Cargando…

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

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 a...

Descripción completa

Detalles Bibliográficos
Autores principales: Chahda, Juan Sebastian, Ambrosi, Priscilla, Mizutani, Claudia M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9587137/
https://www.ncbi.nlm.nih.gov/pubmed/35451554
http://dx.doi.org/10.1002/jez.b.23137
_version_ 1784813842829672448
author Chahda, Juan Sebastian
Ambrosi, Priscilla
Mizutani, Claudia M.
author_facet Chahda, Juan Sebastian
Ambrosi, Priscilla
Mizutani, Claudia M.
author_sort Chahda, Juan Sebastian
collection PubMed
description 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.
format Online
Article
Text
id pubmed-9587137
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-95871372023-03-01 The nested embryonic dorsal domains of BMP‐target genes are not scaled to size during the evolution of Drosophila species Chahda, Juan Sebastian Ambrosi, Priscilla Mizutani, Claudia M. J Exp Zool B Mol Dev Evol Research Articles 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. John Wiley and Sons Inc. 2022-04-22 2023-03 /pmc/articles/PMC9587137/ /pubmed/35451554 http://dx.doi.org/10.1002/jez.b.23137 Text en © 2022 The Authors. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
Chahda, Juan Sebastian
Ambrosi, Priscilla
Mizutani, Claudia M.
The nested embryonic dorsal domains of BMP‐target genes are not scaled to size during the evolution of Drosophila species
title The nested embryonic dorsal domains of BMP‐target genes are not scaled to size during the evolution of Drosophila species
title_full The nested embryonic dorsal domains of BMP‐target genes are not scaled to size during the evolution of Drosophila species
title_fullStr The nested embryonic dorsal domains of BMP‐target genes are not scaled to size during the evolution of Drosophila species
title_full_unstemmed The nested embryonic dorsal domains of BMP‐target genes are not scaled to size during the evolution of Drosophila species
title_short The nested embryonic dorsal domains of BMP‐target genes are not scaled to size during the evolution of Drosophila species
title_sort nested embryonic dorsal domains of bmp‐target genes are not scaled to size during the evolution of drosophila species
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9587137/
https://www.ncbi.nlm.nih.gov/pubmed/35451554
http://dx.doi.org/10.1002/jez.b.23137
work_keys_str_mv AT chahdajuansebastian thenestedembryonicdorsaldomainsofbmptargetgenesarenotscaledtosizeduringtheevolutionofdrosophilaspecies
AT ambrosipriscilla thenestedembryonicdorsaldomainsofbmptargetgenesarenotscaledtosizeduringtheevolutionofdrosophilaspecies
AT mizutaniclaudiam thenestedembryonicdorsaldomainsofbmptargetgenesarenotscaledtosizeduringtheevolutionofdrosophilaspecies
AT chahdajuansebastian nestedembryonicdorsaldomainsofbmptargetgenesarenotscaledtosizeduringtheevolutionofdrosophilaspecies
AT ambrosipriscilla nestedembryonicdorsaldomainsofbmptargetgenesarenotscaledtosizeduringtheevolutionofdrosophilaspecies
AT mizutaniclaudiam nestedembryonicdorsaldomainsofbmptargetgenesarenotscaledtosizeduringtheevolutionofdrosophilaspecies