Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia

Abstract

The Bicoid (Bcd) gradient in Drosophila has long been a model for the action of a morphogen in establishing embryonic polarity. However, it is now clear that bcd is a unique feature of higher Diptera. An evolutionarily ancient gene, orthodenticle (otd), has a bcd-like role in the beetle Tribolium. Unlike the Bcd gradient, which arises by diffusion of protein from an anteriorly localized messenger RNA, the Tribolium Otd gradient forms by translational repression of otd mRNA by a posteriorly localized factor. These differences in gradient formation are correlated with differences in modes of embryonic patterning. Drosophila uses long germ embryogenesis, where the embryo derives from the entire anterior-posterior axis, and all segments are patterned at the blastoderm stage, before gastrulation. In contrast, Tribolium undergoes short germ embryogenesis: the embryo arises from cells in the posterior of the egg, and only anterior segments are patterned at the blastoderm stage, with the remaining segments arising after gastrulation from a growth zone. Here we describe the role of otd in the long germband embryo of the wasp Nasonia vitripennis. We show that Nasonia otd maternal mRNA is localized at both poles of the embryo, and resulting protein gradients pattern both poles. Thus, localized Nasonia otd has two major roles that allow long germ development. It activates anterior targets at the anterior of the egg in a manner reminiscent of the Bcd gradient, and it is required for pre-gastrulation expression of posterior gap genes.

Darwin 200: Beneath the surface

“…This apparent paradox is resolved only when considering gene regulatory networks as a whole. The labs of Reinhard Schroeder, of the University of Tübingen, Germany, and Claude Desplan, of New York University, for example, found that several genes that are activated by Bicoid after fertilization in fruitflies are deposited into the egg before fertilization in the flour beetle 2 and a parasitic wasp 3 . The lack of Bicoid is compensated by minor changes in the action of several other genes in the developmental network.…”

The evolution of developmental gene networks: lessons from comparative studies on holometabolous insects

“…In insects exhibiting long germ embryogenesis, however, head and thoracic segments are patterned further towards the anterior egg pole. It has been proposed that this spatial shift in anterior patterning required the evolution of an instructive anterior patterning gradient to complement the action of existing posterior determinants (Lynch et al 2006a). The localization of maternal mRNAs to the anterior pole of the oocyte is observed in T. castaneum, N. vitripennis and D. melanogaster (Lawrence 1992;Bucher et al 2005;Olesnicky & Desplan 2007); figure 1.…”

“…The mechanism by which maternal protein gradients form in N. vitripennis is slightly different from that of D. melanogaster-rather than proteins diffusing from localized sources of mRNA, on fertilization mRNAs are released from the egg pole and diffuse to form mRNA gradients that are converted into protein gradients via translation. The maternal Orthodenticle-1 gradient functions to activate anterior segmentation genes, such as the gap genes empty spiracles, (zygotic) giant and hunchback (Lynch et al 2006a), while the maternal Giant gradient functions to set the anterior expression boundary of the central gap gene Krüppel (Brent et al 2007). The repressive role of maternal Giant is permissive for anterior development, since, in its absence, Krü ppel expression spreads anteriorly to repress the anterior gap gene hunchback (Brent et al 2007).…”

“…In N. vitripennis anterior patterning is accomplished by two distinct anterior gradients of patterning molecules (Lynch et al 2006a;Brent et al 2007). In contrast to D. melanogaster, where their expression is purely zygotic, in N. vitripennis maternal mRNAs of both orthodenticle-1 and giant are tethered to the anterior pole during oogenesis (for details see Lynch et al 2006a;Brent et al 2007;Olesnicky & Desplan 2007). Following fertilization these mRNAs are translated to form anterior gradients of Orthodenticle-1 and Giant protein.…”

“…The localization of maternal mRNAs to the anterior pole of the oocyte is observed in T. castaneum, N. vitripennis and D. melanogaster (Lawrence 1992;Bucher et al 2005;Olesnicky & Desplan 2007); figure 1. In N. vitripennis and D. melanogaster, diffusion of mRNA and/or translated protein from anterior and posterior sources of maternal mRNAs form largely non-overlapping, and opposing, instructive patterning gradients (Lawrence 1992;Lynch et al 2006a;Olesnicky et al 2006;Brent et al 2007); figure 2 and table 1. In T. castaneum, on the contrary, neither of the anteriorly localized mRNAs identified to date play a significant role in anterior-posterior patterning , and the maternal mRNAs of two genes known to be important anterior determinants in T. castaneumhunchback and orthodenticle-1-are initially distributed uniformly in the egg ( Wolff et al 1995;Schrö der 2003); see table 1.…”