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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 |
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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.
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•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. All rights reserved.</rights><rights>2013 Elsevier Inc. All rights reserved. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c516t-70799a34bd70102e423756f5eb9c776c37da3a18312e2a012ee33bd8cd5138ca3</citedby><cites>FETCH-LOGICAL-c516t-70799a34bd70102e423756f5eb9c776c37da3a18312e2a012ee33bd8cd5138ca3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,777,781,882,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23800450$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Garcia, Mayra</creatorcontrib><creatorcontrib>Nahmad, Marcos</creatorcontrib><creatorcontrib>Reeves, Gregory T.</creatorcontrib><creatorcontrib>Stathopoulos, Angelike</creatorcontrib><title>Size-dependent regulation of dorsal–ventral patterning in the early Drosophila embryo</title><title>Developmental biology</title><addtitle>Dev Biol</addtitle><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.</description><subject>Animals</subject><subject>Body Patterning</subject><subject>Body Size</subject><subject>Cell Nucleus - metabolism</subject><subject>Developmental patterning</subject><subject>Dorsal gradient</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - embryology</subject><subject>Drosophila Proteins - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Developmental</subject><subject>genes</subject><subject>inbred lines</subject><subject>Morphogen</subject><subject>mutants</subject><subject>Mutation</subject><subject>nervous system</subject><subject>Scaling</subject><subject>Snail Family Transcription Factors</subject><subject>snails</subject><subject>transcription factors</subject><subject>Transcription Factors - metabolism</subject><issn>0012-1606</issn><issn>1095-564X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqFkc9u1DAQhy0EokvhCZDARy4J4zhx7ANIqPyVKnEoFdwsx57sepWNg51daTnxDrwhT4LblAoucPJhvvl5Zj5CHjMoGTDxfFseXedDWQHjJYgSKrhDVgxUUzSi_nKXrABYVTAB4oQ8SGkLAFxKfp-cVFwC1A2syOcL_w0LhxOODseZRlzvBzP7MNLQUxdiMsPP7z8OuRbNQCczzxhHP66pH-m8QYomDkf6OoYUpo0fDMVdF4_hIbnXmyHho5v3lFy-ffPp7H1x_vHdh7NX54VtmJiLFlqlDK871wKDCuuKt43oG-yUbVtheesMN0xyVmFl8jqInHdOWtcwLq3hp-Tlkjvtux06u8ypp-h3Jh51MF7_XRn9Rq_DQXMlpKp4Dnh2ExDD1z2mWe98sjgMZsSwT5pJ4CCVkur_aJ1VNG17jfIFtfkwKWJ_OxEDfWVPb_W1PX1lT4PQ2V7uevLnMrc9v3Vl4OkC9CZos44-6cuLnCCyWsmXj18sBOajHzxGnazH0aLzEe2sXfD_HOEXgVm38w</recordid><startdate>20130901</startdate><enddate>20130901</enddate><creator>Garcia, Mayra</creator><creator>Nahmad, Marcos</creator><creator>Reeves, Gregory T.</creator><creator>Stathopoulos, Angelike</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20130901</creationdate><title>Size-dependent regulation of dorsal–ventral patterning in the early Drosophila embryo</title><author>Garcia, Mayra ; Nahmad, Marcos ; Reeves, Gregory T. ; Stathopoulos, Angelike</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c516t-70799a34bd70102e423756f5eb9c776c37da3a18312e2a012ee33bd8cd5138ca3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Body Patterning</topic><topic>Body Size</topic><topic>Cell Nucleus - metabolism</topic><topic>Developmental patterning</topic><topic>Dorsal gradient</topic><topic>Drosophila</topic><topic>Drosophila melanogaster</topic><topic>Drosophila melanogaster - embryology</topic><topic>Drosophila Proteins - metabolism</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Developmental</topic><topic>genes</topic><topic>inbred lines</topic><topic>Morphogen</topic><topic>mutants</topic><topic>Mutation</topic><topic>nervous system</topic><topic>Scaling</topic><topic>Snail Family Transcription Factors</topic><topic>snails</topic><topic>transcription factors</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Garcia, Mayra</creatorcontrib><creatorcontrib>Nahmad, Marcos</creatorcontrib><creatorcontrib>Reeves, Gregory T.</creatorcontrib><creatorcontrib>Stathopoulos, Angelike</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Garcia, Mayra</au><au>Nahmad, Marcos</au><au>Reeves, Gregory T.</au><au>Stathopoulos, Angelike</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Size-dependent regulation of dorsal–ventral patterning in the early Drosophila embryo</atitle><jtitle>Developmental biology</jtitle><addtitle>Dev Biol</addtitle><date>2013-09-01</date><risdate>2013</risdate><volume>381</volume><issue>1</issue><spage>286</spage><epage>299</epage><pages>286-299</pages><issn>0012-1606</issn><eissn>1095-564X</eissn><abstract>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.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>23800450</pmid><doi>10.1016/j.ydbio.2013.06.020</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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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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