Hox genes in spiders: Their significance for development and evolution

Turetzek, Natascha; Pechmann, Matthias; Janßen, Ralf; Prpic, Nikola‐Michael

doi:10.1016/j.semcdb.2022.11.014

Cited by 4 publications

(5 citation statements)

References 115 publications

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“…Subfunctionalisation has already been described for the Hox genes in P. tepidariorum, with differences observed between paralogues in the timing of their activation and their spatial expression domains (Schwager et al 2007;Schwager et al 2017;Turetzek et al 2022). While spatial collinearity is exhibited by both Hox clusters, temporal collinearity is maintained more for cluster A (Schwager et al 2017;Turetzek et al 2022), though this cluster has lost ftz and Hox3 in many species (Figure 3). Previously, it has been hypothesised that cluster integrity is essential for the mechanism of temporal collinearity, whereas spatial collinearity is controlled at the gene level (Duboule 2007;Krumlauf 2018;Ferrier 2019).…”

Section: Discussionmentioning

confidence: 56%

“…In several genomes, Hox genes encompass multiple predicted gene models, even for genomes with annotations generated using transcriptomic data, resulting in an inflation of the estimation of the number of intervening genes. Some estimates count as many as 98 protein coding genes interspersed within the Hox clusters in P. tepidariorum (Turetzek et al 2022), which may be inaccurate both because of the fragmentation of gene models, as well as the scaffold break disrupting Hox cluster B in the previous assembly. The triangle icons in Figure 2 reflect the presence of any intervening genes, rather than the number, to avoid overestimation due to fragmented gene models.…”

Section: Homeobox Gene Clusters In Spider Genomesmentioning

confidence: 99%

“…An independent WGD took place in the arachnopulmonate ancestor (Figure 1), resulting in many homeobox genes retained in duplicate in spiders and scorpions and their relatives, including two ohnologous Hox clusters (Schwager et al 2017;Leite et al 2018;Harper et al 2021;Ontano et al 2021). Between the Hox genes, each ohnologue exhibits different spatial and temporal expression, though overall, spatial and temporal collinearity is largely intact (Schwager et al 2007;Schwager et al 2017;Turetzek et al 2022). Beyond the two Hox clusters, nearly 60% of all homeobox gene families were found to have retained duplicates in spiders and scorpions, with previous descriptions totalling 145 homeobox genes belonging to 80 families in the spider Parasteatoda tepidariorum and 156 genes in 82 families in the scorpion Centruroides sculpturatus (Schwager et al 2017;Leite et al 2018).…”

Section: Introductionmentioning

confidence: 99%

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Evolution of the spider homeobox gene repertoire by tandem and whole genome duplication

Aase-Remedios

Janßen

Leite

et al. 2023

Preprint

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Whole genome duplication (WGD) generates new genetic material that can contribute to the evolution of gene regulatory networks and phenotypes. After WGD, retained ohnologues can undergo subfunctionalisation to partition ancestral functions and/or neofunctionalisation, where one copy assumes a new function. We previously found that there had been a WGD in an ancestor of arachnopulmonates, the lineage including spiders and scorpions but excluding other arachnids like mites, ticks, and harvestmen. This WGD was evidenced by many duplicated homeobox genes, including two Hox clusters, in spiders. However, it was unclear which homeobox paralogues were produced by WGD versus tandem duplications. Understanding this is key to determining the relative contributions of tandem duplications and WGD to arachnopulmonate genome evolution. Here we characterised the distribution of duplicated homeobox genes across eight chromosome-level spider genomes. We found that the majority of retained duplicate homeobox genes in spiders likely originated from WGD. We also found two copies of conserved homeobox gene clusters, including the Hox, NK, HRO, Irx, and SINE, in all eight species. Consistently, we noticed one degenerated copy of each cluster in terms of gene content and organisation while the other remained more intact. Focussing on the NK cluster, we found evidence for regulatory subfunctionalisation between the duplicated NK genes in the spider Parasteatoda tepidariorum to their single-copy orthologues in the harvestman Phalangium opilio. Our study provides new insights into the contributions of multiple modes of duplication to the homeobox gene repertoire during the evolution of spiders and the function of NK genes.

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Section: Discussionmentioning

confidence: 56%

Section: Homeobox Gene Clusters In Spider Genomesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Evolution of the spider homeobox gene repertoire by tandem and whole genome duplication

Aase-Remedios

Janßen

Leite

et al. 2023

Preprint

Self Cite

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“…The regulatory elements responsible for temporal collinearity constrain Hox gene organization, thus it has been hypothesized that Hox cluster integrity is essential for the mechanism of temporal collinearity ( Duboule 2007 ; Krumlauf 2018 ; Ferrier 2019 ). While spatial collinearity is exhibited by both spider Hox clusters, temporal collinearity is more evident in cluster A, though this cluster is less organized ( Schwager et al 2017 ; Turetzek et al 2022 ). Hox cluster organization and regulation vary between animals, for example, in mammals, each Hox cluster is condensed and is regulated globally, while in some invertebrates the Hox cluster is organized and expressed in subclusters ( Kmita and Duboule 2003 ; Deschamps and Duboule 2017 ; Wang et al 2017 ).…”

Section: Discussionmentioning

confidence: 88%

“…1 ), resulting in nearly 60% of homeobox genes retained in duplicate in spiders and scorpions and their relatives, including two Hox clusters ( Schwager et al 2017 ; Leite et al 2018 ; Harper et al 2021 ). Within each Hox gene family, one ohnologue exhibits different spatial and temporal expression compared to the other, though overall, spatial and temporal collinearity is largely intact for each cluster ( Schwager et al 2007 , 2017 ; Turetzek et al 2022 ). Several of the other retained homeobox genes exhibit divergent expression consistent with both sub- and neofunctionalization in Parasteatoda tepidariorum , showing that duplication of these genes has played a role in the evolution of spider development ( Leite et al 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Evolution of the Spider Homeobox Gene Repertoire by Tandem and Whole Genome Duplication

Aase-Remedios,

Janssen,

Leite

et al. 2023

Molecular Biology and Evolution

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Gene duplication generates new genetic material that can contribute to the evolution of gene regulatory networks and phenotypes. Duplicated genes can undergo subfunctionalization to partition ancestral functions and/or neofunctionalization to assume a new function. We previously found there had been a whole genome duplication (WGD) in an ancestor of arachnopulmonates, the lineage including spiders and scorpions but excluding other arachnids like mites, ticks, and harvestmen. This WGD was evidenced by many duplicated homeobox genes, including two Hox clusters, in spiders. However, it was unclear which homeobox paralogues originated by WGD versus smaller-scale events such as tandem duplications. Understanding this is a key to determining the contribution of the WGD to arachnopulmonate genome evolution. Here we characterized the distribution of duplicated homeobox genes across eight chromosome-level spider genomes. We found that most duplicated homeobox genes in spiders are consistent with an origin by WGD. We also found two copies of conserved homeobox gene clusters, including the Hox, NK, HRO, Irx, and SINE clusters, in all eight species. Consistently, we observed one copy of each cluster was degenerated in terms of gene content and organization while the other remained more intact. Focussing on the NK cluster, we found evidence for regulatory subfunctionalization between the duplicated NK genes in the spider Parasteatoda tepidariorum compared to their single-copy orthologues in the harvestman Phalangium opilio. Our study provides new insights into the relative contributions of multiple modes of duplication to the homeobox gene repertoire during the evolution of spiders and the function of NK genes.

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Expression of posterior Hox genes and opisthosomal appendage development in a mygalomorph spider

Janßen¹,

Pechmann²

2023

Dev Genes Evol

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Spiders represent an evolutionary successful group of chelicerate arthropods. The body of spiders is subdivided into two regions (tagmata). The anterior tagma, the prosoma, bears the head appendages and four pairs of walking legs. The segments of the posterior tagma, the opisthosoma, either lost their appendages during the course of evolution or their appendages were substantially modified to fulfill new tasks such as reproduction, gas exchange, and silk production. Previous work has shown that the homeotic Hox genes are involved in shaping the posterior appendages of spiders. In this paper, we investigate the expression of the posterior Hox genes in a tarantula that possesses some key differences of posterior appendages compared to true spiders, such as the lack of the anterior pair of spinnerets and a second set of book lungs instead of trachea. Based on the observed differences in posterior Hox gene expression in true spiders and tarantulas, we argue that subtle changes in the Hox gene expression of the Hox genes abdA and AbdB are possibly responsible for at least some of the morphological differences seen in true spiders versus tarantulas.

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Hox genes in spiders: Their significance for development and evolution

Cited by 4 publications

References 115 publications

Evolution of the spider homeobox gene repertoire by tandem and whole genome duplication

Evolution of the spider homeobox gene repertoire by tandem and whole genome duplication

Evolution of the Spider Homeobox Gene Repertoire by Tandem and Whole Genome Duplication

Expression of posterior Hox genes and opisthosomal appendage development in a mygalomorph spider

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