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Genetic Regulation of Morphogenesis of Drosophila melanogaster Mechanoreceptors

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Abstract

Drosophila mechanoreceptors (bristles), represented by macro- and microchetae, are located on the insect body in an orderly manner and are the result of a deterministic conversion of ectodermal cells of imaginal discs into progenitor neural cells with the following differentiation of derivatives of these cells into components of the mechanoreceptor, which consists of two surface cuticle structures, a bristle with a socket and two underlying neural components: neuron and a glial cell. The morphogenesis of mechanoreceptors occurs through three successive stages: (1) segregation from the mass of ectodermal cells of domains that are potentially competent to the neural pathway of development (proneural clusters (PC)); (2) separation of the parental cell of mechanoreceptor (PCM) in the proneural cluster, and (3) three asymmetric divisions of PCM and its descendant cells with the specialization of daughter cells of the last generation into components of a definitive sensory organ. The formation of the bristle pattern is ordered in space and time. The spatial determination is due to the positioning of the parental cells, and the temporal determination is associated with two synchronization events: the completion of separation of PCM for all mechanoreceptors by the first to tenth hour after the formation of the puparium and the time limit for their entry into the first asymmetric mitosis. Our reconstruction and analysis of the molecular genetic system that provides the listed events of morphogenesis of a single mechanoreceptor (and the bristle pattern as a whole) revealed its hierarchical organization. The elements of the system are grouped into three modules corresponding to the stages of morphogenesis of the sensory organ: the gene networks “Neurogenesis: prepattern,” “Neurogenesis: determination,” and “Neurogenesis: asymmetric division.” The functioning of the system consistently limits the number of cells that are competent for neural development, firstly to dozens at the level of clusters, and then to a single parental cell within the cluster. The main attribute and connecting link of networks is the complex of proneural achaete-scute (AS-C) genes, the functioning of which at the stage of the separation of PCM is controlled by the central regulatory circuit (CRC). The analysis of the functioning of CRC revealed two phases of its activity that are differing in the time of action and the composition of elements. The cardinal difference of the second phase is the change in the content of the Phyl protein, which is responsible for the degradation of the proneural ASC proteins. This review briefly describes the main stages of mechanoreceptor morphogenesis, the composition and interrelationships of the gene networks supporting them, and also considers the inter- and intracellular mechanisms of PCM segregation.

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The work was carried out within the framework of the budgetary project no. FWNR-2022-0020 “Systems Biology and Bioinformatics: Reconstruction, Analysis, and Modeling of the Structural and Functional Organization and Evolution of Human, Animal, Plant, and Microbial Gene Networks.”

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  1. Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, 630090, Novosibirsk, Russia

    D. P. Furman & T. A. Bukharina

  2. Novosibirsk State University, 630090, Novosibirsk, Russia

    D. P. Furman & T. A. Bukharina

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Furman, D.P., Bukharina, T.A. Genetic Regulation of Morphogenesis of Drosophila melanogaster Mechanoreceptors. Russ J Dev Biol 53, 239–251 (2022). https://doi.org/10.1134/S1062360422040038

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