scholarly journals Distinct neuropeptide-receptor modules regulate a sex-specific behavioral response to a pheromone

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Douglas K. Reilly ◽  
Emily J. McGlame ◽  
Elke Vandewyer ◽  
Annalise N. Robidoux ◽  
Caroline S. Muirhead ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Behavioral Response ◽  
Receptor Expression ◽  
Specific Response ◽  
Sensory Cues ◽  
Animal Kingdom ◽  
Dioecious Species ◽  
C Elegans ◽  
Biochemical Studies ◽  
Male Specific

AbstractDioecious species are a hallmark of the animal kingdom, with opposing sexes responding differently to identical sensory cues. Here, we study the response of C. elegans to the small-molecule pheromone, ascr#8, which elicits opposing behavioral valences in each sex. We identify a novel neuropeptide-neuropeptide receptor (NP/NPR) module that is active in males, but not in hermaphrodites. Using a novel paradigm of neuropeptide rescue that we established, we leverage bacterial expression of individual peptides to rescue the sex-specific response to ascr#8. Concurrent biochemical studies confirmed individual FLP-3 peptides differentially activate two divergent receptors, NPR-10 and FRPR-16. Interestingly, the two of the peptides that rescued behavior in our feeding paradigm are related through a conserved threonine, suggesting that a specific NP/NPR combination sets a male state, driving the correct behavioral valence of the ascr#8 response. Receptor expression within pre-motor neurons reveals novel coordination of male-specific and core locomotory circuitries.

scholarly journals Distinct Neuropeptide-Receptor Modules Regulate a Sex-Specific Behavioral Response to a Pheromone

2020 ◽  
Author(s):  
Douglas K. Reilly ◽  
Emily J. McGlame ◽  
Elke Vandewyer ◽  
Annalise M. Robidoux ◽  
Haylea T. Northcott ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Behavioral Response ◽  
Receptor Expression ◽  
Specific Response ◽  
Sensory Cues ◽  
Animal Kingdom ◽  
Dioecious Species ◽  
C Elegans ◽  
Biochemical Studies ◽  
Male Specific

AbstractDioecious species are a hallmark of the animal kingdom, with opposing sexes responding differently to identical sensory cues. Here, we study the response of C. elegans’ to the small-molecule pheromone, ascr#8, which elicits opposing behavioral valences in each sex. We identify a novel neuropeptide-neuropeptide receptor (NP/NPR) module that is active in males, but not in hermaphrodites. Using a novel paradigm of neuropeptide rescue that we established, we leverage bacterial expression of individual peptides to rescue the sex-specific response to ascr#8. Concurrent biochemical studies confirmed individual FLP-3 peptides differentially activate two divergent receptors, NPR-10 and FRPR-16. Interestingly, the two of the peptides that rescued behavior in our feeding paradigm are related through a conserved threonine, suggesting that a specific NP/NPR combination sets a male state, driving the correct behavioral valence of the ascr#8 response. Receptor expression within pre-motor neurons reveals novel coordination of male-specific and core locomotory circuitries.

scholarly journals Transcriptomic profiling of sex-specific olfactory neurons reveals subset-specific receptor expression in C. elegans

2021 ◽  
Author(s):  
Douglas K Reilly ◽  
Erich M Schwarz ◽  
Caroline S Muirhead ◽  
Annalise N Robidoux ◽  
Igor Antoscheckin ◽  
...  
Keyword(s):  
Neural Coding ◽  
Radial Symmetry ◽  
Receptor Expression ◽  
Double Knockout ◽  
Olfactory Neurons ◽  
Transcriptomic Profiling ◽  
C Elegans ◽  
Expression Of Genes ◽  
Gfp Reporter ◽  
Male Specific

The nematode Caenorhabditis elegans utilizes chemosensation to navigate an ever-changing environment for its survival. A class of secreted small-molecule pheromones, termed ascarosides, play an important role in olfactory perception by affecting a host of biological function ranging from development to behavior. The ascaroside ascr#8 mediates sex-specific behaviors, driving avoidance in hermaphrodites and attraction in males. Males sense ascr#8 via the ciliated male-specific cephalic sensory (CEM) neurons, which exhibit radial symmetry along dorsal-ventral and left-right axes. Calcium imaging studies suggest a complex neural coding mechanism that translates stochastic physiological responses in these neurons to reliable behavioral outputs. To test the hypothesis that the neurophysiological complexity arises from differential expression of genes within subsets of these neurons, we performed cell-specific transcriptomic profiling of these sensory neurons. Expression profiling revealed between 20 and 639 genes enriched at least two-fold per CEM neuron and identified multiple G protein coupled receptor (GPCR) candidates enriched in non-overlapping subsets of CEM neurons. GFP reporter analysis confirmed that RNA expression of two of the GPCR genes, srw-97 and dmsr-12, is enriched in specific subsets of the CEM neurons. Single CRISPR-Cas9 knockouts of either srw-97 or dmsr-12 resulted in partial defects, while a double knockout of both srw-97 and dmsr-12 completely abolished the attractive response to ascr#8, suggesting that each receptor acts in a non-redundant manner in discrete olfactory neurons. Together, our results suggest that the evolutionarily distinct GPCRs SRW-97 and DMSR-12 act to facilitate male-specific sensation of ascr#8 through discrete subsets of CEM neurons.

Why Are There Males in the Hermaphroditic Species Caenorhabditis elegans?

Genetics ◽  
2002 ◽  
Vol 160 (3) ◽  
pp. 983-994
Author(s):  
J R Chasnov ◽  
King L Chow
Keyword(s):  
Caenorhabditis Elegans ◽  
Low Frequency ◽  
Genetic System ◽  
Genetic Mutation ◽  
Male Mating ◽  
Theoretical Argument ◽  
Dioecious Species ◽  
C Elegans ◽  
Free Living Nematode ◽  
Male Specific

Abstract The free-living nematode worm Caenorhabditis elegans reproduces primarily as a self-fertilizing hermaphrodite, yet males are maintained in wild-type populations at low frequency. To determine the role of males in C. elegans, we develop a mathematical model for the genetic system of hermaphrodites that can either self-fertilize or be fertilized by males and we perform laboratory observations and experiments on both C. elegans and a related dioecious species C. remanei. We show that the mating efficiency of C. elegans is poor compared to a dioecious species and that C. elegans males are more attracted to C. remanei females than they are to their conspecific hermaphrodites. We postulate that a genetic mutation occurred during the evolution of C. elegans hermaphrodites, resulting in the loss of an attracting sex pheromone present in the ancestor of both C. elegans and C. remanei. Our findings suggest that males are maintained in C. elegans because of the particular genetic system inherited from its dioecious ancestor and because of nonadaptive spontaneous nondisjunction of sex chromosomes, which occurs during meiosis in the hermaphrodite. A theoretical argument shows that the low frequency of male mating observed in C. elegans can support male-specific genes against mutational degeneration. This results in the continuing presence of functional males in a 99.9% hermaphroditic species in which outcrossing is disadvantageous to hermaphrodites.

scholarly journals Timing mechanism of sexually dimorphic nervous system differentiation

2018 ◽  
Author(s):  
Laura Pereira ◽  
Florian Aeschimann ◽  
Chen Wang ◽  
Hannah Lawson ◽  
Esther Serrano-Saiz ◽  
...  
Keyword(s):  
Nervous System ◽  
Transcription Factors ◽  
Sexual Maturation ◽  
Sexual Differentiation ◽  
Rna Binding ◽  
Receptor Expression ◽  
Sexually Dimorphic ◽  
Neuron Type ◽  
C Elegans ◽  
Male Specific

ABSTRACTIn all animals, sexual differentiation of somatic tissue is precisely timed, yet the molecular mechanisms that control the timing of sexual differentiation, particularly in the brain, are poorly understood. We have used sexually dimorphic molecular, anatomical and behavioral features of the C. elegans nervous system to decipher a regulatory pathway that controls the precise timing of sexual differentiation. We find that the sexually dimorphic differentiation of postmitotic neurons in the male nervous system is abrogated in animals that carry a mutation in the miRNA let-7 and prematurely executed in animals either lacking the let-7 inhibitor lin-28, or the direct let-7 target lin-41, an RNA-binding, posttranscriptional regulator. We show that an isoform of a phylogenetically conserved transcription factor, lin-29a, is a critical target of LIN-41 in controlling sexual maturation of sex-shared neurons. lin-29a is expressed in a male-specific manner in a subset of sex-shared neurons at the onset of sexual maturation. lin-29a acts cell-autonomously in these neurons to control the expression of sexually dimorphic neurotransmitter switches, sensory receptor expression, neurite anatomy and connectivity, and locomotor behavior. lin-29a is not only required but also sufficient to impose male-specific features at earlier stages of development and in the opposite sex. The temporal, sexual and spatial specificity of lin-29a expression is controlled intersectionally through the lin-28/let-7/lin-41 heterochronic pathway, sex chromosome configuration and neuron type-specific terminal selector transcription factors. Two Doublesex-like transcription factors represent additional neuron-type specific targets of LIN-41 and are regulated in a similar intersectional manner, indicating the existence of modular outputs downstream of the heterochronic pathway. In conclusion, we have provided insights into the molecular logic of the timing of sexual differentiation in the C. elegans nervous system. Remarkably, the lin28/let7 axis also controls the timing of sexual differentiation in mice and humans thereby hinting toward a striking universality of the control mechanisms of sexual differentiation.

The C. elegans homeodomain gene unc-42 regulates chemosensory and glutamate receptor expression

Development ◽  
1999 ◽  
Vol 126 (10) ◽  
pp. 2241-2251 ◽  
Author(s):  
R. Baran ◽  
R. Aronoff ◽  
G. Garriga
Keyword(s):  
Axon Guidance ◽  
Cell Fate ◽  
Glutamate Receptor ◽  
Sensory Neurons ◽  
Motor Neurons ◽  
Neural Circuits ◽  
Receptor Expression ◽  
Homeodomain Protein ◽  
Sensory Stimuli ◽  
C Elegans

Genes that specify cell fate can influence multiple aspects of neuronal differentiation, including axon guidance, target selection and synapse formation. Mutations in the unc-42 gene disrupt axon guidance along the C. elegans ventral nerve cord and cause distinct functional defects in sensory-locomotory neural circuits. Here we show that unc-42 encodes a novel homeodomain protein that specifies the fate of three classes of neurons in the Caenorhabditis elegans nervous system: the ASH polymodal sensory neurons, the AVA, AVD and AVE interneurons that mediate repulsive sensory stimuli to the nematode head and anterior body, and a subset of motor neurons that innervate head and body-wall muscles. unc-42 is required for the expression of cell-surface receptors that are essential for the mature function of these neurons. In mutant animals, the ASH sensory neurons fail to express SRA-6 and SRB-6, putative chemosensory receptors. The AVA, AVD and AVE interneurons and RME and RMD motor neurons of unc-42 mutants similarly fail to express the GLR-1 glutamate receptor. These results show that unc-42 performs an essential role in defining neuron identity and contributes to the establishment of neural circuits in C. elegans by regulating the transcription of glutamate and chemosensory receptor genes.

Differential responses of Aplysia siphon motor neurons and interneurons to tail and mantle stimuli: implications for behavioral response specificity

1996 ◽  
Vol 76 (6) ◽  
pp. 3895-3909 ◽  
Author(s):  
X. Fang ◽  
G. A. Clark
Keyword(s):  
Motor Neurons ◽  
Behavioral Response ◽  
Neural Mechanisms ◽  
Specific Response ◽  
Differential Activation ◽  
Coordinate Regulation ◽  
Common Path ◽  
Forward Bending ◽  
Withdrawal Response ◽  
Response Specificity

1. Tail shock and mantle shock elicit different forms of siphon responses in Aplysia (flaring and backward bending vs. constriction and forward bending, respectively). Moreover, training with these two unconditioned stimuli (USs) in US-alone or classical conditioning paradigms differentially modifies the direction of the response to a siphon tap subsequently presented. As a first step toward addressing neural mechanisms underlying this response specificity, we systematically mapped the central siphon withdrawal circuit to determine which motor neurons and interneurons are differentially engaged by, and potentially modified by, tail and mantle USs. We utilized semi-intact preparations consisting of the intact mantle organs (including the gill and siphon), the tail, and the abdominal and circumesophageal ganglia. USs were delivered either cutaneously through silver wires implanted in the tail and mantle or via suction electrodes to the tail and branchial nerves. 2. We found that one class of central siphon motor neurons, the LFSB cells, was preferentially activated by tail USs, whereas other siphon motor neurons, the LBs cells and RDs cells, were preferentially activated by mantle USs. These motor neurons thus appear to be the final common path for the differential siphon movements to these USs. In addition, because activation of these cells can elicit neuromuscular facilitation and thereby enhance siphon movements, this differential activation may contribute to behavioral response specificity by imposing a specific response bias. 3. L29 interneurons, which both mediate and modulate the siphon withdrawal response, responded preferentially and exhibited synaptic facilitation selectively in response to tail shock USs. In contrast, L34 and the interneuron II network did not show differential activation. Facilitation at L29-LFSB connections following training with tail shock may contribute to tail-directed siphon responses to siphon tap and may thus be an additional mechanism contributing to behavioral response specificity. Possibly, facilitation at other L29 connections could also enhance its modulatory capabilities. 4. The generation of specific response topographies thus appears to involve the coordinate regulation of diverse neuronal elements and multiple mechanisms, which may contribute to different aspects of learning.

scholarly journals A sexually dimorphic neuroendocrine cascade acts through shared sensory neurons to regulate behavior inC. elegans

2018 ◽  
Author(s):  
Zoë A. Hilbert ◽  
Dennis H. Kim
Keyword(s):  
Sexually Dimorphic ◽  
Animal Kingdom ◽  
Specific Expression ◽  
C Elegans ◽  
Pigment Dispersing Factor ◽  
Behavioral Decision ◽  
Specific Effects ◽  
Sexually Dimorphic Expression ◽  
Male Specific ◽  
Dimorphic Expression

ABSTRACTSexually dimorphic behaviors are observed in species across the animal kingdom, however the relative contributions of sex-specific and sex-shared nervous systems to such behaviors are not fully understood. Building on our previous work which described the sexually dimorphic expression of a neuroendocrine ligand, DAF-7, and its role in behavioral decision-making inC. elegans(Hilbert and Kim, 2017), we show here that sex-specific expression ofdaf-7is regulated by another neuroendocrine ligand, Pigment Dispersing Factor (PDF-1), which has previously been implicated in regulating male-specific behavior (Barrios et al., 2012). Our analysis revealed that PDF-1 acts sex- and cell-specifically in the ASJ neurons to regulate the expression ofdaf-7and we show that differences in the expression of the PDFR-1 receptor account for the sex-specific effects of this pathway. Our data suggest that modulation of the sex-shared nervous system by neuroendocrine signaling pathways can play a role in shaping sexually dimorphic behaviors.

The Caenorhabditis elegans odr-2 Gene Encodes a Novel Ly-6-Related Protein Required for Olfaction

Genetics ◽  
2001 ◽  
Vol 157 (1) ◽  
pp. 211-224 ◽  
Author(s):  
Joseph H Chou ◽  
Cornelia I Bargmann ◽  
Piali Sengupta
Keyword(s):  
Caenorhabditis Elegans ◽  
Motor Neurons ◽  
Amino Terminus ◽  
Signaling Proteins ◽  
Related Protein ◽  
Olfactory Neurons ◽  
Unique Role ◽  
C Elegans ◽  
Founding Member ◽  
High Concentrations

Abstract Caenorhabditis elegans odr-2 mutants are defective in the ability to chemotax to odorants that are recognized by the two AWC olfactory neurons. Like many other olfactory mutants, they retain responses to high concentrations of AWC-sensed odors; we show here that these residual responses are caused by the ability of other olfactory neurons (the AWA neurons) to be recruited at high odor concentrations. odr-2 encodes a membrane-associated protein related to the Ly-6 superfamily of GPI-linked signaling proteins and is the founding member of a C. elegans gene family with at least seven other members. Alternative splicing of odr-2 yields three predicted proteins that differ only at the extreme amino terminus. The three isoforms have different promoters, and one isoform may have a unique role in olfaction. An epitope-tagged ODR-2 protein is expressed at high levels in sensory neurons, motor neurons, and interneurons and is enriched in axons. The AWC neurons are superficially normal in their development and structure in odr-2 mutants, but their function is impaired. Our results suggest that ODR-2 may regulate AWC signaling within the neuronal network required for chemotaxis.

Cellular Samurai: katanin and the severing of microtubules

2000 ◽  
Vol 113 (16) ◽  
pp. 2821-2827 ◽  
Author(s):  
L. Quarmby
Keyword(s):  
Epithelial Cells ◽  
Essential Role ◽  
Aaa Atpase ◽  
C Elegans ◽  
Microtubule Severing ◽  
Biochemical Studies ◽  
New Evidence

Recent biochemical studies of the AAA ATPase, katanin, provide a foundation for understanding how microtubules might be severed along their length. These in vitro studies are complemented by a series of recent reports of direct in vivo observation of microtubule breakage, which indicate that the in vitro phenomenon of catalysed microtubule severing is likely to be physiological. There is also new evidence that microtubule severing by katanin is important for the production of non-centrosomal microtubules in cells such as neurons and epithelial cells. Although it has been difficult to establish the role of katanin in mitosis, new genetic evidence indicates that a katanin-like protein, MEI-1, plays an essential role in meiosis in C. elegans. Finally, new proteins involved in the severing of axonemal microtubules have been discovered in the deflagellation system of Chlamydomonas.

Identification Of A Novel Gene Altered In The RQ1 Mutant Strain Affecting Motor Axon Migration In Caenorhabditis Elegans

2021 ◽  
Author(s):  
Haider Z. Naqvi
Keyword(s):  
Caenorhabditis Elegans ◽  
Axon Guidance ◽  
Motor Neurons ◽  
Genetic Background ◽  
Germ Line ◽  
Strong Indication ◽  
Wild Type ◽  
C Elegans ◽  
Novel Gene ◽  
Mutation Region

Novel genetic enhancer screens were conducted targeting mutants involved in the guidance of axons of the DA and DB classes of motor neurons in C. elegans. These mutations are expected in genes that function in parallel to the unc-g/Netrin pathway. The screen was conducted in an unc-5(e53) genetic background and enhancers of the axon guidance defects caused by the absence of UNC-5 were identified. Three mutants were previously identified in the screen called rq1, rq2 and rq3 and two additional mutants called H2-4 and M1-3, were isolated in this study. In order to identify the gene affected by the rq1 mutation, wild-type copies of genes in the mapped rq1 mutation region were injected into the mutants to rescue the phenotypic defects. This is a strong indication that the gene of interest is a novel gene called H04D03.1. Promising results indicate that the H04D03.1 protein also works in germ-line apoptosis.

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