bristle rounded bundles of longitudinally oriented fibrils lie just beneath the cell surface at regularly spaced intervals. Fiber bundles constitute about 20% of the cross sectional area. The cytoplasmic surface between these bundles is active in enveloping the nerve fiber associated with the bristle and in sending out cytoplasmic processes associated with which the longitudinally oriented bristle ridges form. Singed bristles are bent and twisted and the fiber bundles are present as flattened bands constituting only about 5% of the cross-sectional area. In Sb mutants the total cross-sectional area of fiber bundle material is the same as that in Oregon R, but fiber bundles are smaller and more numerous, being distributed over the larger surface of this thicker and shorter bristle. They constitute only 7% of the cross-sectional area of the bristle. In Sn3Sb mutants characteristics of each gene are exaggerated and an extremely short, wide, and irregular bristle is formed.A close description of the fine structure of developing scales and bristles (Paweletz and Schlote, '64; Overton, '66; Locke, '66; Lawrence, '66) suggests that the orientation and grouping of microtubules and microfibrils are important in the morphogenesis of these cells. It is difficult to interfere experimentally in a system of this kind to confirm this suggestion. Although shape changes in scales have been produced by heat treatment (Kohler and Feldotto, '37), irradiation (Lobbecke and Muller, '60), and administration of DNA base analogues (Caspari, Muth and Pohley, '65) none of these changes are such that they could be easily analyzed at the fine structure level. Attempts to analyze factors involved i n the development of cell shape have also been made by considering the effects of genetic interference (Shoup, '67; Waddington, '62). This approach has been utilized here. Singed mutants which have bent and twisted bristles and stubble mutants which have regularly shaped but short and thick bristles were compared with wild type bristles and with singed stubble when present together. Although mutations which eliminate certain microtubules in other systems are known (Warr et al., '66) in the bristle mutants studied here there was no evident effect on the microtubules. However, the fiber bundles which are associated with the cell surface of the developing bristle rudiment were markedly different in their size, shape, and number in the mutants. Thus a difference i n cell shape can be correlated with differences in the amount and distribution of this fibrous material. Microtubules may, of course, also be involved in cell elongation but the present work provides no critical test of this. MATERIALS AND METHODSMutants studied were sn3 (1-21.0),...

Fascin links Btl/FGFR signalling to the actin cytoskeleton during Drosophila tracheal morphogenesis

“…Development (2014) cells (Cant et al, 1994), dendrite terminal branchlets in sensory neurons (Nagel et al, 2012), actin bundles in the bristles (Cant et al, 1994;Overton, 1967;Tilney et al, 1995) or lamellae microspikes in plasmatocytes (Zanet et al, 2009). In these structures sn promotes the formation of straight and stiff structures, whereas its absence leads to the formation of curved ones.…”

A Balance of Capping Protein and Profilin Functions Is Required to Regulate Actin Polymerization inDrosophilaBristle

“…During pupal development, the bristle cell elaborates a long process that contains prominent longitudinal bundles of actin filaments associated with the plasma membrane (Overton, 1967;Appel et al, 1993). Cuticle is deposited on the surface of this process, and then as development proceeds, the actin cytoskeleton disassembles, the cell regresses, and the remaining hollow tube of cuticle becomes the adult bristle.…”

Mutational Analysis of Stubble-stubbloid Gene Structure and Function in Drosophila Leg and Bristle Morphogenesis

“…The more consistent and severe phenotype may require the constant and abundant presence of the truncated protein in bristles as suggested by the difference in bristle phenotype between Sb 1 , in which the truncated Sb 1 transcript is expressed in amounts comparable to the wild-type transcript, and Sb 63b , in which the similarly truncated transcript is overexpressed compared to the wild-type transcript. Sb 1 bristles are longer than those of Sb 63b and while Sb 1 bristles often have extra actin bundles, the number of bundles (11-18) overlaps with that of wild type (Lees and Picken 1945;Overton 1967).…”

“…We propose that ECM constraint is an additional external force in bristle morphogenesis. Lees and Picken (1945), Overton (1967), and Tilney et al (2003) all found that the total bristle volume is the same in wild-type and Sb mutants; the increased bundle number and thickness in the mutants corresponds to the decrease in length. The extra bundles are most numerous in severe dominant mutants that produce a truncated protein entirely lacking the stubblin protease, e.g., Sb 63b (Appel et al 1993).…”

“…Within the extending bristle cell, a scaffold is formed by a core of microtubules surrounded by modules of membrane-associated actin microfilament bundles joined end to end (Overton 1967;Appel et al 1993;Tilney et al 1995Tilney et al , 1996Tilney et al , 1998Wulfkuhle et al 1998). The bristle grows as individual actin filaments continuously form at the bristle tip on the cytoplasmic side of the plasma membrane and are gathered together to form progressively larger and more tightly crosslinked bundles by the sequential action of two actin-binding proteins, forked and singed (Lees and Picken 1945;Tilney et al 1996).…”