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Size-dependent regulation of dorsal–ventral patterning in the early Drosophila embryo

How natural variation in embryo size affects patterning of the Drosophila embryo dorsal–ventral (DV) axis is not known. Here we examined quantitatively the relationship between nuclear distribution of the Dorsal transcription factor, boundary positions for several target genes, and DV axis length. D...

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Published in:Developmental biology 2013-09, Vol.381 (1), p.286-299
Main Authors: Garcia, Mayra, Nahmad, Marcos, Reeves, Gregory T., Stathopoulos, Angelike
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description How natural variation in embryo size affects patterning of the Drosophila embryo dorsal–ventral (DV) axis is not known. Here we examined quantitatively the relationship between nuclear distribution of the Dorsal transcription factor, boundary positions for several target genes, and DV axis length. Data were obtained from embryos of a wild-type background as well as from mutant lines inbred to size select embryos of smaller or larger sizes. Our data show that the width of the nuclear Dorsal gradient correlates with DV axis length. In turn, for some genes expressed along the DV axis, the boundary positions correlate closely with nuclear Dorsal levels and with DV axis length; while the expression pattern of others is relatively constant and independent of the width of the Dorsal gradient. In particular, the patterns of snail (sna) and ventral nervous system defective (vnd) correlate with nuclear Dorsal levels and exhibit scaling to DV length; while the pattern of intermediate neuroblasts defective (ind) remains relatively constant with respect to changes in Dorsal and DV length. However, in mutants that exhibit an abnormal expansion of the Dorsal gradient which fails to scale to DV length, only sna follows the Dorsal distribution and exhibits overexpansion; in contrast, vnd and ind do not overexpand suggesting some additional mechanism acts to refine the dorsal boundaries of these two genes. Thus, our results argue against the idea that the Dorsal gradient works as a global system of relative coordinates along the DV axis and suggest that individual targets respond to changes in embryo size in a gene-specific manner. [Display omitted] •DV axis size variation in wild-type embryos is ∼14%, and inbred lines increase spread.•The width of the Dorsal gradient scales with respect to DV axis length.•Dorsal target genes respond to changes in DV axis length in a gene-specific manner.•Snail scales and follows the Dorsal gradient, whereas ind remains relatively constant.•Scaling breaks down in one inbred line and relates to a maternal-effect mutation.
doi_str_mv 10.1016/j.ydbio.2013.06.020
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[Display omitted] •DV axis size variation in wild-type embryos is ∼14%, and inbred lines increase spread.•The width of the Dorsal gradient scales with respect to DV axis length.•Dorsal target genes respond to changes in DV axis length in a gene-specific manner.•Snail scales and follows the Dorsal gradient, whereas ind remains relatively constant.•Scaling breaks down in one inbred line and relates to a maternal-effect mutation.</description><identifier>ISSN: 0012-1606</identifier><identifier>EISSN: 1095-564X</identifier><identifier>DOI: 10.1016/j.ydbio.2013.06.020</identifier><identifier>PMID: 23800450</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Body Patterning ; Body Size ; Cell Nucleus - metabolism ; Developmental patterning ; Dorsal gradient ; Drosophila ; Drosophila melanogaster ; Drosophila melanogaster - embryology ; Drosophila Proteins - metabolism ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Developmental ; genes ; inbred lines ; Morphogen ; mutants ; Mutation ; nervous system ; Scaling ; Snail Family Transcription Factors ; snails ; transcription factors ; Transcription Factors - metabolism</subject><ispartof>Developmental biology, 2013-09, Vol.381 (1), p.286-299</ispartof><rights>2013 Elsevier Inc.</rights><rights>Copyright © 2013 Elsevier Inc. 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However, in mutants that exhibit an abnormal expansion of the Dorsal gradient which fails to scale to DV length, only sna follows the Dorsal distribution and exhibits overexpansion; in contrast, vnd and ind do not overexpand suggesting some additional mechanism acts to refine the dorsal boundaries of these two genes. Thus, our results argue against the idea that the Dorsal gradient works as a global system of relative coordinates along the DV axis and suggest that individual targets respond to changes in embryo size in a gene-specific manner. 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identifier ISSN: 0012-1606
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subjects Animals
Body Patterning
Body Size
Cell Nucleus - metabolism
Developmental patterning
Dorsal gradient
Drosophila
Drosophila melanogaster
Drosophila melanogaster - embryology
Drosophila Proteins - metabolism
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Developmental
genes
inbred lines
Morphogen
mutants
Mutation
nervous system
Scaling
Snail Family Transcription Factors
snails
transcription factors
Transcription Factors - metabolism
title Size-dependent regulation of dorsal–ventral patterning in the early Drosophila embryo
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