The nested embryonic dorsal domains of BMP‐target genes are not scaled to size during the evolution of Drosophila species

• Published in: Journal of experimental zoology. Part B, Molecular and developmental evolution Molecular and developmental evolution, 2023-03, Vol.340 (2), p.131-142
• Main Authors: Chahda, Juan Sebastian, Ambrosi, Priscilla, Mizutani, Claudia M.
• Format: Article
• Language: English
• Subjects: amnioserosa; Animals; Body Patterning - genetics; dorso‐ventral patterning; DPP/BMP‐4 gradient; Drosophila - genetics; Drosophila - metabolism; Drosophila melanogaster - genetics; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Drosophila species; ectoderm; embryogenesis; evolution of development; gastrulation; gene regulation; Phenotype; scaling of morphogenetic gradients
• ISSN: 1552-5007; 1552-5015
• DOI: 10.1002/jez.b.23137

Egg size is a fast‐evolving trait among Drosophilids expected to change the spatial distribution of morphogens that pattern the embryonic axes. Here we asked whether the patterning of the dorsal region of the embryo by the Decapentaplegic/Bone Morphogenetic Protein‐4 (DPP/BMP‐4) gradient is scaled among Drosophila species with different egg sizes. This region specifies the extra‐embryonic tissue amnioserosa and the ectoderm. We find that the entire dorsal region scales with embryo size, but the gene expression patterns regulated by DPP are not proportional, suggesting that the DPP gradient is differentially scaled during evolution. To further test whether the DPP gradient can scale or not in Drosophila melanogaster, we created embryos with expanded dorsal regions that mimic changes in scale seen in other species and measured the resulting domains of DPP‐target genes. We find that the proportions of these domains are not maintained, suggesting that the DPP gradient is unable to scale in the embryo. These and previous findings suggest that the embryonic dorso‐ventral patterning lack scaling in the ventral and dorsal sides but is robust in the lateral region where the neuroectoderm is specified and two opposing gradients, Dorsal/NFkappa‐B and DPP, intersect. We propose that the lack of scaling of the DPP gradient may contribute to changes in the size of the amnioserosa and the numbers of ectodermal cells with specific cortical tensions, which are expected to generate distinct mechanical forces for gastrulating embryos of different sizes. Research highlights (1) The patterning of the dorsal embryonic region of Drosophila species are not scaled to embryonic size. (2) The Decapentaplegic (DPP) gradient does not scale in Drosophila melanogaster embryos with expanded dorsal region. (3) Evolutionary changes in amnioserosa and ectodermal domain sizes should modify mechanical forces during gastrulation of embryos of different sizes. Representation of gene expression domains within the dorsal region of embryos from Drosophila species that vary in egg size. The dorsal region marked by decapentaplegic (dpp) expression expands proportionally with embryo size. However, the ratios of expression domain widths of DPP‐target genes appear skewed between Drosophila melanogaster and Drosophila sechellia, suggesting that the DPP/BMP‐4 gradients scale differentially within these two species. Additional experiments in D. melanogaster show that this gradient does not scale when the