Non-canonical dorsoventral patterning in the moth midge Clogmia albipunctata

Wotton, Karl R.; Alcaine Colet, Anna, 1992-; Jaeger, Johannes; Jiménez-Guri, Eva

doi:http://dx.doi.org/10.1186/s13227-017-0083-9

Non-canonical dorsoventral patterning in the moth midge Clogmia albipunctata

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Wotton KR, Alcaine-Colet A, Jaeger J, Jiménez-Guri E. Non-canonical dorsoventral patterning in the moth midge Clogmia albipunctata. EvoDevo. 2017 Dec;8(1):20. DOI: 10.1186/s13227-017-0083-9

Abstract

Background. Bone morphogenetic proteins (BMPs) are of central importance for dorsal–ventral (DV) axis specification. They are core components of a signalling cascade that includes the BMP ligand decapentaplegic (DPP) and its antagonist short gastrulation (SOG) in Drosophila melanogaster. These components are very ancient, with orthologs involved in DV patterning in both protostomes and deuterostomes. Despite such strong conservation, recent comparative work in insects has revealed interesting differences in the way the patterning function of the DV system is achieved in different species. Results. In this paper, we characterise the expression patterns of the principal components of the BMP DV patterning system, as well as its signalling outputs and downstream targets, in the non-cyclorrhaphan moth midge Clogmia albipunctata (Diptera: Psychodidae). We previously reported ventral expression patterns of dpp in the pole regions of C. albipunctata blastoderm embryos. Strikingly, we also find ventral sog and posteriorly restricted tkv expression, as well as expanded polar activity of pMad. We use our results from gene knock-down by embryonic RNA interference to propose a mechanism of polar morphogen shuttling in C. albipunctata. We compare these results to available data from other species and discuss scenarios for the evolution of DV signalling in the holometabolan insects. Conclusions. A comparison of gene expression patterns across hemipteran and holometabolan insects reveals that expression of upstream signalling factors in the DV system is very variable, while signalling output is highly conserved. This has two major implications: first, as long as ligand shuttling and other upstream regulatory mechanisms lead to an appropriately localised activation of BMP signalling at the dorsal midline, it is of less importance exactly where the upstream components of the DV system are expressed. This, in turn, explains why the early-acting components of the DV patterning system in insects exhibit extensive amounts of developmental systems drift constrained by highly conserved downstream signalling output.