Diversity of epithelial morphogenesis during eggshell formation in drosophilids

Miriam Osterfield, Trudi Schüpbach, Eric Wieschaus, Stanislav Y. Shvartsman

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

The eggshells of drosophilid species provide a powerful model for studying the origins of morphological diversity. The dorsal appendages, or respiratory filaments, of these eggshells display a remarkable interspecies variation in number and shape, and the epithelial patterning underlying the formation of these structures is an area of active research. To extend the analysis of dorsal appendage formation to include morphogenesis, we developed an improved 3D image reconstruction approach. This approach revealed considerable interspecies variation in the cell shape changes and neighbor exchanges underlying appendage formation. Specifically, although the appendage floor in Drosophila melanogaster is formed through spatially ordered neighbor exchanges, the same structure in Scaptodrosophila pattersoni is formed through extreme changes in cell shape, whereas Drosophila funebris appears to display a combination of both cellular mechanisms. Furthermore, localization patterns of Par3/Bazooka suggest a self-organized, cell polarity-based origin for the variability of appendage number in S. pattersoni. Our results suggest that species deploy different combinations of apically and basally driven mechanisms to convert a two-dimensional primordium into a three-dimensional structure, and provide new directions for exploring the molecular origins of interspecies morphological variation.

Original languageEnglish (US)
Pages (from-to)1971-1977
Number of pages7
JournalDevelopment (Cambridge)
Volume142
Issue number11
DOIs
StatePublished - Jan 1 2015
Externally publishedYes

Fingerprint

Egg Shell
Cell Shape
Morphogenesis
Cell Polarity
Computer-Assisted Image Processing
Drosophila melanogaster
Drosophila
Research
Direction compound

Keywords

  • Drosophila
  • Epithelial morphogenesis
  • Evolution
  • Scaptodrosophila
  • Tube formation

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

Cite this

Diversity of epithelial morphogenesis during eggshell formation in drosophilids. / Osterfield, Miriam; Schüpbach, Trudi; Wieschaus, Eric; Shvartsman, Stanislav Y.

In: Development (Cambridge), Vol. 142, No. 11, 01.01.2015, p. 1971-1977.

Research output: Contribution to journalArticle

Osterfield, Miriam ; Schüpbach, Trudi ; Wieschaus, Eric ; Shvartsman, Stanislav Y. / Diversity of epithelial morphogenesis during eggshell formation in drosophilids. In: Development (Cambridge). 2015 ; Vol. 142, No. 11. pp. 1971-1977.
@article{21030da0e3aa4fb1944c6798272bf5be,
title = "Diversity of epithelial morphogenesis during eggshell formation in drosophilids",
abstract = "The eggshells of drosophilid species provide a powerful model for studying the origins of morphological diversity. The dorsal appendages, or respiratory filaments, of these eggshells display a remarkable interspecies variation in number and shape, and the epithelial patterning underlying the formation of these structures is an area of active research. To extend the analysis of dorsal appendage formation to include morphogenesis, we developed an improved 3D image reconstruction approach. This approach revealed considerable interspecies variation in the cell shape changes and neighbor exchanges underlying appendage formation. Specifically, although the appendage floor in Drosophila melanogaster is formed through spatially ordered neighbor exchanges, the same structure in Scaptodrosophila pattersoni is formed through extreme changes in cell shape, whereas Drosophila funebris appears to display a combination of both cellular mechanisms. Furthermore, localization patterns of Par3/Bazooka suggest a self-organized, cell polarity-based origin for the variability of appendage number in S. pattersoni. Our results suggest that species deploy different combinations of apically and basally driven mechanisms to convert a two-dimensional primordium into a three-dimensional structure, and provide new directions for exploring the molecular origins of interspecies morphological variation.",
keywords = "Drosophila, Epithelial morphogenesis, Evolution, Scaptodrosophila, Tube formation",
author = "Miriam Osterfield and Trudi Sch{\"u}pbach and Eric Wieschaus and Shvartsman, {Stanislav Y.}",
year = "2015",
month = "1",
day = "1",
doi = "10.1242/dev.119404",
language = "English (US)",
volume = "142",
pages = "1971--1977",
journal = "Development (Cambridge)",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "11",

}

TY - JOUR

T1 - Diversity of epithelial morphogenesis during eggshell formation in drosophilids

AU - Osterfield, Miriam

AU - Schüpbach, Trudi

AU - Wieschaus, Eric

AU - Shvartsman, Stanislav Y.

PY - 2015/1/1

Y1 - 2015/1/1

N2 - The eggshells of drosophilid species provide a powerful model for studying the origins of morphological diversity. The dorsal appendages, or respiratory filaments, of these eggshells display a remarkable interspecies variation in number and shape, and the epithelial patterning underlying the formation of these structures is an area of active research. To extend the analysis of dorsal appendage formation to include morphogenesis, we developed an improved 3D image reconstruction approach. This approach revealed considerable interspecies variation in the cell shape changes and neighbor exchanges underlying appendage formation. Specifically, although the appendage floor in Drosophila melanogaster is formed through spatially ordered neighbor exchanges, the same structure in Scaptodrosophila pattersoni is formed through extreme changes in cell shape, whereas Drosophila funebris appears to display a combination of both cellular mechanisms. Furthermore, localization patterns of Par3/Bazooka suggest a self-organized, cell polarity-based origin for the variability of appendage number in S. pattersoni. Our results suggest that species deploy different combinations of apically and basally driven mechanisms to convert a two-dimensional primordium into a three-dimensional structure, and provide new directions for exploring the molecular origins of interspecies morphological variation.

AB - The eggshells of drosophilid species provide a powerful model for studying the origins of morphological diversity. The dorsal appendages, or respiratory filaments, of these eggshells display a remarkable interspecies variation in number and shape, and the epithelial patterning underlying the formation of these structures is an area of active research. To extend the analysis of dorsal appendage formation to include morphogenesis, we developed an improved 3D image reconstruction approach. This approach revealed considerable interspecies variation in the cell shape changes and neighbor exchanges underlying appendage formation. Specifically, although the appendage floor in Drosophila melanogaster is formed through spatially ordered neighbor exchanges, the same structure in Scaptodrosophila pattersoni is formed through extreme changes in cell shape, whereas Drosophila funebris appears to display a combination of both cellular mechanisms. Furthermore, localization patterns of Par3/Bazooka suggest a self-organized, cell polarity-based origin for the variability of appendage number in S. pattersoni. Our results suggest that species deploy different combinations of apically and basally driven mechanisms to convert a two-dimensional primordium into a three-dimensional structure, and provide new directions for exploring the molecular origins of interspecies morphological variation.

KW - Drosophila

KW - Epithelial morphogenesis

KW - Evolution

KW - Scaptodrosophila

KW - Tube formation

UR - http://www.scopus.com/inward/record.url?scp=84929888197&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84929888197&partnerID=8YFLogxK

U2 - 10.1242/dev.119404

DO - 10.1242/dev.119404

M3 - Article

C2 - 25953345

AN - SCOPUS:84929888197

VL - 142

SP - 1971

EP - 1977

JO - Development (Cambridge)

JF - Development (Cambridge)

SN - 0950-1991

IS - 11

ER -