A bow-tie genetic architecture for morphogenesis suggested by a genome-wide RNAi screen in Caenorhabditis elegans

Matthew D. Nelson, Elinor Zhou, Karin Kiontke, Hélène Fradin, Grayson Maldonado, Daniel Martin, Khushbu Shah, David H A Fitch

Research output: Contribution to journalArticle

Abstract

During animal development, cellular morphogenesis plays a fundamental role in determining the shape and function of tissues and organs. Identifying the components that regulate and drive morphogenesis is thus a major goal of developmental biology. The four-celled tip of the Caenorhabditis elegans male tail is a simple but powerful model for studying the mechanism of morphogenesis and its spatiotemporal regulation. Here, through a genome-wide post-embryonic RNAi-feeding screen, we identified 212 components that regulate or participate in male tail tip morphogenesis. We constructed a working hypothesis for a gene regulatory network of tail tip morphogenesis. We found regulatory roles for the posterior Hox genes nob-1 and php-3, the TGF-β pathway, nuclear hormone receptors (e.g. nhr-25), the heterochronic gene blmp-1, and the GATA transcription factors egl-18 and elt-6. The majority of the pathways converge at dmd-3 and mab-3. In addition, nhr-25 and dmd-3/mab-3 regulate each others' expression, thus placing these three genes at the center of a complex regulatory network. We also show that dmd-3 and mab-3 negatively regulate other signaling pathways and affect downstream cellular processes such as vesicular trafficking (e.g. arl-1, rme-8) and rearrangement of the cytoskeleton (e.g. cdc-42, nmy-1, and nmy-2). Based on these data, we suggest that male tail tip morphogenesis is governed by a gene regulatory network with a bow-tie architecture.

Original languageEnglish (US)
Article numbere1002010
JournalPLoS Genetics
Volume7
Issue number3
DOIs
StatePublished - Mar 2011

Fingerprint

morphogenesis
Caenorhabditis elegans
RNA Interference
Morphogenesis
genome
Genome
Tail
tail
gene
Gene Regulatory Networks
GATA Transcription Factors
developmental biology
Developmental Biology
animal development
trafficking
genes
Homeobox Genes
hormone receptors
Cytoplasmic and Nuclear Receptors
cytoskeleton

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Cancer Research
  • Genetics(clinical)

Cite this

A bow-tie genetic architecture for morphogenesis suggested by a genome-wide RNAi screen in Caenorhabditis elegans. / Nelson, Matthew D.; Zhou, Elinor; Kiontke, Karin; Fradin, Hélène; Maldonado, Grayson; Martin, Daniel; Shah, Khushbu; Fitch, David H A.

In: PLoS Genetics, Vol. 7, No. 3, e1002010, 03.2011.

Research output: Contribution to journalArticle

Nelson, Matthew D. ; Zhou, Elinor ; Kiontke, Karin ; Fradin, Hélène ; Maldonado, Grayson ; Martin, Daniel ; Shah, Khushbu ; Fitch, David H A. / A bow-tie genetic architecture for morphogenesis suggested by a genome-wide RNAi screen in Caenorhabditis elegans. In: PLoS Genetics. 2011 ; Vol. 7, No. 3.
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