Evolution of the Ventral Midline in Insect Embryos

Robert P. Zinzen; Jessica Cande; Matthew Ronshaugen; Dmitri Papatsenko; Mike Levine

doi:10.1016/j.devcel.2006.10.012

Evolution of the Ventral Midline in Insect Embryos

Robert P. Zinzen, Jessica Cande, Matthew Ronshaugen, Dmitri Papatsenko, Mike Levine

Research output: Contribution to journal › Article › peer-review

48 Scopus citations

Abstract

The ventral midline is a source of signals that pattern the nerve cord of insect embryos. In dipterans such as the fruitfly Drosophila melanogaster (D.mel.) and the mosquito Anopheles gambiae (A.gam.), the midline is narrow and spans just 1-2 cells. However, in the honeybee, Apis mellifera (A.mel.), the ventral midline is broad and encompasses 5-6 cells. slit and other midline-patterning genes display a corresponding expansion in expression. Evidence is presented that this difference is due to divergent cis regulation of the single-minded (sim) gene, which encodes a bHLH-PAS transcription factor essential for midline differentiation. sim is regulated by a combination of Notch signaling and a Twist (Twi) activator gradient in D.mel., but it is activated solely by Twi in A.mel. We suggest that the Twi-only mode of regulation-and the broad ventral midline-represents the ancestral form of CNS patterning in Holometabolous insects.

Original language	English (US)
Pages (from-to)	895-902
Number of pages	8
Journal	Developmental cell
Volume	11
Issue number	6
DOIs	https://doi.org/10.1016/j.devcel.2006.10.012
State	Published - Dec 2006
Externally published	Yes

All Science Journal Classification (ASJC) codes

General Biochemistry, Genetics and Molecular Biology
Molecular Biology
Cell Biology
Developmental Biology

Keywords

DEVBIO
EVO_ECOL

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10.1016/j.devcel.2006.10.012

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title = "Evolution of the Ventral Midline in Insect Embryos",

abstract = "The ventral midline is a source of signals that pattern the nerve cord of insect embryos. In dipterans such as the fruitfly Drosophila melanogaster (D.mel.) and the mosquito Anopheles gambiae (A.gam.), the midline is narrow and spans just 1-2 cells. However, in the honeybee, Apis mellifera (A.mel.), the ventral midline is broad and encompasses 5-6 cells. slit and other midline-patterning genes display a corresponding expansion in expression. Evidence is presented that this difference is due to divergent cis regulation of the single-minded (sim) gene, which encodes a bHLH-PAS transcription factor essential for midline differentiation. sim is regulated by a combination of Notch signaling and a Twist (Twi) activator gradient in D.mel., but it is activated solely by Twi in A.mel. We suggest that the Twi-only mode of regulation-and the broad ventral midline-represents the ancestral form of CNS patterning in Holometabolous insects.",

keywords = "DEVBIO, EVO_ECOL",

author = "Zinzen, {Robert P.} and Jessica Cande and Matthew Ronshaugen and Dmitri Papatsenko and Mike Levine",

note = "Funding Information: We thank Nipam Patel and Sharon Amacher for helpful discussions; Fred Biemar, Joung-Woo Hong, Yury Goltsev, Kate Senger, and the editors for comments; and Sue Brown, Andrea Wills, and Angela DePace for technical assistance. Tom Parisian at Honeybee Genetics and the Harry J. Laidlaw, Jr. Honey Bee Research Facility at the University of California, Davis helped with bee husbandry. This work was funded by a grant from the National Institutes of Health (GM 46638) and by the Moore Foundation (Center for Integrative Genomics). ",

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AU - Zinzen, Robert P.

AU - Cande, Jessica

AU - Ronshaugen, Matthew

AU - Papatsenko, Dmitri

AU - Levine, Mike

N1 - Funding Information: We thank Nipam Patel and Sharon Amacher for helpful discussions; Fred Biemar, Joung-Woo Hong, Yury Goltsev, Kate Senger, and the editors for comments; and Sue Brown, Andrea Wills, and Angela DePace for technical assistance. Tom Parisian at Honeybee Genetics and the Harry J. Laidlaw, Jr. Honey Bee Research Facility at the University of California, Davis helped with bee husbandry. This work was funded by a grant from the National Institutes of Health (GM 46638) and by the Moore Foundation (Center for Integrative Genomics).

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N2 - The ventral midline is a source of signals that pattern the nerve cord of insect embryos. In dipterans such as the fruitfly Drosophila melanogaster (D.mel.) and the mosquito Anopheles gambiae (A.gam.), the midline is narrow and spans just 1-2 cells. However, in the honeybee, Apis mellifera (A.mel.), the ventral midline is broad and encompasses 5-6 cells. slit and other midline-patterning genes display a corresponding expansion in expression. Evidence is presented that this difference is due to divergent cis regulation of the single-minded (sim) gene, which encodes a bHLH-PAS transcription factor essential for midline differentiation. sim is regulated by a combination of Notch signaling and a Twist (Twi) activator gradient in D.mel., but it is activated solely by Twi in A.mel. We suggest that the Twi-only mode of regulation-and the broad ventral midline-represents the ancestral form of CNS patterning in Holometabolous insects.

AB - The ventral midline is a source of signals that pattern the nerve cord of insect embryos. In dipterans such as the fruitfly Drosophila melanogaster (D.mel.) and the mosquito Anopheles gambiae (A.gam.), the midline is narrow and spans just 1-2 cells. However, in the honeybee, Apis mellifera (A.mel.), the ventral midline is broad and encompasses 5-6 cells. slit and other midline-patterning genes display a corresponding expansion in expression. Evidence is presented that this difference is due to divergent cis regulation of the single-minded (sim) gene, which encodes a bHLH-PAS transcription factor essential for midline differentiation. sim is regulated by a combination of Notch signaling and a Twist (Twi) activator gradient in D.mel., but it is activated solely by Twi in A.mel. We suggest that the Twi-only mode of regulation-and the broad ventral midline-represents the ancestral form of CNS patterning in Holometabolous insects.

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Evolution of the Ventral Midline in Insect Embryos

Abstract

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