Reimagining pheromone signalling in the model nematode Caenorhabditis elegans

Viney, Mark; Harvey, Simon C.

doi:10.1371/journal.pgen.1007046

Cited by 16 publications

(13 citation statements)

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“…Determining genotype-phenotype relationships is the heart of genetics. Understanding how the relationships between traits, genotypes, and environments are controlled is also crucial to find traits relevant to the evolved context of the species [1][2][3][4][5][6][7]. The identification and characterization of allelic variants associated with complex traits have been a major challenge in plant and animal breeding as well as disease genetics.…”

Section: Introductionmentioning

confidence: 99%

A multi-parent recombinant inbred line population of C. elegans allows identification of novel QTLs for complex life history traits

Snoek¹,

Volkers²,

Nijveen³

et al. 2019

BMC Biol

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Background: The nematode Caenorhabditis elegans has been extensively used to explore the relationships between complex traits, genotypes, and environments. Complex traits can vary across different genotypes of a species, and the genetic regulators of trait variation can be mapped on the genome using quantitative trait locus (QTL) analysis of recombinant inbred lines (RILs) derived from genetically and phenotypically divergent parents. Most RILs have been derived from crossing two parents from globally distant locations. However, the genetic diversity between local C. elegans populations can be as diverse as between global populations and could thus provide means of identifying genetic variation associated with complex traits relevant on a broader scale.Results: To investigate the effect of local genetic variation on heritable traits, we developed a new RIL population derived from 4 parental wild isolates collected from 2 closely located sites in France: Orsay and Santeuil. We crossed these 4 genetically diverse parental isolates to generate a population of 200 multi-parental RILs and used RNA-seq to obtain sequence polymorphisms identifying almost 9000 SNPs variable between the 4 genotypes with an average spacing of 11 kb, doubling the mapping resolution relative to currently available RIL panels for many loci. The SNPs were used to construct a genetic map to facilitate QTL analysis. We measured life history traits such as lifespan, stress resistance, developmental speed, and population growth in different environments, and found substantial variation for most traits. We detected multiple QTLs for most traits, including novel QTLs not found in previous QTL analysis, including those for lifespan and pathogen responses. This shows that recombining genetic variation across C. elegans populations that are in geographical close proximity provides ample variation for QTL mapping. Conclusion: Taken together, we show that using more parents than the classical two parental genotypes to construct a RIL population facilitates the detection of QTLs and that the use of wild isolates facilitates the detection of QTLs. The use of multi-parent RIL populations can further enhance our understanding of local adaptation and life history trade-offs.

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Section: Introductionmentioning

confidence: 99%

A multi-parent recombinant inbred line population of C. elegans allows identification of novel QTLs for complex life history traits

Snoek¹,

Volkers²,

Nijveen³

et al. 2019

BMC Biol

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“…This is partly due to the competing challenges of (1) studying population 40 ecology in the laboratory, and (2) the paucity of laboratory model organisms that are suitable for 41 ecological studies. The model nematode Pristionchus pacificus displays two types of phenotypic 42 plasticity that critically impact life history, developmental pathway and mouth form, providing an 43 experimentally tractable system to explore cross-generational influence 12,13 . 44…”

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confidence: 99%

Adult influence on juvenile phenotypes by stage-specific pheromone production

Werner

Claaßen

Renahan

et al. 2018

Preprint

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1Animals and plants can predict decreasing food supplies by recognition of population density, 2 and respond by adjusting behavioral and morphological traits. Population density in nematodes 3 is detected through pheromones, influencing dormant (dauer) stage entry, and in some lineages 4 alternative mouth-form decision (bacterivorous vs. predatory). Whether age is a relevant 5 parameter in recognizing population density is not well understood. Here, we utilized the mouth-6 form plasticity of the model nematode Pristionchus pacificus and developmental pheromone 7 profiling to study potential parent:progeny communication. Surprisingly, we observed adult-8 specific production of molecules that induce the predatory morph, even though adult mouth 9 forms are no longer plastic. We introduce a novel dye-based method to differentiate populations 10 in mixed-generation cultures, and found adults, but not peers, influence developing juvenile 11 mouth forms. Finally, we applied a logistic growth model that demonstrates adults both lower 12 the population carrying capacity and decrease the time until resource depletion. In the 13 necromenic life cycle of P. pacificus, we view mouth-form plasticity as an alternative 'Malthusian 14 escape' strategy to dauer that responds to age-specific population densities. The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/291591 doi: bioRxiv preprint first posted online Mar. 29, 2018; Population density is an important ecological parameter that correlates with increased 26 competition for resources 1 . In addition to density-dependent selection 2 , which operates on 27 evolutionary time scales, some organisms can respond dynamically to population density by 28 phenotypic plasticity. For example, plants can sense crowding by detecting the ratio of red 29 (chlorophyll absorbing) to far red (non-absorbing) light, and respond by various shade-30 avoidance strategies including higher shoots 3 . Locusts undergo solitary to swarm (i.e. 31 gregarious) transition, and aphids can develop wings, both as a result of increased physical 32 mechanosensory contact [4][5][6] . Intriguingly, population density can also have transgenerational 33 effects. For example, adult crowding of the desert locust Schistocerca gregaria 7,8 and migratory 34 locust Locusta migratoria 9 also influences the egg size, number, and morphology of their 35 progeny, and high population densities of red squirrels elicit hormonal regulation in mothers to 36 influence faster developing offspring 10 . Nevertheless, while incorporating age into population 37 structures has significantly advanced density-dependent selection theory 11 , surprisingly little 38age-specific refinement has been incorporated into models of phenotypic plasticity, especially at 39 the mechanistic level. This is partly due to the competing challenges of (1) studying population 40 ecology in the laboratory, and (2) the paucity of laboratory model organisms that are suitable for 41 ecological studies. The model nematode ...

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“…Signalling pathways have been extensively investigated in the free-living nematode Caenorhabditis elegans [6, 7], which is arguably the best-characterised and most tractable metazoan model organism [8, 9]. Particularly well studied are pathways governing/regulating growth, development, reproduction and lifespan [10–14], including those of the canonical “dauer signalling” complex [15–19]. Here, environmental signals are received by chemosensory neurons through the cyclic guanosine monophosphate (cGMP) signalling pathway [15], then transduced via the transforming growth factor-β (TGF-β) signalling and insulin/insulin-like growth factor 1 (IGF-1) signalling pathways in neuroendocrine tissues [17, 18], and converted to steroid hormone signals (e.g.…”

Section: Introductionmentioning

confidence: 99%

Dauer signalling pathway model for Haemonchus contortus

Wang

Korhonen

et al. 2019

Parasites Vectors

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Background Signalling pathways have been extensively investigated in the free-living nematode Caenorhabditis elegans , but very little is known about these pathways in parasitic nematodes. Here, we constructed a model for the dauer-associated signalling pathways in an economically highly significant parasitic worm, Haemonchus contortus . Methods Guided by data and information available for C. elegans , we used extensive genomic and transcriptomic datasets to infer gene homologues in the dauer-associated pathways, explore developmental transcriptomic, proteomic and phosphoproteomic profiles in H. contortus and study selected molecular structures. Results The canonical cyclic guanosine monophosphate (cGMP), transforming growth factor-β (TGF-β), insulin-like growth factor 1 (IGF-1) and steroid hormone signalling pathways of H. contortus were inferred to represent a total of 61 gene homologues. Compared with C. elegans , H. contortus has a reduced set of genes encoding insulin-like peptides, implying evolutionary and biological divergences between the parasitic and free-living nematodes. Similar transcription profiles were found for all gene homologues between the infective stage of H. contortus and dauer stage of C. elegans . High transcriptional levels for genes encoding G protein-coupled receptors (GPCRs), TGF-β, insulin-like ligands (e.g. ins-1 , ins-17 and ins-18 ) and transcriptional factors (e.g. daf-16 ) in the infective L3 stage of H. contortus were suggestive of critical functional roles in this stage. Conspicuous protein expression patterns and extensive phosphorylation of some components of these pathways suggested marked post-translational modifications also in the L3 stage. The high structural similarity in the DAF-12 ligand binding domain among nematodes indicated functional conservation in steroid (i.e. dafachronic acid) signalling linked to worm development. Conclusions Taken together, this pathway model provides a basis to explore hypotheses regarding biological processes and regulatory mechanisms ( via particular microRNAs, phosphorylation events and/or lipids) associated with the development of H. contortus and related nematodes as well as parasite-host cross talk, which could aid the discovery of new therapeutic targets. Electronic supplementary material The online version of this article (10.1186/s13071-019-3419-6) contains supplementary material, which is available to authorized users.

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Reimagining pheromone signalling in the model nematode Caenorhabditis elegans

Cited by 16 publications

References 42 publications

A multi-parent recombinant inbred line population of C. elegans allows identification of novel QTLs for complex life history traits

A multi-parent recombinant inbred line population of C. elegans allows identification of novel QTLs for complex life history traits

Adult influence on juvenile phenotypes by stage-specific pheromone production

Dauer signalling pathway model for Haemonchus contortus

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