Dynamic gene expression is required for anterior regionalization in a spider

Abstract

Patterning of a multicellular embryo requires precise spatiotemporal control of gene expression during development. The gradient of the morphogen bicoid regulates anterior regionalization in the syncytial blastoderm of Drosophila. However many arthropod embryos develop from a cellular blastoderm that does not allow the formation of transcription factor gradients. Here we show that correct anterior development of the cellularized embryo of the spider Achaearanea tepidariorum requires an anterior-to-posterior wave of dynamic gene expression for positioning the stripes of hairy, hedgehog, and orthodenticle expression. Surprisingly, this dynamic repositioning of the expression of these segmentation genes is blocked in orthodenticle pRNAi embryos and no anterior structures are specified in those embryos. Our data suggest that dynamic gene expression across a field of cells is required for anterior regionalization in spiders and provides an explanation for the problem of how positional values for anterior segmentation genes are specified via a morphogen-independent mechanism across a field of cells.Achaearanea tepidariorum ͉ evolution and development ͉ hairy ͉ orthodenticle ͉ segmentation

The Wnt and Delta-Notch signalling pathways interact to direct pair-rule gene expression via caudal during segment addition in the spider Parasteatoda tepidariorum

“…This result is consistent with previous analysis of these and other pair-rule orthologues in the Central American wandering spider Cupiennius salei (Damen et al, 2000(Damen et al, , 2005. Our data provide further evidence for differences in the regulation of prosomal and opisthosomal segments in spiders, whereby gap and pair-rule gene orthologues respectively direct the formation of segments in these tagmata (Damen et al, 2000(Damen et al, , 2005Pechmann et al, 2009Pechmann et al, , 2011Schwager et al, 2009). Interestingly, this also indicates that the roles of eve and run-1 in spiders is restricted to formation of more posterior segments than, for example, in the insects D. melanogaster and Tribolium, and the myriapods Strigamia maritima and Glomeris marginata, in which eve is expressed in a segmental pattern in four segments more anterior to O1/T2 (Frasch et al, 1987;Brown et al, 1997;Janssen et al, 2011;Brena and Akam, 2013).…”

Regressive evolution of the arthropod tritocerebral segment linked to functional divergence of the Hox genelabial

“…This dynamic wave is mainly organized by an autoregulatory loop that involves Hedgehog-signalling and the transcription factors orthodenticle and odd-paired [15,16]. The expression domains of several genes that are initially located at the rim of the germ disc during stage 5, are travelling to a more posterior position during stages 6-8.…”

Evolutionary crossroads in developmental biology: the spiderParasteatoda tepidariorum

“…For example, a number of studies have helped to reveal developmental genetic mechanisms that are probably ancestral to arthropods, and perhaps even other animals, and are therefore useful for furthering our understanding of metazoan body plan evolution. In addition, recent studies of spiders have also allowed the identification of novel developmental mechanisms, including a role for hh in axis formation (Akiyama- , an auto-regulatory signalling network involving hh and otd to control anterior patterning (Kanayama et al, 2011;Pechmann et al, 2009), and the recent finding of a role of Dll as a gap gene (Pechmann et al, 2011).…”