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Convergent evolution of small molecule pheromones in Pristionchus nematodes.

ABSTRACT: The small molecules that mediate chemical communication between nematodes-so-called 'nematode-derived-modular-metabolites' (NDMMs)-are of major interest because of their ability to regulate development, behavior, and life-history. Pristionchus pacificus nematodes produce an impressive diversity of structurally complex NDMMs, some of which act as primer pheromones that are capable of triggering irreversible developmental switches. Many of these NDMMs have only ever been found in P. pacificus but no attempts have been made to study their evolution by profiling closely related species. This study brings a comparative perspective to the biochemical study of NDMMs through the systematic MS/MS- and NMR-based analysis of exo-metabolomes from over 30 Pristionchus species. We identified 36 novel compounds and found evidence for the convergent evolution of complex NDMMs in separate branches of the Pristionchus phylogeny. Our results demonstrate that biochemical innovation is a recurrent process in Pristionchus nematodes, a pattern that is probably typical across the animal kingdom.

SUBMITTER: Dong C

PROVIDER: S-EPMC7224695 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Convergent evolution of small molecule pheromones in Pristionchus nematodes.

Dong Chuanfu C Weadick Cameron J CJ Truffault Vincent V Sommer Ralf J RJ

eLife 20200427

The small molecules that mediate chemical communication between nematodes-so-called 'nematode-derived-modular-metabolites' (NDMMs)-are of major interest because of their ability to regulate development, behavior, and life-history. Pristionchus pacificus nematodes produce an impressive diversity of structurally complex NDMMs, some of which act as primer pheromones that are capable of triggering irreversible developmental switches. Many of these NDMMs have only ever been found in P. paci ...[more]

PMID: 32338597

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Project description:BackgroundAn organism can respond to changing environmental conditions by adjusting gene regulation and by forming alternative phenotypes. In nematodes, these mechanisms are coupled because many species will form dauer larvae, a stress-resistant and non-aging developmental stage, when exposed to unfavorable environmental conditions, and execute gene expression programs that have been selected for the survival of the animal in the wild. These dauer larvae represent an environmentally induced, homologous developmental stage across many nematode species, sharing conserved morphological and physiological properties. Hence it can be expected that some core components of the associated transcriptional program would be conserved across species, while others might diverge over the course of evolution. However, transcriptional and metabolic analysis of dauer development has been largely restricted to Caenorhabditis elegans. Here, we use a transcriptomic approach to compare the dauer stage in the evolutionary model system Pristionchus pacificus with the dauer stage in C. elegans.ResultsWe have employed Agilent microarrays, which represent 20,446 P. pacificus and 20,143 C. elegans genes to show an unexpected divergence in the expression profiles of these two nematodes in dauer and dauer exit samples. P. pacificus and C. elegans differ in the dynamics and function of genes that are differentially expressed. We find that only a small number of orthologous gene pairs show similar expression pattern in the dauers of the two species, while the non-orthologous fraction of genes is a major contributor to the active transcriptome in dauers. Interestingly, many of the genes acquired by horizontal gene transfer and orphan genes in P. pacificus, are differentially expressed suggesting that these genes are of evolutionary and functional importance.ConclusionOur data set provides a catalog for future functional investigations and indicates novel insight into evolutionary mechanisms. We discuss the limited conservation of core developmental and transcriptional programs as a common aspect of animal evolution.

Dataset Information

Convergent evolution of small molecule pheromones in Pristionchus nematodes.

Publications

Convergent evolution of small molecule pheromones in <i>Pristionchus</i> nematodes.

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