Male pheromones modulate synaptic transmission at the C. elegans neuromuscular junction in a sexually dimorphic manner
- ShanghaiTech University, China
- The University of Queensland, Australia
- College of Life Science and Technology, China
- Massachusetts General Hospital, United States
- Shanghai Jiao Tong University School of Medicine, China
Abstract
The development of functional synapses in the nervous system is important for animal physiology and behaviors, and its disturbance has been linked with many neurodevelopmental disorders. The synaptic transmission efficacy can be modulated by the environment to accommodate external changes, which is crucial for animal reproduction and survival. However, the underlying plasticity of synaptic transmission remains poorly understood. Here we show that in C. elegans, the male environment increases the hermaphrodite cholinergic transmission at the neuromuscular junction (NMJ), which alters hermaphrodites' locomotion velocity and mating efficiency. We identify that the male-specific pheromones mediate this synaptic transmission modulation effect in a developmental stage-dependent manner. Dissection of the sensory circuits reveals that the AWB chemosensory neurons sense those male pheromones and further transduce the information to NMJ using cGMP signaling. Exposure of hermaphrodites to the male pheromones specifically increases the accumulation of presynaptic CaV2 calcium channels and clustering of postsynaptic acetylcholine receptors at cholinergic synapses of NMJ, which potentiates cholinergic synaptic transmission. Thus, our study demonstrates a circuit mechanism for synaptic modulation and behavioral flexibility by sexual dimorphic pheromones.
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All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided. For other information (such as primers), we already included them in the methods.
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Funding
Basic Research Project from the Science and Technology Commission (19JC1414100)
- Xia-Jing Tong
Shanghai Pujiang Program (18PJ1407600)
- Xia-Jing Tong
Shanghai Pujiang Program (17PJ1405400)
- Qian Li
Shanghai Brain-Intelligence Project from the Science and Technology Commission of Shanghai Municipality (18JC1420302)
- Qian Li
Program for Special Appointment at Shanghai Institutions of Higher Learning (QD2018017)
- Qian Li
Innovative research team of high-level local universities in Shanghai, National Institute of Neurological Disorder and Stroke (NS32196)
- Josh M Kaplan
National Institutes of Health research grant (NEI 1R21EY029450-01)
- Josh M Kaplan
National Health and Medical Research Council (APP1122351)
- Zhi-Tao Hu
National Natural Science Foundation of China (31741054)
- Xia-Jing Tong
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Qian et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Male pheromones modulate synaptic transmission at the C. elegans neuromuscular junction in a sexually dimorphic manner
eLife 10:e67170.
https://doi.org/10.7554/eLife.67170
