Abstract
BackgroundDeveloping neurons form dendritic trees with cell type-specific patterns of growth, branching and targeting. Dendrites of Drosophila peripheral sensory neurons have emerged as a premier genetic model, though the molecular mechanisms that underlie and regulate their morphogenesis remain incompletely understood. Still less is known about this process in central neurons and the extent to which central and peripheral dendrites share common organisational principles and molecular features. To address these issues, we have carried out two comparable gain-of-function screens for genes that influence dendrite morphologies in peripheral dendritic arborisation (da) neurons and central RP2 motor neurons.ResultsWe found 35 unique loci that influenced da neuron dendrites, including five previously shown as required for da dendrite patterning. Several phenotypes were class-specific and many resembled those of known mutants, suggesting that genes identified in this study may converge with and extend known molecular pathways for dendrite development in da neurons. The second screen used a novel technique for cell-autonomous gene misexpression in RP2 motor neurons. We found 51 unique loci affecting RP2 dendrite morphology, 84% expressed in the central nervous system. The phenotypic classes from both screens demonstrate that gene misexpression can affect specific aspects of dendritic development, such as growth, branching and targeting. We demonstrate that these processes are genetically separable. Targeting phenotypes were specific to the RP2 screen, and we propose that dendrites in the central nervous system are targeted to territories defined by Cartesian co-ordinates along the antero-posterior and the medio-lateral axes of the central neuropile. Comparisons between the screens suggest that the dendrites of peripheral da and central RP2 neurons are shaped by regulatory programs that only partially overlap. We focused on one common candidate pathway controlled by the ecdysone receptor, and found that it promotes branching and growth of developing da neuron dendrites, but a role in RP2 dendrite development during embryonic and early larval stages was not apparent.ConclusionWe identified commonalities (for example, growth and branching) and distinctions (for example, targeting and ecdysone response) in the molecular and organizational framework that underlies dendrite development of peripheral and central neurons.
Highlights
Developing neurons form dendritic trees with cell type-specific patterns of growth, branching and targeting
A gain-of-function screen for genes that influence the morphologies of peripheral neuron dendrites Screening in embryos To identify genes affecting da dendrite morphogenesis, we focused on da neurons of the dorsal peripheral nervous system (PNS) cluster, visualised selectively by GAL4109(2)80 and a transgene encoding a membrane-targeted green fluorescent protein (GFP) reporter, UAS-mCD8::GFP [15,21]
We crossed each of 141 Gene Search (GS) expression lines into this background and assayed in late stage 17 Drosophila embryos the effects on: overall PNS integrity; the number and position of GFP-positive cell bodies in the dorsal cluster; the extent of dendrite outgrowth of dorsal cluster da neurons; and their pattern of branching
Summary
Developing neurons form dendritic trees with cell type-specific patterns of growth, branching and targeting. Dendrites of Drosophila peripheral sensory neurons have emerged as a premier genetic model, though the molecular mechanisms that underlie and regulate their morphogenesis remain incompletely understood. Still less is known about this process in central neurons and the extent to which central and peripheral dendrites share common organisational principles and molecular features. Dendrites are the primary sites for the reception of sensory and synaptic input to neurons This input is influenced by the architecture of the dendritic tree [1,2] and by the targeting of dendrites into appropriate territories [3,4]. Within the peripheral nervous system (PNS) of Drosophila, studies to date indicate that genetic programs regulate the outgrowth, size, branching pattern and orientation of dendritic arborisation (da) sensory neurons [2,6]. Dendrites in the CNS differ from PNS sensory neuron dendrites in that they are not specialised for the reception of particular external stimuli [17,18,19,20] but instead form connections with presynaptic terminals of other neurons, and develop in a highly complex environment, the central neuropile
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