Development of the Drosophila olfactory sense organs utilizes cell-cell interactions as well as lineage (original) (raw)
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Mechanisms of Development, 2000
We have shown that the basic helix±loop±helix transcription factor Atonal is suf®cient for speci®cation of one of the three subsets of olfactory sense organs on the Drosophila antenna. Misexpression of Atonal in all sensory precursors in the antennal disc results in their conversion to coeloconic sensilla. The mechanism by which speci®c sense organ fate is triggered remains unclear. We have shown that the homeodomain transcription factor Cut which acts in the chordotonal±external sense organ choice does not play a role in olfactory sense organ development. The expression of atonal in speci®c domains of the antennal disc is regulated by an interplay of the patterning genes, Hedgehog and Wingless, and Drosophila epidermal growth factor receptor pathway. q
Developmental Biology, 2003
The Drosophila antenna has a diversity of chemosensory organs within a single epidermal field. We have some idea from recent studies of how the three broad categories of sense-organs are specified at the level of progenitor choice. However, little is known about how cell fates within single sense-organs are specified. Selection of individual primary olfactory progenitors is followed by organization of groups of secondary progenitors, which divide in a specific order to form a differentiated sensillum. The combinatorial expression of Prospero Elav, and Seven-up allows us to distinguish three secondary progenitor fates. The lineages of these cells have been established by clonal analysis and marker distribution following mitosis. High Notch signaling and the exclusion of these markers identifies PIIa; this cell gives rise to the shaft and socket. The sheath/neuron lineage progenitor PIIb, expresses all three markers; upon division, Prospero asymmetrically segregates to the sheath cell. In the coeloconica, PIIb undergoes an additional division to produce glia. PIIc is present in multiinnervated sense-organs and divides to form neurons. An understanding of the lineage and development of olfactory sense-organs provides a handle for the analysis of how olfactory neurons acquire distinct terminal fates.
The emergence of sense organs in the wing disc of Drosophila
Development (Cambridge, England), 1991
We have examined the origin of a set of precisely located sense organs in the notum and wing of Drosophila, in transformant flies where lacZ is expressed in the progenitor cells of the sense organs (the sensory mother cells) and in their progeny. Here we describe the temporal pattern of appearance and divisions of the sensory mother cells that will form the eleven macrochaetes and the two trichoid sensilla of the notum, and five campaniform sensilla on the wing blade. The complete pattern of sensory mother cells develops in a strict sequence that extends over most of the third larval instar and the first 10 h after puparium formation. The delay between the onset of lacZ expression and the first differentiative division ranges from 30 h, in the case of the earliest mother cells, to 2 h for the latest mother cells. The first division shows a preferential orientation which is also specific for each sensory mother cell. Up to this stage, there is no marked difference between the three t...
The determination of sense organ in Drosophila: Effect of the neurogenic mutations in the embryo
Development
We have examined the early pattern of sensory mother cells in embryos mutant for six different neurogenic loci. Our results show that the neurogenic loci are required to restrict the number of competent cells that will become sensory mother cells, but are not involved in controlling the localization or the position-dependent specification of competent cells. We conclude that these loci are involved in setting up a system of mutual inhibition, which transforms graded differences within the proneural clusters into an all-or-none difference between one cell, which becomes the sense organ progenitor cell, and the other cells, which remain epidermal.
Eight sensory structures (campaniform sensilla), appearing identical in the light and scanning electron microscopes, are found in specific locations on the wings of Drosophiia. Their axons enter one of 2 central tracts, a medial one or a lateral one. The topographic arrangement of the sensilla on the wing is not reflected in this central projection pattern. There is, however, a strict correlation between the time when a sensillum develops and the path its axon follows: The 4 sensilla whose axons form the medial projection are born and differentiate early during the development of the wing, while the other 4 sensilla, all of which project laterally, arise during a second wave of differentiation.
Developmental Biology, 1998
This cell is believed to recruit neighbours to form a cluster of cells which then divides to form a mature sense organ. In most systems so far studied, sense organ type appears to be specified by the identity of proneural genes involved in the selection of precursors. The regulation of proneural gene expression is, in turn, controlled by the prepatterning genes. In the antenna, the only known proneural function is that of atonal, a gene that is involved in founder cell choice in the sensilla coeloconica, and no prepatterning gene function has yet been demonstrated. In this study, we show that Lozenge, a protein which possesses a DNA binding domain similar to that of the Acute myeloid leukemia-1/Runt transcription factors, functions in a dose-dependent manner to specify the fate of the other two types of sense organs in the antenna: the sensilla trichoidea and the sensilla basiconica. Our results suggest that Lozenge may act on the epidermal field, resulting in founder cells acquiring specific cell fates that lead to the development of an appropriate type of sense organ.
Role of proneural genes in the formation of the larval olfactory organ of Drosophila
Development Genes and Evolution, 2007
In this paper, we address the role of proneural genes in the formation of the dorsal organ in the Drosophila larva. This organ is an intricate compound comprising the multineuronal dome—the exclusive larval olfactory organ—and a number of mostly gustatory sensilla. We first determine the numbers of neurons and of the different types of accessory cells in the dorsal organ. From these data, we conclude that the dorsal organ derives from 14 sensory organ precursor cells. Seven of them appear to give rise to the dome, which therefore may be composed of seven fused sensilla, whereas the other precursors produce the remaining sensilla of the dorsal organ. By a loss-of-function approach, we then analyze the role of atonal, amos, and the achaete-scute complex (AS-C), which in the adult are the exclusive proneural genes required for chemosensory organ specification. We show that atonal and amos are necessary and sufficient in a complementary way for four and three of the sensory organ precursors of the dome, respectively. AS-C, on the other hand, is implicated in specifying the non-olfactory sensilla, partially in cooperation with atonal and/or amos. Similar links for these proneural genes with olfactory and gustatory function have been established in the adult fly. However, such conserved gene function is not trivial, given that adult and larval chemosensory organs are anatomically very different and that the development of adult olfactory sensilla involves cell recruitment, which is unlikely to play a role in dome formation.
Origin and morphogenesis of sensory neurons in an insect antenna
Developmental Biology, 1976
Each antenna1 flagellum of the moth, Manduca sexta, contains about 2.5 x lo" primary sensory neurons. The neurons are components of small sensory organs (sensilla) and send axons through antenna1 nerves to the brain. The neurons, sensilla, and nerves differentiate as the antenna develops, during the 18 days of metamorphosis from pupa to adult. Neurons arise from divisions of epidermal cells between 25 and 60 hr after pupal ecdysis and elaborate axons and dendrites soon thereafter. Neurons have the bipolar form, ciliated dendrite, and glial sheath characteristic of the adult within a few days of their birth. The axons grow along small pupal nerves to form the adult antenna1 nerves, and the dendrites grow beyond the apical margin of the epidermis, where they are enveloped by a growing process of the sensilla's trichogen cell. Cuticle secreted by the trichogen cell forms the seta or sensory hair of the sensillum. Later, the neuronal somata migrate from the basal to the apical margin of the epidermis. Finally, the cytoplasm withdraws from the seta, leaving the dendrites imprisoned in a cylinder of cuticle. All of the neurons in the flagellum differentiate nearly synchronously, facilitating correlation of morphogenetic results presented here with biochemical and electrophysiological analyses of the developing neurons. 300 Copyright G 19% by Acadeinic Press, Inc. All rights of reproduction in any form reserved.
Sensory neurons and peripheral pathways in Drosophila embryos
Roux's Archives of Developmental Biology, 1986
The thoracic and abdominal segments of the Drosophila embryo contain 373 neurons innervating external sensory structures and 162 neurons innervating chordotonal organs. These neurons are arranged in ventral, lateral and dorsal clusters within each segment, in a highly invariant pattern. Two fascicles are formed in each segment as the sensory axons grow ventrally towards the CNS and meet motor axons growing dorsally from the CNS. In all but the last segment, the anterior fascicle is contributed by the dorsal and lateral neurons, while the posterior one is formed by the ventral neurons. Five distinct segmental patterns are described, corresponding to (1) the prothorax, (2) the other two thoracic segments, (3) the first seven abdominal segments, (4) the eighth and (5) the ninth (and possibly the tenth) abdominal segments.
Position-reading and the emergence of sense organ precursors in Drosophila
Progress in Neurobiology, 1994
Genetic analysis of development in Drosophila melanogaster has advanced our understanding of "position reading", where the expression of particular genes informs a cell of its position in the developing animal. The first step in localization of fly sense organs is the local expression of a gene conferring neural competence on epidermal cells. The four genes of the achaete-scute (AS-C) complex play crucial roles in the localization of sense organs. The resolution of local expression of AS-C genes along one dimension is about 10%; accuracy is improved by the balancing local expression of AS-C antagonist genes such as extramacrochaete. Position reading seems to depend primarily on such patterns of gene expression, and not upon the compartmental identity of the cells. No evidence has been found for differing roles of the four AS-C genes in the generation of sense organ progenitor cells or in the specification of neuronal properties of innervating neurons. The formation of each sense organ may be a unique case where the different proneural and neurogenic gene products have varying importance, and fortuitous local effects acting on this complex combination of factors have come to be important. The fly may be evolving from a flexible regular pattern to an inflexible irregular pattern strongly dependent on local factors, turning the fly into a crystallized system. (Written by R. Wayne Davies.) CONTENTS Abbreviations