Functional evolution of a morphogenetic gradient

Abstract

Bone Morphogenetic Proteins (BMPs) pattern the dorsal-ventral axis of bilaterian embryos; however, their roles in the evolution of body plan are largely unknown. We examined their functional evolution in fly embryos. BMP signaling specifies two extraembryonic tissues, the serosa and amnion, in basal-branching flies such as Megaselia abdita, but only one, the amnioserosa, in Drosophila melanogaster. The BMP signaling dynamics are similar in both species until the beginning of gastrulation, when BMP signaling broadens and intensifies at the edge of the germ rudiment in Megaselia, while remaining static in Drosophila. Here we show that the differences in gradient dynamics and tissue specification result from evolutionary changes in the gene regulatory network that controls the activity of a positive feedback circuit on BMP signaling, involving the tumor necrosis factor alpha homolog eiger. These data illustrate an evolutionary mechanism by which spatiotemporal changes in morphogen gradients can guide tissue complexity.DOI: http://dx.doi.org/10.7554/eLife.20894.001

Decoupling from yolk sac is required for extraembryonic tissue spreading in the scuttle fly Megaselia abdita

“…Directly adjacent to the unambiguously identified serosa anlage, we identified a single row of cells ( Figure 1B,B’’ ), which increased in apical cell area ( Figure 1C,C’’ ) but eventually did not become part of the spreading serosa ( Figure 1D,D’’ ). These cells did not divide ( Figure 1E ), and, consistent with patterning information in the early blastoderm embryo ( Figure 1A ; ( Kwan et al, 2016 ; Rafiqi et al, 2012 )), formed the presumptive amnion. Next to the amnion, cells increased in apical cell area temporarily ( Figure 1B,B’’’,C,C’’’ ) but eventually divided and decreased in size ( Figure 1D,D’’’,E ), suggesting differentiation into ectodermal cells.…”

“…Previous analyses of M. abdita amnion development have led to conflicting hypotheses regarding its position and topology. Based on either cell outline or marker gene expression, the M. abdita amnion has been suggested to consist of either a dorsally closed epithelium or a thin lateral stripe of cells ( Rafiqi et al, 2008 ; Kwan et al, 2016 ). To resolve this question, we aimed to follow expansion and development of the presumptive amnion in our time-lapse recordings.…”

“…In D. melanogaster , the amnioserosa is set up as a single extraembryonic epithelium by expression of the Hox3 transcription factor Zerknüllt (Zen), which is controlled by peak levels of BMP signaling along the dorsal midline of the blastoderm embryo ( Gavin-Smyth and Ferguson, 2014 ). In contrast to D. melanogaster , M. abdita develops two distinct extraembryonic tissues, the serosa and, bordering it, the amnion ( Kwan et al, 2016 ; Rafiqi et al, 2008 ; Rafiqi et al, 2012 ). In the M. abdita blastoderm embryo, expression of the zen orthologue defines the serosa anlage along the dorsal midline ( Rafiqi et al, 2008 ).…”

“…In the M. abdita blastoderm embryo, expression of the zen orthologue defines the serosa anlage along the dorsal midline ( Rafiqi et al, 2008 ). Adjacent to this zen -defined serosa anlage, but within the range of dorsal BMP signaling, a narrow domain void of both zen and general embryonic patterning genes was identified as putative amnion anlage ( Figure 1A ; ( Kwan et al, 2016 ; Rafiqi et al, 2012 )). Cells of the serosa and amnion anlage undergo synchronous cell shape changes and eventually differentiate into squamous epithelia.…”

BMPs direct sensory interneuron identity in the developing spinal cord using signal-specific not morphogenic activities

“…The BMPs have been widely assumed to pattern the dorsal spinal cord as a morphogen gradient by analogy with Shh signaling in the ventral spinal cord. Studies in Drosophila ( Kwan et al, 2016 ; Bier and De Robertis, 2015 ), zebrafish ( Tribulo et al, 2003 ; Tucker et al, 2008 ) and the developing telencephalon ( Watanabe et al, 2016 ) have provided support that BMPs can act as morphogens. However, we found no evidence for this model in the spinal cord, either in our in vivo or in vitro studies.…”