Ancient gene duplications have shaped developmental stage-specific expression in Pristionchus pacificus

BACKGROUND: The development of multicellular organisms is accompanied by gene expression changes in differentiating cells. Profiling stage-specific expression during development may reveal important insights into gene sets that contributed to the morphological diversity across the animal kingdom. RESULTS: We sequenced RNA-seq libraries throughout a developmental timecourse of the nematode Pristionchus pacificus. The transcriptomes reflect early larval stages, adult worms including late larvae, and growth-arrested dauer larvae and allowed the identification of developmentally regulated gene clusters. Our data reveals similar trends as previous transcriptome profiling of dauer worms and represents the first expression data for early larvae in P. pacificus. Gene expression clusters characterizing early larval stages show most significant enrichments of chaperones, while collagens are most significantly enriched in transcriptomes of late larvae and adult worms. By combining expression data with phylogenetic analysis, we found that developmentally regulated genes are found in paralogous clusters that have arisen through lineage-specific duplications after the split from the Caenorhabditis elegans branch. CONCLUSIONS: We propose that gene duplications of developmentally regulated genes represent a plausible evolutionary mechanism to increase the dosage of stage-specific expression. Consequently, this may contribute to the substantial divergence in expression profiles that has been observed across larger evolutionary time scales

Transcriptional adaptation in caenorhabditis elegans

Transcriptional adaptation is a recently described phenomenon by which a mutation in one gene leads to the transcriptional modulation of related genes, termed adapting genes. At the molecular level, it has been proposed that the mutant mRNA, rather than the loss of protein function, activates this response. While several examples of transcriptional adaptation have been reported in zebrafish embryos and in mouse cell lines, it is not known whether this phenomenon is observed across metazoans. Here we report transcriptional adaptation in C. elegans, and find that this process requires factors involved in mutant mRNA decay, as in zebrafish and mouse. We further uncover a requirement for Argonaute proteins and Dicer, factors involved in small RNA maturation and transport into the nucleus. Altogether, these results provide evidence for transcriptional adaptation in C. elegans, a powerful model to further investigate underlying molecular mechanisms.publishedVersio

Modes of Inheritance and Adaptive Values of Mouth-Form Dimorphism in the Nematode Pristionchus pacificus

Phänotypische Plastizität (Entwicklungsplastizität) ist die Fähigkeit eines Organismus seinen Phänotyp als Reaktion auf wechselnde Umweltbedingungen zu verändern. Polyphänismen sind ein besonderer Fall der phänotypischen Plastizität, die zu alternativen Phänotypen führen, die funktionell unabhängig sein können und auf Entwicklungsschalter zurückzuführen sind. Der Nematode Pristionchus pacificus, ein Labormodell für die vergleichende mechanistische Biologie, zeigt eine phänotypische Plastizität seiner Mundöffnung und wurde bekannt als Modell, um die Verbindung zwischen regulatorischen Entwicklungsmechanismen und Umweltinteraktionen zu erforschen. P. pacificus weist einen Dimorphismus seiner Mundform auf und die Tiere sind entweder "stenostomat" (St) mit einer schmalen Mundöffnung oder "eurystomat" (Eu) mit einer breiten Mundöffnung. Neuste Untersuchungen zeigten, dass die Sulfatase eud-1 sowohl die irreversible Umschaltung zwischen diesen beiden Formen als auch die Mikro- und Makroevolution des Mundformverhältnisses in Pristionchus Arten steuert. Das Hauptziel dieser Arbeit ist zu einer systematischen genetischen und molekularen Charakterisierung der Mundformplastizität in P. pacificus beizutragen. Ich zeige, dass diese Plastizität geschlechtsspezifisch ist und dass eine Korrelation zwischen der Mundform der Mutter und die ihrer männlichen Nachkommen besteht. Außerdem zeige ich, dass die zwei Formen gewisse Fitnessvorteile unter verschiedenen Umweltbedingungen haben; St Würmer entwickeln sich schneller bei bakterieller Ernährung, wohingegen Eu Tiere einen Vorteil als Räuber haben, wenn nur Beutetiere als Nahrungsquelle bereitgestellt werden. Um die genetische Grundlage und die molekularen Mechanismen zur Steuerung des Entwicklungsschalters zu bestimmen, führte ich ein Mutagenese-Experiment durch und durchsuchte zusätzlich die P. pacificus Mutantensammlung nach pleiotropischen Mutanten. Indem ich Mutationen in fünf verschiedenen Loci analysierte, konnte ich zeigen, dass die Mundformplastizität unter starker epigenetischer Kontrolle steht, einschließlich Chromatin-Remodeling und lange nichtcodierende RNA-vermittelte Genregulation. Mein wichtigstes Ergebnis war die Entdeckung eines neuen antisense Transkripts im eud-1 Locus, welches als positiver Regulator des die Sulfatase codierenden eud-1 Transkripts fungiert. Diese Arbeit liefert erste Einblicke in die epigenetische Kontrolle der P. pacificus Mundformplastizität und zeigt ein unerwartet hohes Maß an Komplexität in der Regulation eines einfachen Dimorphismus

Adaptive value of a predatory mouth-form in a dimorphic nematode

Polyphenisms can be adaptations to environments that are heterogeneous in space and time, but to persist they require conditional-specific advantages. The nematode Pristionchus pacificus is a facultative predator that displays an evolutionarily conserved polyphenism of its mouthparts. During development, P. pacificus irreversibly executes either a eurystomatous (Eu) or stenostomatous (St) mouth-form, which differ in the shape and number of movable teeth. The Eu form, which has an additional tooth, is more complex than the St form and is thus more highly derived relative to species lacking teeth. Here, we investigate a putative fitness trade-off for the alternative feeding-structures of P. pacificus. We show that the complex Eu form confers a greater ability to kill prey. When adults were provided with a prey diet, Eu nematodes exhibited greater fitness than St nematodes by several measures, including longevity, offspring survival and fecundity when followed by bacterial feeding. However, the two mouth-forms had similar fecundity when fed ad libitum on bacteria, a condition that would confer benefit on the more rapidly developing St form. Thus, the two forms show conditional fitness advantages in different environments. This study provides, to our knowledge, the first functional context for dimorphism in a model for the genetics of plasticity

Data from: First insights into the nature and evolution of antisense transcription in nematodes

Background: The development of multicellular organisms is coordinated by various gene regulatory mechanisms that ensure correct spatio-temporal patterns of gene expression. Recently, the role of antisense transcription in gene regulation has moved into focus of research. To characterize genome-wide patterns of antisense transcription and to study their evolutionary conservation, we sequenced a strand-specific RNA-seq library of the nematode Pristionchus pacificus. Results: We identified 1112 antisense configurations of which the largest group represents 465 antisense transcripts (ASTs) that are fully embedded in introns of their host genes. We find that most ASTs show homology to protein-coding genes and are overrepresented in proteomic data. Together with the finding, that expression levels of ASTs and host genes are uncorrelated, this indicates that most ASTs in P. pacificus do not represent non-coding RNAs and do not exhibit regulatory functions on their host genes. We studied the evolution of antisense gene pairs across 20 nematode genomes, showing that the majority of pairs is lineage-specific and even the highly conserved vps-4, ddx-27, and sel-2 loci show abundant structural changes including duplications, deletions, intron gains and loss of antisense transcription. In contrast, host genes in general, are remarkably conserved and encode exceptionally long introns leading to unusually large blocks of conserved synteny. Conclusions: Our study has shown that in P. pacificus antisense transcription as such does not define non-coding RNAs but is rather a feature of highly conserved genes with long introns. We hypothesize that the presence of regulatory elements imposes evolutionary constraint on the intron length, but simultaneously, their large size makes them a likely target for translocation of genomic elements including protein-coding genes that eventually end up as ASTs

phylogenetic analysis of antisense gene pairs in nematodes

This archived folder contains sequences, alignments and trees that were used for the publication "First insights into the nature and evolution of antisense transcription in nematodes" (Figure 3,4,5) by Rödelsperger, Menden, Serobyan, Witte, Baskaran (BMC Evolutionary Biology, 2016). The protein sequences (.fa files) were obtained by aligning C. elegans reference sequences against 19 other nematode genomes with the help of the Software exonerate. Multiple sequence alignments (*_alignment.fa) for homologous proteins were generated by the MUSCLE software and Maximum-likelihood trees were estimated by the phangorn R-package (.nexml files)

Chromatin remodelling and antisense-mediated up-regulation of the developmental switch gene eud-1 control predatory feeding plasticity

Phenotypic plasticity has been suggested to act through developmental switches, but little is known about associated molecular mechanisms. In the nematode Pristionchus pacificus, the sulfatase eud-1 was identified as part of a developmental switch controlling mouth-form plasticity governing a predatory versus bacteriovorous mouth-form decision. Here we show that mutations in the conserved histone-acetyltransferase Ppa-lsy-12 and the methyl-binding-protein Ppa-mbd-2 mimic the eud-1 phenotype, resulting in the absence of one mouth-form. Mutations in both genes cause histone modification defects and reduced eud-1 expression. Surprisingly, Ppa-lsy-12 mutants also result in the down-regulation of an antisense-eud-1 RNA. eud-1 and antisense-eud-1 are co-expressed and further experiments suggest that antisense-eud-1 acts through eud-1 itself. Indeed, overexpression of the antisense-eud-1 RNA increases the eud-1-sensitive mouth-form and extends eud-1 expression. In contrast, this effect is absent in eud-1 mutants indicating that antisense-eud-1 positively regulates eud-1. Thus, chromatin remodelling and antisense-mediated up-regulation of eud-1 control feeding plasticity in Pristionchus

Additional file 1 of Ancient gene duplications have shaped developmental stage-specific expression in Pristionchus pacificus

Table with expression fold changes and p-values. Excel file with all expression FPKM values for all genes, fold changes and FDR corrected p-values for all genes that were found to be significantly differentially expressed in at least one comparison. The file also includes the assignments of genes to expression biclusters. (XLS 19558 kb

Additional file 2 of Ancient gene duplications have shaped developmental stage-specific expression in Pristionchus pacificus

Supplemental figures, tables, and data. PDF file with supplemental figures, tables, and data. (PDF 800 kb

Transcriptional adaptation in caenorhabditis elegans

Transcriptional adaptation is a recently described phenomenon by which a mutation in one gene leads to the transcriptional modulation of related genes, termed adapting genes. At the molecular level, it has been proposed that the mutant mRNA, rather than the loss of protein function, activates this response. While several examples of transcriptional adaptation have been reported in zebrafish embryos and in mouse cell lines, it is not known whether this phenomenon is observed across metazoans. Here we report transcriptional adaptation in C. elegans, and find that this process requires factors involved in mutant mRNA decay, as in zebrafish and mouse. We further uncover a requirement for Argonaute proteins and Dicer, factors involved in small RNA maturation and transport into the nucleus. Altogether, these results provide evidence for transcriptional adaptation in C. elegans, a powerful model to further investigate underlying molecular mechanisms