GCY-20 signaling controls suppression of Caenorhabditis elegans egg laying by moderate cold

Summary: Organisms sensing environmental cues and internal states and integrating the sensory information to control fecundity are essential for survival and proliferation. The present study finds that a moderate cold temperature of 11°C reduces egg laying in Caenorhabditis elegans. ASEL and AWC neu...

Full description

Bibliographic Details
Main Authors: Rong Li, Yu Xu, Xin Wen, Yuan-Hua Chen, Ping-Zhou Wang, Jia-Lu Zhao, Piao-Ping Wu, Jing-Jing Wu, Hui Liu, Jia-Hao Huang, Si-Jia Li, Zheng-Xing Wu
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124724000366
_version_ 1797291743069077504
author Rong Li
Yu Xu
Xin Wen
Yuan-Hua Chen
Ping-Zhou Wang
Jia-Lu Zhao
Piao-Ping Wu
Jing-Jing Wu
Hui Liu
Jia-Hao Huang
Si-Jia Li
Zheng-Xing Wu
author_facet Rong Li
Yu Xu
Xin Wen
Yuan-Hua Chen
Ping-Zhou Wang
Jia-Lu Zhao
Piao-Ping Wu
Jing-Jing Wu
Hui Liu
Jia-Hao Huang
Si-Jia Li
Zheng-Xing Wu
author_sort Rong Li
collection DOAJ
description Summary: Organisms sensing environmental cues and internal states and integrating the sensory information to control fecundity are essential for survival and proliferation. The present study finds that a moderate cold temperature of 11°C reduces egg laying in Caenorhabditis elegans. ASEL and AWC neurons sense the cold via GCY-20 signaling and act antagonistically on egg laying through the ASEL and AWC/AIA/HSN circuits. Upon cold stimulation, ASEL and AWC release glutamate to activate and inhibit AIA interneurons by acting on highly and lowly sensitive ionotropic GLR-2 and GLC-3 receptors, respectively. AIA inhibits HSN motor neuron activity via acetylcholinergic ACR-14 receptor signaling and suppresses egg laying. Thus, ASEL and AWC initiate and reduce the cold suppression of egg laying. ASEL’s action on AIA and egg laying dominates AWC’s action. The biased opposite actions of these neurons on egg laying provide animals with a precise adaptation of reproductive behavior to environmental temperatures.
first_indexed 2024-03-07T19:42:08Z
format Article
id doaj.art-030e837c4b374e62ae14dc2b4b052e25
institution Directory Open Access Journal
issn 2211-1247
language English
last_indexed 2024-03-07T19:42:08Z
publishDate 2024-02-01
publisher Elsevier
record_format Article
series Cell Reports
spelling doaj.art-030e837c4b374e62ae14dc2b4b052e252024-02-29T05:18:43ZengElsevierCell Reports2211-12472024-02-01432113708GCY-20 signaling controls suppression of Caenorhabditis elegans egg laying by moderate coldRong Li0Yu Xu1Xin Wen2Yuan-Hua Chen3Ping-Zhou Wang4Jia-Lu Zhao5Piao-Ping Wu6Jing-Jing Wu7Hui Liu8Jia-Hao Huang9Si-Jia Li10Zheng-Xing Wu11Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaCollege of Life Science, Henan Agricultural University, Zhengzhou, Henan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaKey Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, China; Corresponding authorSummary: Organisms sensing environmental cues and internal states and integrating the sensory information to control fecundity are essential for survival and proliferation. The present study finds that a moderate cold temperature of 11°C reduces egg laying in Caenorhabditis elegans. ASEL and AWC neurons sense the cold via GCY-20 signaling and act antagonistically on egg laying through the ASEL and AWC/AIA/HSN circuits. Upon cold stimulation, ASEL and AWC release glutamate to activate and inhibit AIA interneurons by acting on highly and lowly sensitive ionotropic GLR-2 and GLC-3 receptors, respectively. AIA inhibits HSN motor neuron activity via acetylcholinergic ACR-14 receptor signaling and suppresses egg laying. Thus, ASEL and AWC initiate and reduce the cold suppression of egg laying. ASEL’s action on AIA and egg laying dominates AWC’s action. The biased opposite actions of these neurons on egg laying provide animals with a precise adaptation of reproductive behavior to environmental temperatures.http://www.sciencedirect.com/science/article/pii/S2211124724000366CP: Neuroscience
spellingShingle Rong Li
Yu Xu
Xin Wen
Yuan-Hua Chen
Ping-Zhou Wang
Jia-Lu Zhao
Piao-Ping Wu
Jing-Jing Wu
Hui Liu
Jia-Hao Huang
Si-Jia Li
Zheng-Xing Wu
GCY-20 signaling controls suppression of Caenorhabditis elegans egg laying by moderate cold
Cell Reports
CP: Neuroscience
title GCY-20 signaling controls suppression of Caenorhabditis elegans egg laying by moderate cold
title_full GCY-20 signaling controls suppression of Caenorhabditis elegans egg laying by moderate cold
title_fullStr GCY-20 signaling controls suppression of Caenorhabditis elegans egg laying by moderate cold
title_full_unstemmed GCY-20 signaling controls suppression of Caenorhabditis elegans egg laying by moderate cold
title_short GCY-20 signaling controls suppression of Caenorhabditis elegans egg laying by moderate cold
title_sort gcy 20 signaling controls suppression of caenorhabditis elegans egg laying by moderate cold
topic CP: Neuroscience
url http://www.sciencedirect.com/science/article/pii/S2211124724000366
work_keys_str_mv AT rongli gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT yuxu gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT xinwen gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT yuanhuachen gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT pingzhouwang gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT jialuzhao gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT piaopingwu gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT jingjingwu gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT huiliu gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT jiahaohuang gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT sijiali gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold
AT zhengxingwu gcy20signalingcontrolssuppressionofcaenorhabditiselegansegglayingbymoderatecold