title: Functional Conservation and Divergence of daf-22 Paralogs in Pristionchus pacificus Dauer Development.
abstract: Small-molecule signaling in nematode dauer formation has emerged as a major model to study chemical communication in development and evolution. Developmental arrest as nonfeeding and stress-resistant dauer larvae represents the major survival and dispersal strategy. Detailed studies in Caenorhabditis elegans and Pristionchus pacificus revealed that small-molecule communication changes rapidly in evolution resulting in extreme structural diversity of small-molecule compounds. In C. elegans, a blend of ascarosides constitutes the dauer pheromone, whereas the P. pacificus dauer pheromone includes additional paratosides and integrates building blocks from diverse primary metabolic pathways. Despite this complexity of small-molecule structures and functions, little is known about the biosynthesis of small molecules in nematodes outside C. elegans Here, we show that the genes encoding enzymes of the peroxisomal β-oxidation pathway involved in small-molecule biosynthesis evolve rapidly, including gene duplications and domain switching. The thiolase daf-22, the most downstream factor in C. elegans peroxisomal β-oxidation, has duplicated in P. pacificus, resulting in Ppa-daf-22.1, which still contains the sterol-carrier-protein (SCP) domain that was lost in C. elegans daf-22, and Ppa-daf-22.2. Using the CRISPR/Cas9 system, we induced mutations in both P. pacificus daf-22 genes and identified an unexpected complexity of functional conservation and divergence. Under well-fed conditions, ascaroside biosynthesis proceeds exclusively via Ppa-daf-22.1 In contrast, starvation conditions induce Ppa-daf-22.2 activity, resulting in the production of a specific subset of ascarosides. Gene expression studies indicate a reciprocal up-regulation of both Ppa-daf-22 genes, which is, however, independent of starvation. Thus, our study reveals an unexpected functional complexity of dauer development and evolution.
authors.affiliation: Max-Planck Institute for Developmental Biology, Spemannstrasse 37, Tübingen, Germany.
authors.forename: Gabriel V
authors.initials: GV
authors.lastname: Markov
authors.affiliation: Max-Planck Institute for Developmental Biology, Spemannstrasse 37, Tübingen, Germany.
authors.forename: Jan M
authors.initials: JM
authors.lastname: Meyer
authors.affiliation: Boyce Thompson Institute, Cornell University Department of Chemistry and Chemical Biology, Cornell University.
authors.forename: Oishika
authors.initials: O
authors.lastname: Panda
authors.affiliation: Boyce Thompson Institute, Cornell University.
authors.forename: Alexander B
authors.initials: AB
authors.lastname: Artyukhin
authors.affiliation: Max-Planck Institute for Developmental Biology, Spemannstrasse 37, Tübingen, Germany.
authors.forename: Marc
authors.initials: M
authors.lastname: Claaßen
authors.affiliation: Max-Planck Institute for Developmental Biology, Spemannstrasse 37, Tübingen, Germany.
authors.forename: Hanh
authors.initials: H
authors.lastname: Witte
authors.affiliation: Boyce Thompson Institute, Cornell University Department of Chemistry and Chemical Biology, Cornell University.
authors.forename: Frank C
authors.initials: FC
authors.lastname: Schroeder
authors.affiliation: Max-Planck Institute for Developmental Biology, Spemannstrasse 37, Tübingen, Germany ralf.sommer@tuebingen.mpg.de.
authors.forename: Ralf J
authors.initials: RJ
authors.lastname: Sommer
mesh_terms: D000818:Animals; D005075:Biological Evolution; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000378:metabolism; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D017124:Conserved Sequence; D019143:Evolution, Molecular; D006017:Glycolipids / Q000378:metabolism; D007814:Larva / Q000235:genetics; D053858:Metabolic Networks and Pathways; D010675:Pheromones / Q000378:metabolism; D017168:Rhabditida / Q000235:genetics* / Q000378:metabolism; D015398:Signal Transduction; D013045:Species Specificity; D013438:Sulfhydryl Compounds / Q000378:metabolism
chemical_list: D029742:Caenorhabditis elegans Proteins; D006017:Glycolipids; D010675:Pheromones; D013438:Sulfhydryl Compounds
keywords: C. elegans; Pristionchus pacificus; ascarosides; daf-22; dauer development; phenotypic plasticity; β-oxidation.