Abstract
BackgroundIn holometabolous insects such as Drosophila melanogaster, neuroblasts produce an initial population of diverse neurons during embryogenesis and a much larger set of adult-specific neurons during larval life. In the ventral CNS, many of these secondary neuronal lineages differ significantly from one body segment to another, suggesting a role for anteroposterior patterning genes.ResultsHere we systematically characterize the expression pattern and function of the Hox gene Ultrabithorax (Ubx) in all 25 postembryonic lineages. We find that Ubx is expressed in a segment-, lineage-, and hemilineage-specific manner in the thoracic and anterior abdominal segments. When Ubx is removed from neuroblasts via mitotic recombination, neurons in these segments exhibit the morphologies and survival patterns of their anterior thoracic counterparts. Conversely, when Ubx is ectopically expressed in anterior thoracic segments, neurons exhibit complementary posterior transformation phenotypes.ConclusionOur findings demonstrate that Ubx plays a critical role in conferring segment-appropriate morphology and survival on individual neurons in the adult-specific ventral CNS. Moreover, while always conferring spatial identity in some sense, Ubx has been co-opted during evolution for distinct and even opposite functions in different neuronal hemilineages.
Highlights
In holometabolous insects such as Drosophila melanogaster, neuroblasts produce an initial population of diverse neurons during embryogenesis and a much larger set of adult-specific neurons during larval life
The former are in a compact layer next to the neuropil, whereas the latter are in superficial clusters that extend from the larval neuron layer to the surface of the central nervous system (CNS)
The second thoracic segment (T2) lineages that exhibit any Ubx expression are 0, 3, 11, 12, and 19, all of which are in the engrailed domain
Summary
In holometabolous insects such as Drosophila melanogaster, neuroblasts produce an initial population of diverse neurons during embryogenesis and a much larger set of adult-specific neurons during larval life. The insect ventral CNS, like the body as a whole, is built on a plan of repeating segmental units that undergo regional specialization. The neurons of a segmental unit arise from a stereotyped two-dimensional array of 30 uniquely identifiable neural stem cells (neuroblasts, NB) per hemisegment [1,2,3]. These NBs undergo repeated asymmetric divisions, thereby producing a series of ganglion mother cells, GMCs [4], each of which divides to produce a pair of postmitotic daughters [5,6]. Within the thorax particular lineages exhibit segment-specific differences in their cellular composition [10]
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