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A SoxB gene acts as an anterior gap gene and regulates posterior segment addition in the spider Parasteatoda tepidariorum

Christian L. B. Paese, Anna Schoenauer, Daniel J. Leite, Steven Russell, Alistair P. McGregor

Posted on: 18 May 2018 , updated on: 19 May 2018

Preprint posted on 10 April 2018

Article now published in eLife at http://dx.doi.org/10.7554/elife.37567

Spider Sox spins a tail: an evo-devo study from @McGregorLab and @sr120 reveals a conserved role for SoxB1 in segmentation and posterior development.

Selected by Erik Clark

Background

The common house spider (Parasteatoda tepidariorium) is a fascinating model for evo-devo, and for segmentation in particular. Spiders belong to the most basally-branching group of arthropods in relation to insects – and therefore developmental characteristics shared with Drosophila are likely to be conserved across the whole arthropod phylum. In addition, they produce their segmented body using three separate patterning mechanisms: leg-bearing segments are patterned simultaneously by gap genes (like Drosophila), abdominal segments are patterned sequentially from a posterior segment addition zone (like Tribolium), and head segments are patterned in a less well understood manner using travelling and splitting waves of hedgehog expression.

SoxB1 genes (Sox1, 2, and 3 in vertebrates) are important developmental genes, but have not been studied much in arthropods other than Drosophila. One SoxB1 gene, Dichaete, is likely to be necessary for segmentation in insects – is this role conserved in spiders?

 

Key Findings

Paese et al find that while the spider Dichaete ortholog is not involved in embryonic development, a closely related SoxB1 gene, Sox21b-1, is. (Spider Sox genes are catalogued by the same authors in another recent preprint, see Related Research.) Parental RNAi knockdown of Sox21b-1 causes segmentation gene expression to be lost within the region that normally gives rise to the leg-bearing segments, while the segment addition zone fails to develop at all. In some embryos, early embryonic events are perturbed, and the embryo never gets beyond the symmetrical germ disc phase.

Further experiments show that sox21b-1 has a crucial early role in setting up the segment addition zone, being required for the expression of such key players as Wnt, Notch, and Caudal (Cdx). Sox21b-1 also seems to be important for promoting cell proliferation, since cells in the RNAi embryos are larger and divide less often.

 

Sox21b-1 knockdown severely perturbs segmentation (Class I, II). In the most strongly-affected embryos, early development is perturbed as well (Class III).

 

Significance

The primary function of SoxB1, conserved across metazoans, is to promote neurogenesis. This study now indicates that SoxB1 also plays key roles in posterior elongation (likely conserved across bilaterians – compare the neuromesodermal progenitor role of Sox2 in vertebrates), and in segmentation (conserved across arthropods).

However, evolutionary conservation is only one side of the story, as the study also highlights a striking example of evolutionary contingency. Insects and spiders have copies of both Dichaete and Sox21b, but Dichaete plays the segmentation role in insects while Sox21b plays the segmentation role in spiders. It will be interesting to look at the expression and function of SoxB1 genes in other arthropod species, and reconstruct the evolutionary history that has led to this counter-intuitive result.

 

Related Research

Russell SRH et al (1996) The Dichaete gene of Drosophila melanogaster encodes a SOX-domain protein required for embryonic segmentation. Development 122: 3669-3676

Paese CLB, Leite DJ, Schoenauer A, McGregor AP, Russell S (2017) Duplication and divergence of Sox genes in spiders. bioRxiv https://doi.org/10.1101/212647

Clark E and Peel AD (2018) Evidence for the temporal regulation of insect segmentation by a conserved sequence of transcription factors. Development dev.155580

Tags: evo-devo, parasteatoda, patterning, segmentation, sox, soxb, spider

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Author's response

The author team shared

This work came about as a result of a sabbatical visit to the McGregor lab by Steve in 2017. The emerging evidence that SoxB genes played important roles in segmentation and neurogenesis across the insects raised the question of whether these functions were more widely conserved in arthropods. In addition, the work on the Parasteatoda genome sequence led by Alistair offered an interesting opportunity to look at the fate of the Sox family after a whole genome duplication. It has been a fantastic collaboration and SR is grateful to Alistair and Chris for introducing him to the wonderful world of spiders.

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