Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect

Abstract

Bone morphogenetic protein (BMP) signaling plays a major role in dorsoventral patterning in vertebrates and in Drosophila. Remarkably, in Tribolium, a beetle with an ancestral type of insect development, early BMP͞dpp exhibits differential expression along the anteroposterior axis. However, the BMP͞Dpp inhibitor Sog͞chordin is expressed ventrally and establishes a dorsal domain of BMP͞Dpp activity by transporting BMPs toward the dorsal side, like in Drosophila. Loss of Tribolium Sog not only abolishes dorsoventral polarity in the ectoderm, but also leads to the complete absence of the CNS. This phenotype suggests that sog is the main BMP antagonist in Tribolium, in contrast to vertebrates and Drosophila, which possess redundant antagonists. Surprisingly, Sog also is required for head formation in Tribolium, as are the BMP antagonists in vertebrates. Thus, in Tribolium, the system of BMP and its antagonists is less complex than in Drosophila or vertebrates and combines features from both, suggesting that it might represent an ancestral state.amnion ͉ serosa ͉ dorsoventral patterning ͉ neuroectoderm ͉ growth zone ͉ Tribolium castaneum

Functional evolution of a morphogenetic gradient

“…While the identity of regulatory factors of the positive feedback circuit may be evolutionarily labile (in Tribolium doc and hnt appear to be dispensable for amnion specification [Horn and Panfilio, 2016]), we propose that the mechanism of amnion specification through feedback-driven BMP signaling dynamics applies to a wide range of insects, because in Tribolium the pMad domain also gradually shifts to become elevated in the presumptive amnion during early gastrula stages (van der Zee et al, 2006; Nunes da Fonseca et al, 2008). The principle of evolving tissue complexity through changes in positive feedback circuits of morphogen gradients has not yet been documented in other developmental contexts, but it may also apply to unrelated traits, such as eyespots on butterfly wings (Monteiro, 2015).…”

Candidate Gene Screen in the Red Flour Beetle Tribolium Reveals Six3 as Ancient Regulator of Anterior Median Head and Central Complex Development

“…However, Tc-Dpp activity (detected by antibodies against pMad) does not occur at the site of expression and is clearly distant from the arising Tc-rx , Tc-chx , Tc-six4 , Tc-sine oculis or Tc-fas2 domains [21]. Also the Tc-dpp RNAi phenotypes differ from Drosophila mutants in that the head anlagen are expanded and appear to have lost their dorso-ventral orientation (shown by expansion of Tc-otd1 and the proneural gene Tc-ASH ) in an overall ventralized embryo [21]. Hence, the early expression of dpp at the future dorsal midline might be ancestral, but its function with respect to medially repressing gene expression has probably evolved in Drosophila .…”

“…Nevertheless, it is expressed along the rim of the head anlagen at blastoderm stages, some parts of which will become the site of dorsal fusion [163], [164]. However, Tc-Dpp activity (detected by antibodies against pMad) does not occur at the site of expression and is clearly distant from the arising Tc-rx , Tc-chx , Tc-six4 , Tc-sine oculis or Tc-fas2 domains [21]. Also the Tc-dpp RNAi phenotypes differ from Drosophila mutants in that the head anlagen are expanded and appear to have lost their dorso-ventral orientation (shown by expansion of Tc-otd1 and the proneural gene Tc-ASH ) in an overall ventralized embryo [21].…”

Extracellular Movement of Signaling Molecules

“…For example, Bone Morphogenetic Proteins (BMPs) use carrier proteins to regulate their dispersal during patterning of the dorsal-ventral axis (Eldar et al 2002; Shimmi et al 2005; van der Zee et al 2006; Ben-Zvi et al 2008; Umulis et al 2009). In Xenopus , BMPs have very low mobility, possibly due to high-affinity interactions with extracellular matrix (ECM) molecules (Ohkawara et al 2002).…”