Evolution of the dorsal-ventral patterning network in the mosquito,Anopheles gambiae

Abstract

The dorsal-ventral patterning of the Drosophila embryo is controlled by a well-defined gene regulation network. We wish to understand how changes in this network produce evolutionary diversity in insect gastrulation. The present study focuses on the dorsal ectoderm in two highly divergent dipterans, the fruitfly Drosophila melanogaster and the mosquito Anopheles gambiae. In D. melanogaster, the dorsal midline of the dorsal ectoderm forms a single extra-embryonic membrane, the amnioserosa. In A. gambiae, an expanded domain forms two distinct extra-embryonic tissues, the amnion and serosa. The analysis of approximately 20 different dorsal-ventral patterning genes suggests that the initial specification of the mesoderm and ventral neurogenic ectoderm is highly conserved in flies and mosquitoes. By contrast, there are numerous differences in the expression profiles of genes active in the dorsal ectoderm. Most notably, the subdivision of the extra-embryonic domain into separate amnion and serosa lineages in A. gambiae correlates with novel patterns of gene expression for several segmentation repressors. Moreover, the expanded amnion and serosa anlage correlates with a broader domain of Dpp signaling as compared with the D. melanogaster embryo. Evidence is presented that this expanded signaling is due to altered expression of the sog gene.

Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen

“…6). Genetic changes upstream of zen must have occurred in the Drosophila lineage to allow these changes in zen expression and function (31). In addition, genetic changes immediately downstream of zen must have occurred to allow the coexpression of ''serosa genes'' (zen and Kr) together with C15, pnr, dorsoccross (doc), and tail-up (tup) (25,32,33), which have been described as amnion markers in other species (14, 31) (Fig.…”

“…4). The coexpression of zen and amnion genes could have resulted from the loss of a transcriptional repressor of amnion genes downstream of zen (31). However, despite the apparent derepression of amnion markers in the amnioserosa, their Drosophila homologues have either no or only a subtle role in the initial differentiation of the amnioserosa when zen is expressed.…”

BMP-dependent serosa and amnion specification in the scuttle fly Megaselia abdita

“…This tissue is specified along the dorsal midline of the blastoderm and closes the dorsal side of the germband. In non-schizophoran dipterans, dorsal blastoderm folds over the gastrulating embryo and differentiates into two tissues: a cuticle-secreting serosa underneath the eggshell and an amnion that either lines the ventral side or closes the dorsal side of the germband (Goltsev et al, 2007;Rafiqi et al, 2008;Goltsev et al, 2009). Dorsal patterning of the dipteran embryo must have changed with the evolutionary transition from two extra-embryonic tissue types to one, but whether the transition involved altered BMP activity or genetic changes downstream or independent of this signaling pathway is unknown.…”

“…Using an antibody against pMad (the phosphorylated, activated BMP signal transducer), it has been shown that, in the mosquito Anopheles gambiae, BMP activity covers a much broader area of the dorsal blastoderm than in D. melanogaster (Goltsev et al, 2007). This difference correlates with clearly distinct expression patterns of short gastrulation (sog) and tolloid (tld), which encode extracellular BMP signaling components.…”

“…They therefore proposed that laterally released BMP dimers accumulate along the dorsal midline, generating peak levels there. The resulting BMP activity gradient would specify serosal tissue at peak levels and amniotic tissue at a lower activity threshold (Goltsev et al, 2007). However, this model does not account for the fact that, immediately posterior to the serosa anlage, prospective amnion tissue straddles the dorsal midline.…”