Abstract
A core principle of nervous system organization is the diversification of neuron classes into subclasses that share large sets of features but differ in select traits. We describe here a molecular mechanism necessary for motor neurons to acquire subclass-specific traits in the nematode Caenorhabditis elegans. Cholinergic motor neuron classes of the ventral nerve cord can be subdivided into subclasses along the anterior-posterior (A-P) axis based on synaptic connectivity patterns and molecular features. The conserved COE-type terminal selector UNC-3 not only controls the expression of traits shared by all members of a neuron class, but is also required for subclass-specific traits expressed along the A-P axis. UNC-3, which is not regionally restricted, requires region-specific cofactors in the form of Hox proteins to co-activate subclass-specific effector genes in post-mitotic motor neurons. This intersectional gene regulatory principle for neuronal subclass diversification may be conserved from nematodes to mice.
Highlights
An obligatory first step toward understanding nervous system development, function and evolution is the cataloguing of its individual building blocks
We undertook a candidate gene approach examining the precise expression pattern of terminal differentiation genes that code for neurotransmitter receptors, signaling proteins or ion channels that were previously reported to be expressed in motor neurons (MNs) or that we identified in surveys of expression patterns of specific gene families
We conclude that Hox genes control the expression of subclass-specific genes within the DA neuronal class. Consistent with their subclass-specific expression, we find that Hox genes are required for subclass-specific effector gene expression in post-embryonically generated MN classes, such as the VA class (Figure 1B). egl-5 is expressed in the VA12 neuron and not in other VA neurons along the ventral nerve cord (VNC), and we find that the VA12-expressed genes mig-13 and flp18 are under the control of egl-5 (Figure 4C–E)
Summary
An obligatory first step toward understanding nervous system development, function and evolution is the cataloguing of its individual building blocks. Such cataloguing involves the classification of neurons into classes and the subdivision of classes into more refined subclasses. Neurons have been grouped into specific classes and subclasses based on anatomical and electrophysiological features. Neurons can be grouped together based on a number of shared molecular, functional and anatomical traits, but can be further subdivided into individual subclasses based on subclass-specific traits.
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