The phasmid sensillum is one of the seven classes of sense organs that are common to both sexes in C. In one of his seminal papers, John Sulston described a sexual dimorphism in the phasmid sensilla of adult animals ( Sulston et al., 1980). Here we identify a novel way in which sex-specific neurons are generated in the nervous system: through a direct glia-to-neuron transdifferentiation of sex-shared cells. Generation of sex-specific neurons requires sex-specific cell death ( Sulston et al., 1983) or neurogenesis events resulting from sex differences in the cell division patterns and neurodevelopmental programmes of post-embryonic cell lineages (reviewed in Barr et al., 2018). Sex-specific neurons are primarily involved in controlling distinct aspects of reproductive behaviours, such as egg-laying in the hermaphrodite and mating in the male (reviewed in Emmons, 2018). The second mechanism involves the generation of sex-specific neurons ( Sammut et al., 2015 Sulston and Horvitz, 1977 Sulston et al., 1980). The first involves the acquisition of sexually dimorphic features in sex-shared neurons during sexual maturation, which include changes in terminal gene expression, such as odorant receptors, neurotransmitters and synaptic regulators ( Hilbert and Kim, 2017 Jarrell et al., 2012 Oren-Suissa et al., 2016 Ryan et al., 2014 Serrano-Saiz et al., 2017a Serrano-Saiz et al., 2017b Pereira et al., 2019 Weinberg et al., 2018). Studies in the nematode Caenorhabditis elegans, in which the development and function of neural circuits can be interrogated with single cell resolution, have revealed two general developmental mechanisms underlying sexual dimorphism in the nervous system. The coordinated execution of innate, stereotyped sexual behaviours, such as courtship and mating, requires sexually dimorphic sensory-motor circuits that are genetically specified during development (reviewed in Auer and Benton, 2016 Barr et al., 2018 Yang and Shah, 2014). Our findings reveal programmed transdifferentiation as a developmental mechanism underlying flexibility in innate behaviour. One step of the mating sequence regulated by these neurons is an alternative readjustment movement performed when intromission becomes difficult to achieve. These neurons ensure coordinated backward movement along the mate’s body during mating. We show that the neurons generated are cholinergic, peptidergic, and ciliated putative proprioceptors which integrate into male-specific circuits for copulation. This glia-to-neuron cell fate switch occurs during male sexual maturation under the cell-autonomous control of the sex-determination pathway. We reveal here a novel mechanism by which male-specific neurons are generated in Caenorhabditis elegans through the direct transdifferentiation of sex-shared glial cells. The extent to which nervous systems are sexually dimorphic and the cellular and molecular mechanisms that regulate these differences are only beginning to be understood. Sexually dimorphic behaviours require underlying differences in the nervous system between males and females.
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