Developmental genetic studies of the embryonic development and metamorphosis of the pedipalp using the spider Parasteatoda tepidariorum (C. L. Koch, 1841)
Final Report Abstract
The spider pedipalps are the appendage pair in front of the four pairs of walking legs. They are the most functionally versatile and morphologically diverse appendage type in spiders. Despite this importance of the pedipalp for many aspects of spider biology and evolution, the developmental and genetic basis for its development and specific morphology are largely unknown. Using the spider model species Parasteatoda tepidariorum we have produced transcriptomic data of pedipalps, legs and opisthosomas of different postembryonic stages and sexes. We have analysed these resources using comparative transcriptomics and cluster analysis in order to identify genes that are specifically expressed or specifically down-regulated in the pedipalp at a certain developmental stage or sex. In addition, we have performed a candidate gene screen for genes potentially interacting with labial1 (lab1) based on all known or potential interaction partners of labial (lab) in the fly Drosophila melanogaster. The gene lab1 is so far the only gene with a confirmed role in pedipalp appendage and pedipalp segment specification in P. tepidariorum, and the screen was therefore based on the idea that genes that interact in some way with lab1 might also be involved in pedipalp appendage or pedipalp segment development. This screen identified three interesting candidate genes, namely proboscipedia A, extradenticle1 and extradenticle2. The transcriptome analysis has provided us with a high number of potential candidates involved in the formation of the pedipalp, especially its unique copulatory organ (the bulb) in male spiders. Juvenile pedipalps have up-regulated a higher number of genes annotated to be involved in cellular and developmental processes, suggesting that the processes in juvenile pedipalps may still be similar to embryonic pedipalps. Subadult male pedipalps down-regulate genes with annotated functions in the cytoskeleton and up-regulate genes involved in RNA metabolism and processing, consistent with our recent findings of metamorphosis-like processes in the subadult, including histolysis and the presence of histoblast-like cell groups. Combined with the cluster analysis we identified a high number of genes likely involved in bulb formation and the generation of detailed adult pedipalp morphology, including Cathepsin and Serpin (pointing to remodelling of the extracellular matrix), a gene related to Doublesex and mab-3 (pointing to sex specification via conserved factors), and diverse cuticle proteins, chitin decomposition enzymes and a Hornerin homolog (pointing to structural processes of epidermal keratinization and cuticle formation, restructuring, morphology and shape). In addition, a significant portion of the genes are previously uncharacterized, spider specific genes, most of them without conserved domains. This suggests that the development of the pedipalp with its bulb (in the male), itself a spider-specific structure, uses a surprisingly high number of lineage- specific genes with no homologs outside spiders, and this is a challenge for future research, because no hints can be gleaned from more advanced models. Our results open new avenues to investigate hitherto unstudied processes in spider development, but also pose new challenges for progress in methodology and techniques in our model system Parasteatoda tepidariorum in the years to come.
Publications
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(2015). Regressive evolution of the arthropod tritocerebral segment linked to functional divergence of the Hox gene labial. Proceedings of the Royal Society B: Biological Sciences 282, 20151162
Pechmann M, Schwager EE, Turetzek N, Prpic NM
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(2016). Neofunctionalization of a duplicate dachshund gene underlies the evolution of a novel leg segment in arachnids. Molecular Biology and Evolution 33, 109-121
Turetzek N, Pechmann M, Schomburg C, Schneider J, Prpic NM
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(2017). Rapid diversification of homothorax expression patterns after gene duplication in spiders. BMC Evolutionary Biology 17:168
Turetzek N, Khadjeh S, Schomburg C, Prpic NM
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(2017). The house spider genome reveals an ancient whole-genome duplication during arachnid evolution. BMC Biology 15: 62
Schwager EE, Sharma PP, Clarke T, Leite DJ, Wierschin T, Pechmann M, Akiyama-Oda Y, Esposito L, Bechsgaard J, Bilde T, Buffry AD, Chao H, Dinh H, Doddapaneni H, Dugan S, Eibner C, Extavour CG, Funch P, Garb J, Gonzalez LB, Gonzalez VL, Griffiths-Jones S, Han Y, Hayashi C, Hilbrant M, Hughes DST, Janssen R, Lee SL, Maeso I, Murali SC, Muzny DM, Nunes da Fonseca R, Paese CLB, Qu J, Ronshaugen M, Schomburg C, Schönauer A, Stollewerk A, Torres- Oliva M, Turetzek N, Vanthournout B, Werren JH, Wolff C, Worley KC, Bucher G, Gibbs RA, Coddington J, Oda H, Stanke M, Ayoub NA, Prpic NM, Flot JF, Posnien N, Richards S, McGregor AP
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(2018). Homeobox gene duplication and divergence in arachnids. Molecular Biology and Evolution 35, 2240-2253
Leite DJ, Baudouin-Gonzalez L, Iwasaki-Yokozawa S, Lozano-Fernandez J, Turetzek N, Akiyama-Oda Y, Prpic NM, Pisani D, Oda H, Sharma PP, McGregor A
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(2020). Candidate gene screen for potential interaction partners and regulatory targets of the Hox gene labial in the spider Parasteatoda tepidariorum. Development Genes and Evolution
Schomburg C, Turetzek N, Prpic NM
