Abstract
BackgroundDuring the development of the central nervous system (CNS) of Drosophila, neuronal stem cells, the neuroblasts (NBs), first generate a set of highly diverse neurons, the primary neurons that mature to control larval behavior, and then more homogeneous sets of neurons that show delayed maturation and are primarily used in the adult. These latter, 'secondary' neurons show a complex pattern of expression of broad, which encodes a transcription factor usually associated with metamorphosis, where it acts as a key regulator in the transitions from larva and pupa.ResultsThe Broad-Z3 (Br-Z3) isoform appears transiently in most central neurons during embryogenesis, but persists in a subset of these cells through most of larval growth. Some of the latter are embryonic-born secondary neurons, whose development is arrested until the start of metamorphosis. However, the vast bulk of the secondary neurons are generated during larval growth and bromodeoxyuridine incorporation shows that they begin expressing Br-Z3 about 7 hours after their birth, approximately the time that they have finished outgrowth to their initial targets. By the start of metamorphosis, the oldest secondary neurons have turned off Br-Z3 expression, while the remainder, with the exception of the very youngest, maintain Br-Z3 while they are interacting with potential partners in preparation for neurite elaboration. That Br-Z3 may be involved in early sprouting is suggested by ectopically expressing this isoform in remodeling primary neurons, which do not normally express Br-Z3. These cells now sprout into ectopic locations. The expression of Br-Z3 is transient and seen in all interneurons, but two other isoforms, Br-Z4 and Br-Z1, show a more selective expression. Analysis of MARCM clones shows that the Br-Z4 isoform is expressed by neurons in virtually all lineages, but only in those cells born during a window during the transition from the second to the third larval instar. Br-Z4 expression is then maintained in this temporal cohort of cells into the adult.ConclusionThese data show the potential for diverse functions of Broad within the developing CNS. The Br-Z3 isoform appears in all interneurons, but not motoneurons, when they first begin to interact with potential targets. Its function during this early sorting phase needs to be defined. Two other Broad isoforms, by contrast, are stably expressed in cohorts of neurons in all lineages and are the first examples of persisting molecular 'time-stamps' for Drosophila postembryonic neurons.
Highlights
During the development of the central nervous system (CNS) of Drosophila, neuronal stem cells, the neuroblasts (NBs), first generate a set of highly diverse neurons, the primary neurons that mature to control larval behavior, and more homogeneous sets of neurons that show delayed maturation and are primarily used in the adult
The sequential generation of distinct populations of neurons is a common feature across all taxa. Nowhere is this more striking than in the development of the nervous system of insects having complete metamorphosis, such as Drosophila, where the central nervous system (CNS) must deal sequentially with the behavior of two radically different stages, the larva and the adult. This dichotomy is reflected in the proliferative activity of the neuronal stem cells (neuroblasts (NBs)) that produce the neurons for both larval and adult versions of the CNS
IFmigmuurneo1cytochemistry showing staining with a monoclonal antibody (MAb) directed against the core region of the Broad transcription factor Immunocytochemistry showing staining with a MAb directed against the core region of the Broad transcription factor. (A, B) Whole mounts of Drosophila (A) and Manduca (B) embryos just prior to hatching
Summary
During the development of the central nervous system (CNS) of Drosophila, neuronal stem cells, the neuroblasts (NBs), first generate a set of highly diverse neurons, the primary neurons that mature to control larval behavior, and more homogeneous sets of neurons that show delayed maturation and are primarily used in the adult These latter, 'secondary' neurons show a complex pattern of expression of broad, which encodes a transcription factor usually associated with metamorphosis, where it acts as a key regulator in the transitions from larva and pupa. The sequential generation of distinct populations of neurons is a common feature across all taxa (for example, [13]) Nowhere is this more striking than in the development of the nervous system of insects having complete metamorphosis, such as Drosophila, where the central nervous system (CNS) must deal sequentially with the behavior of two radically different stages, the larva and the adult. These transcription factors encode different identities within the lineage and underlie the diversity of early neuronal types [7,8]
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