Decision letter: Two consecutive microtubule-based epithelial seaming events mediate dorsal closure in the scuttle fly Megaselia abdita

Evolution of morphogenesis is generally associated with changes in genetic regulation. Here, we report evidence indicating that dorsal closure, a conserved morphogenetic process in dipterans, evolved as the consequence of rearrangements in epithelial organization rather than signaling regulation. In Drosophila melanogaster, dorsal closure consists of a two-tissue system where the contraction of extraembryonic amnioserosa and a JNK/Dpp-dependent epidermal actomyosin cable result in microtubule-dependent seaming of the epidermis. We find that dorsal closure in Megaselia abdita, a three-tissue system comprising serosa, amnion and epidermis, differs in morphogenetic rearrangements despite conservation of JNK/Dpp signaling. In addition to an actomyosin cable, M. abdita dorsal closure is driven by the rupture and contraction of the serosa and the consecutive microtubule-dependent seaming of amnion and epidermis. Our study indicates that the evolutionary transition to a reduced system of dorsal closure involves simplification of the seaming process without changing the signaling pathways of closure progression.

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Author response: Two consecutive microtubule-based epithelial seaming events mediate dorsal closure in the scuttle fly Megaselia abdita

10.7554/elife.33807.037 ◽

2018 ◽

Author(s):

Juan Jose Fraire-Zamora ◽

Johannes Jaeger ◽

Jérôme Solon

Keyword(s):

Author Response ◽

Dorsal Closure ◽

Megaselia Abdita

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Two consecutive microtubule-based epithelial seaming events mediate dorsal closure in the scuttle fly Megaselia abdita

10.1101/229492 ◽

2017 ◽

Author(s):

Juan J. Fraire-Zamora ◽

Johannes Jaeger ◽

Jérôme Solon

Keyword(s):

Drosophila Melanogaster ◽

Signaling Pathways ◽

Genetic Regulation ◽

Dorsal Closure ◽

Evolutionary Transition ◽

Morphogenetic Process ◽

Signaling Regulation ◽

Tissue System ◽

Epithelial Fusion ◽

Megaselia Abdita

AbstractEvolution of morphogenesis is generally associated with changes in genetic regulation. Here we report evidence indicating that dorsal closure, a conserved morphogenetic process in dipterans, evolved as the consequence of rearrangements in epithelial organization rather than signaling regulation. In Drosophila melanogaster, dorsal closure consists of a two-tissue system where the contraction of extraembryonic amnioserosa and a JNK/Dpp-dependent epidermal actomyosin cable result in microtubule-dependent seaming of the epidermis. We find that dorsal closure in Megaselia abdita, a three-tissue system comprising serosa, amnion and epidermis, differs in morphogenetic rearrangements despite conservation of JNK/Dpp signaling. In addition to an actomyosin cable, M. abdita dorsal closure is driven by the rupture and contraction of the serosa and the consecutive microtubule-dependent seaming of amnion and epidermis. Our study indicates that the evolutionary transition to a reduced system of dorsal closure involves simplification of the seaming process without changing the signaling pathways of closure progression.Impact StatementEvolutionary reduction in tissue number involves the simplification of the seaming process but not signaling during epithelial fusion.

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Faculty Opinions recommendation of Transiently reorganized microtubules are essential for zippering during dorsal closure in Drosophila melanogaster.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1033874.539803 ◽

2007 ◽

Author(s):

Elizabeth Gavis

Keyword(s):

Drosophila Melanogaster ◽

Dorsal Closure

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Faculty Opinions recommendation of Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1099404.555655 ◽

2008 ◽

Author(s):

Mary Baylies

Keyword(s):

Dynamic Analysis ◽

Dorsal Closure

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The AF-6 Homolog Canoe Acts as a Rap1 Effector During Dorsal Closure of the Drosophila Embryo

Genetics ◽

10.1093/genetics/165.1.159 ◽

2003 ◽

Vol 165 (1) ◽

pp. 159-169

Author(s):

Benjamin Boettner ◽

Phoebe Harjes ◽

Satoshi Ishimaru ◽

Michael Heke ◽

Hong Qing Fan ◽

...

Keyword(s):

Molecular Mechanisms ◽

Genetic Interaction ◽

Critical Role ◽

Adherens Junction ◽

Small Gtpases ◽

Drosophila Embryo ◽

Dorsal Closure ◽

Cell Sheets ◽

Jnk Pathway

Abstract Rap1 belongs to the highly conserved Ras subfamily of small GTPases. In Drosophila, Rap1 plays a critical role in many different morphogenetic processes, but the molecular mechanisms executing its function are unknown. Here, we demonstrate that Canoe (Cno), the Drosophila homolog of mammalian junctional protein AF-6, acts as an effector of Rap1 in vivo. Cno binds to the activated form of Rap1 in a yeast two-hybrid assay, the two molecules colocalize to the adherens junction, and they display very similar phenotypes in embryonic dorsal closure (DC), a process that relies on the elongation and migration of epithelial cell sheets. Genetic interaction experiments show that Rap1 and Cno act in the same molecular pathway during DC and that the function of both molecules in DC depends on their ability to interact. We further show that Rap1 acts upstream of Cno, but that Rap1, unlike Cno, is not involved in the stimulation of JNK pathway activity, indicating that Cno has both a Rap1-dependent and a Rap1-independent function in the DC process.

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The Genes raw and ribbon Are Required for Proper Shape of Tubular Epithelial Tissues in Drosophila

Genetics ◽

10.1093/genetics/147.1.243 ◽

1997 ◽

Vol 147 (1) ◽

pp. 243-253 ◽

Cited By ~ 1

Author(s):

Joseph Jack ◽

Guy Myette

Keyword(s):

Embryonic Development ◽

Salivary Glands ◽

Cell Shape ◽

Malpighian Tubules ◽

Dorsal Closure ◽

Epithelial Tissues ◽

Cell Rearrangement

Abstract The products of two genes, raw and ribbon (rib), are required for the proper morphogenesis of a variety of tissues. Malpighian tubules mutant for raw or rib are wider and shorter than normal tubules, which are only two cells in circumference when they are fully formed. The mutations alter the shape of the tubules beginning early in their formation and block cell rearrangement late in development, which normally lengthens and narrows the tubes. Mutations of both genes affect a number of other tissues as well. Both genes are required for dorsal closure and retraction of the CNS during embryonic development. In addition, rib mutations block head involution, and broaden and shorten other tubular epithelia (salivary glands, tracheae, and hindgut) in much same manner as they alter the shape of the Malpighian tubules. In tissues in which the shape of cells can be observed readily, rib mutations alter cell shape, which probably causes the change in shape of the organs that are affected. In double mutants raw enhances the phenotypes of all the tissues that are affected by rib but unaffected by raw alone, indicating that raw is also active in these tissues.

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