Nematode nuclear receptors as integrators of sensory information

Sural, Surojit; Hobert, Oliver

doi:10.1016/j.cub.2021.07.019

Cited by 20 publications

(19 citation statements)

References 32 publications

(37 reference statements)

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“…Being consistent with this idea is the significant expansion of the GPCR family, which are the chemoreceptors that detect not only external odors and chemicals but also internal peptides (46, 47). A recent study hypothesized that the nuclear hormone receptors (NHRs) may control the expression of GPCRs for the integration of sensory information in sensory neurons (48). Interestingly, we found that the NHR families were also significantly expanded in C. elegans .…”

Section: Discussionmentioning

confidence: 99%

Dynamic evolution of recently duplicated genes in Caenorhabditis elegans

Lau

Zheng

2022

Preprint

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As a major origin of evolutionary novelties, gene duplication is a widespread phenomenon across species. However, the evolutionary force that determines the fate of duplicate genes is still under debate. Here, we studied the functional evolution of duplicate genes at both macroevolution and microevolution scales using the genomic sequences of eleven Caenorhabditis species and 773 C. elegans wild isolates. We found that compared to older duplicate genes and single-copy genes, recently duplicated gene copies showed rapid turnover, large genetic diversity, and signs of balancing and positive selection within the species. Young duplicate genes have low basal expression restricted to a few tissues but show highly responsive expression towards pathogenic infections. Recently duplicated genes are enriched in chemosensory perception, protein degradation, and innate immunity, implicating their functions in enhancing adaptability to external perturbations. Importantly, we found that young duplicate genes are rarely essential, while old duplicate genes have the same level of essentiality as singletons, suggesting that essentiality develops over a long time. Together, our work in C. elegans demonstrates that natural selection shapes the dynamic evolutionary trajectory of duplicate genes.

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Section: Discussionmentioning

confidence: 99%

Dynamic evolution of recently duplicated genes in Caenorhabditis elegans

Lau

Zheng

2022

Preprint

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“…This observation suggests that, among NHR members, those phylogenetically conserved could have a prevalent role in neuron specification. Alternatively, lack of phenotypes for nematode-specific NHRs could be attributed to more redundant actions among them or to specialized functions in particular neuron types and gene targets as recently suggested ( Sural and Hobert 2021 ).…”

Section: Resultsmentioning

confidence: 95%

Joint actions of diverse transcription factor families establish neuron-type identities and promote enhancer selectivity

et al. 2022

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To systematically investigate the complexity of neuron-specification regulatory networks we performed an RNA interference (RNAi) screen against all 875 transcription factors (TFs) encoded in Caenorhabditis elegans genome and searched for defects in nine different neuron types of the monoaminergic (MA) superclass and two cholinergic motoneurons. We identified 91 TF candidates required for correct generation of these neuron types of which 28 were confirmed by mutant analysis. We found that correct reporter expression in each individual neuron type requires at least nine different TFs. Individual neuron types do not usually share TFs involved in their specification but share a common pattern of TFs belonging to the five most common TF families: Homeodomain (HD), basic Helix Loop Helix (bHLH), Zinc Finger (ZF), Basic Leucine Zipper Domain (bZIP) and Nuclear Hormone Receptors (NHR). HD TF members are over-represented, supporting a key role for this family in the establishment of neuronal identities. We found a similar TF family distribution for TF mutants with assigned phenotypes in any neuron type in C. elegans, Drosophila or mouse. In addition, we studied terminal differentiation complexity focusing on the dopaminergic terminal regulatory program. We found two HD TFs (UNC-62 and VAB-3) that work together with known dopaminergic terminal selectors (AST-1, CEH-43, CEH-20). Combined TF binding sites for these five TFs constitute a cis-regulatory signature enriched in the regulatory regions of dopaminergic effector genes. Our results provide new insights on neuron-type regulatory programs in C. elegans that could help better understand neuron specification and evolution of neuron types.

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“…However, we noted that the expression of several neuropeptide genes and in particular, multiple transcription factors was significantly altered in PD vs control adults (Figure 5D, File S2). Affected transcription factors belong to multiple subfamilies including the greatly expanded nuclear hormone receptor family, members of which are predicted to be co-expressed in sensory neurons along with putative chemoreceptor GPCRs, and which have been suggested to act as receptors for external and internal cues (Sural and Hobert, 2021; Taylor et al, 2021). Together, these results indicate that passage through the dauer stage alters the expression of genes from multiple families, and that the expression of genes in individual sensory neurons such as AWA is also affected.…”

Section: Resultsmentioning

confidence: 99%

Developmental history modulates adult olfactory behavioral preferences via regulation of chemoreceptor expression inC. elegans

Kyani-Rogers

Philbrook

McLachlan

et al. 2022

Preprint

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Developmental experiences play critical roles in shaping adult physiology and behavior. We and others previously showed that adult C. elegans which transiently experienced dauer arrest during development (PD: post-dauer) exhibit distinct gene expression profiles as compared to control adults which bypassed the dauer stage. In particular, the expression patterns of subsets of chemoreceptor genes are markedly altered in PD adults. Whether altered chemoreceptor levels drive behavioral plasticity in PD adults is unknown. Here we show that PD adults exhibit enhanced attraction to a panel of food-related attractive volatile odorants including the bacterially-produced chemical diacetyl. Diacetyl-evoked responses in the AWA olfactory neuron pair are increased in both dauer larvae and PD adults, and we find that these increased responses are correlated with upregulation of the diacetyl receptor ODR-10 in AWA likely via both transcriptional and post-transcriptional mechanisms. We show that transcriptional upregulation of odr-10 expression in dauer larvae is in part mediated by the DAF-16 FOXO transcription factor. Via transcriptional profiling of sorted populations of AWA neurons from control and PD adults, we further show that the expression of a subset of additional chemoreceptor genes in AWA is regulated similarly to odr-10 in PD animals. Our results suggest that developmental experiences may be encoded at the level of olfactory receptor regulation, and provide a simple mechanism by which C. elegans is able to precisely modulate its behavioral preferences as a function of its current and past experiences.

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Nematode nuclear receptors as integrators of sensory information

Cited by 20 publications

References 32 publications

Dynamic evolution of recently duplicated genes in Caenorhabditis elegans

Dynamic evolution of recently duplicated genes in Caenorhabditis elegans

Joint actions of diverse transcription factor families establish neuron-type identities and promote enhancer selectivity

Developmental history modulates adult olfactory behavioral preferences via regulation of chemoreceptor expression inC. elegans

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