Expression of pair-rule gene homologues in a chelicerate: early patterning of the two-spotted spider miteTetranychus urticae

Abstract

Embryo segmentation has been studied extensively in the fruit fly,Drosophila. These studies have demonstrated that a mechanism acting with dual segment periodicity is required for correct patterning of the body plan in this insect, but the evolutionary origin of the mechanism, the pair-rule system, is unclear. We have examined the expression of the homologues of two Drosophila pair-rule genes, runt andpaired (Pax Group III), in segmenting embryos of the two-spotted spider mite (Tetranychus urticae Koch). Spider mites are chelicerates, a group of arthropods that diverged from the lineage leading toDrosophila at least 520 million years ago. In T. urticae,the Pax Group III gene Tu-pax3/7 was expressed during patterning of the prosoma, but not the opisthosoma, in a series of stripes which appear first in even numbered segments, and then in odd numbered segments. The miterunt homologue (Tu-run) in contrast was expressed early in a circular domains that resolved into a segmental pattern. The expression patterns of both of these genes also indicated they are regulated very differently from their Drosophila homologues. The expression pattern of Tu-pax3/7 lends support to the possibility that a pair-rule patterning mechanism is active in the segmentation pathways of chelicerates.

Evolutionary conservation and divergence of the segmentation process in arthropods

“…Similarly, a prd ortholog is segmentally expressed in the growth zone of another chelicerate, the spider mite Tetranychus. But, in the anterior segments of the prosoma, this Tetranychus prd ortholog Tu-Pax3/7 is initially expressed in a double segmental pattern (Dearden et al, 2002). In myriapods, a similar dynamic expression is seen for pair rule gene orthologs in the unpatterned growth zone.…”

“…In chelicerates (e.g., the spider Cupiennius salei, the spider mite Tetranychus urticae) and myriapods (e.g., the centipedes Strigamia maritima, Lithobius atkinsoni, and the millipede Glomeris marginata), pair rule gene orthologs are expressed in stripes in the growth zone before overt segmentation (Damen et al, 2000;2005;Schoppmeier and Damen, 2005a;Dearden et al, 2002;Hughes and Kaufman, 2002a,b;Chipman et al, 2004;Janssen, 2005;Davis et al, 2005). Most data are available for the spider Cupiennius where orthologs of seven pair rule genes have been studied [eve, hairy (h), runt (run), oddskipped (odd), odd-paired (opa), prd, and slp].…”

Early patterning of the spider embryo: a cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells

“…Comparative analysis is expected to provide data for understanding the ancestral developmental mechanisms of the arthropods. An increasing number of developmental genes have been isolated and examined in the spider and other chelicerates, illuminating similarities and differences between Drosophila and chelicerates (Telford and Thomas, 1998a;Telford and Thomas, 1998b;Damen et al, 2000;Abzhanov et al, 1999;Stollewerk et al, 2001;Damen, 2002;Dearden et al, 2002).…”

Dynamic gene expression is required for anterior regionalization in a spider

“…The gradients of Bcd or Otd acting in holometabolous insects depend on the lack of cell membranes in the syncytial blastoderm embryo that allows diffusion of these transcription factors to form gradients (2)(3)(4)(7)(8)(9). The blastoderm stages of many other arthropod embryos, however, are cellularized rather than syncytial, which does not allow the formation of transcription factor diffusion gradients (12)(13)(14)(15)(16). Very little is known about the mechanisms that account for regionalization of gene expression patterns during anterior patterning in these cellularized embryos.…”