Developmental programming modulates olfactory behavior in C. elegans via endogenous RNAi pathways

Sims, Jennie R.; Ow, Maria C.; Nishiguchi, Mailyn A.; Kim, Kyuhyung; Sengupta, Piali; Hall, Sarah E.

doi:10.7554/elife.11642

Cited by 38 publications

(89 citation statements)

References 98 publications

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“…A 25 bp sequence mediates the lag-2 promoter response to TGFβ signaling and the environment Closer inspection of the TRE upstream of lag-2 revealed homology to a cis-acting regulatory sequence named the PD motif, which was characterized in the osm-9 promoter in the context of continuous versus postdauer (PD) development (Sims et al, 2016). The osm-9 PD motif consists of two sequence elements: a DAF-3-binding site (osm-9p-DBS) and a conserved sequence (osm-9p-Cons) that is found in the upstream regulatory regions of ∼1000 genes of the C. elegans genome (Sims et al, 2016).…”

Section: Daf-7/tgfβ Signaling Promotes Lag-2 Expressionmentioning

confidence: 99%

“…The osm-9 PD motif consists of two sequence elements: a DAF-3-binding site (osm-9p-DBS) and a conserved sequence (osm-9p-Cons) that is found in the upstream regulatory regions of ∼1000 genes of the C. elegans genome (Sims et al, 2016). At the lag-2 locus, we identified an 8 bp sequence with homology to the osm-9 promoter that partially overlaps with the osm-9p-DBS at −577 to −570 upstream of the lag-2 ATG (lag-2p-DBS).…”

Section: Daf-7/tgfβ Signaling Promotes Lag-2 Expressionmentioning

confidence: 99%

“…In the osm-9 promoter, DAF-3 SMAD is enriched at the osm-9p-DBS within the PD motif to downregulate osm-9 in ADL neurons of animals that passed through the dauer stage (Sims et al, 2016). To determine whether DAF-3 is enriched at the PD motif elements upstream of lag-2, we performed DAF-3 immunoprecipitation on whole worms using a commercially available antibody followed by quantitative PCR of the lag-2 upstream sequences in the wild type and the daf-3(mgDf90) mutant.…”

Section: Daf-3 Binds Upstream Of Lag-2mentioning

confidence: 99%

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Linking the environment, DAF-7/TGFβ signaling and LAG-2/DSL ligand expression in the germline stem cell niche

Pekar

Hui

et al. 2017

Development

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The developmental accumulation of proliferative germ cells in the C. elegans hermaphrodite is sensitive to the organismal environment. Previously, we found that the TGFβ signaling pathway links the environment and proliferative germ cell accumulation. Neuronal DAF-7/TGFβ causes a DAF-1/TGFβR signaling cascade in the gonadal distal tip cell (DTC), the germline stem cell niche, where it negatively regulates a DAF-3 SMAD and DAF-5 Sno-Ski. LAG-2, a founding DSL ligand family member, is produced in the DTC and activates the GLP-1/Notch receptor on adjacent germ cells to maintain germline stem cell fate. Here, we show that DAF-7/TGFβ signaling promotes expression of lag-2 in the DTC in a daf-3-dependent manner. Using ChIP and one-hybrid assays, we find evidence for direct interaction between DAF-3 and the lag-2 promoter. We further identify a 25 bp DAF-3 binding element required for the DTC lag-2 reporter response to the environment and to DAF-7/TGFβ signaling. Our results implicate DAF-3 repressor complex activity as a key molecular mechanism whereby the environment influences DSL ligand expression in the niche to modulate developmental expansion of the germline stem cell pool.

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Section: Daf-7/tgfβ Signaling Promotes Lag-2 Expressionmentioning

confidence: 99%

Section: Daf-7/tgfβ Signaling Promotes Lag-2 Expressionmentioning

confidence: 99%

Section: Daf-3 Binds Upstream Of Lag-2mentioning

confidence: 99%

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Linking the environment, DAF-7/TGFβ signaling and LAG-2/DSL ligand expression in the germline stem cell niche

Pekar

Hui

et al. 2017

Development

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“…For example, stable downregulation of the guanylyl cyclase gene odr-1 in AWC neurons is required for experiencedependent olfactory adaptation to the odorant butanone, and is dependent upon MUT-7 and NRDE-3-mediated heterochromatin formation at the odr-1 locus (Juang et al 2013). Similarly, our recent work has shown that downregulation of the osm-9 TRPV channel gene in ADL neurons of animals that passed through the dauer stage is dependent upon a majority of the Mutator proteins and NRDE-3 AGO, resulting in altered responses to ascr#3 in adults (Sims et al 2016).…”

Section: Rnai Is Required In Neurons For Behavioral Adaptation To Envmentioning

confidence: 73%

“…ADL-and ASI-specific mut-16 rescue constructs were described previously (Sims et al 2016). Rab-3p::mut-16:: gfp, trx-1p::mut-16::gfp, unc-130p::mut-16::gfp, gpa-4p:: mut-16::gfp, and sre-1p::mut-16::gfp were cloned into the TOPO-XL (Life Technologies) and injected into mut-16(pk710) at a concentration of 8 ng/ml.…”

Section: Mut-16 Rescuesmentioning

confidence: 99%

Endogenous RNAi Pathways Are Required in Neurons for Dauer Formation in Caenorhabditis elegans

Bharadwaj¹,

Hall

2017

Genetics

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Animals can adapt to unfavorable environments through changes in physiology or behavior. In the nematode, Caenorhabditis elegans, environmental conditions perceived early in development determine whether the animal enters either the reproductive cycle, or enters into an alternative diapause stage named dauer. Here, we show that endogenous RNAi pathways play a role in dauer formation in crowding (high pheromone), starvation, and high temperature conditions. Disruption of the Mutator proteins or the nuclear Argonaute CSR-1 result in differential dauer-deficient phenotypes that are dependent upon the experienced environmental stress. We provide evidence that the RNAi pathways function in chemosensory neurons for dauer formation, upstream of the TGF-b and insulin signaling pathways. In addition, we show that Mutator MUT-16 expression in a subset of individual pheromone-sensing neurons is sufficient for dauer formation in high pheromone conditions, but not in starvation or high temperature conditions. Furthermore, we also show that MUT-16 and CSR-1 are required for expression of a subset of G proteins with functions in the detection of pheromone components. Together, our data suggest a model where Mutator-amplified siRNAs that associate with the CSR-1 pathway promote expression of genes required for the detection and signaling of environmental conditions to regulate development and behavior in C. elegans. This study highlights a mechanism whereby RNAi pathways mediate the link between environmental stress and adaptive phenotypic plasticity in animals.

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Estimating eDNA shedding and decay rates for muskellunge in early stages of development

2023

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Estimating population size and species distribution is essential for fisheries management and conservation. Traditionally, estimates rely on live-capture and visual surveys; however, these approaches are challenging for low density or elusive species and sensitive habitats. Environmental DNA (eDNA) has shown potential to improve fisheries management, offering a sensitive tool for species detection while reducing some of the unintended harm, uncertainties, and cost of traditional approaches. For eDNA to be incorporated into quantitative population estimates, variability in factors such as DNA shedding and decay must be understood. We assess shedding and decay rates for three developmental stages of muskellunge (Esox masquinongy), a recreational species of social and economic importance and an apex predator of conservation priority in the St. Lawrence River. By housing fish at different biomass levels, we attempt to assess how crowding, and underlying behavioral and/or metabolic responses, affects shedding and decay. Additionally, we collected water from spawning bays and compared eDNA detections to live-capture data. Total eDNA shedding rates for muskellunge were similar to values reported in previous studies of freshwater fishes and ranged from 9.92 × 10 3 copies/h/fish for larvae to 1.32 × 10 6 copies/h/fish for juveniles. Adjusting shedding rates for fish mass revealed no significant difference between larvae and juveniles. eDNA decay rates varied between life stages and experimental aquaria, with coefficients ranging from 0.064 to 0.259. We were unable to detect eDNA from hardened embryos even at high density. Muskellunge DNA was quantified in over 27% of samples from spawning bays, including bays where muskellunge were not captured with traditional approaches. The recovery of muskellunge eDNA in quantifiable levels, often in the absence of live capture, highlights the potential for eDNA approaches to supplement muskellunge monitoring and management. eDNA shedding and decay rates estimated here may also aid in interpretation of future data.

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Developmental programming modulates olfactory behavior in C. elegans via endogenous RNAi pathways

Cited by 38 publications

References 98 publications

Linking the environment, DAF-7/TGFβ signaling and LAG-2/DSL ligand expression in the germline stem cell niche

Linking the environment, DAF-7/TGFβ signaling and LAG-2/DSL ligand expression in the germline stem cell niche

Endogenous RNAi Pathways Are Required in Neurons for Dauer Formation in Caenorhabditis elegans

Estimating eDNA shedding and decay rates for muskellunge in early stages of development

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