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  • Review Article
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How drosophila appendages develop

Nature Reviews Molecular Cell Biology volume 2, pages 89–97 (2001)Cite this article

Key Points

  • Drosophila appendages (legs, antennae, mouthparts, analia, wings and halteres) arise from imaginal discs in specific segments.

  • The critical event that permits embryonic cells to develop into the appendage primordia is expression of a homeobox gene called Distal-less ( Dll).

  • All imaginal discs subdivide into anterior and posterior compartments. The wing also subdivides into dorsal and ventral compartments in later stages in development.

  • Cells at compartment borders produce morphogens — secreted signalling molecules such as hedgehog (Hh), wingless (Wg) and decapentaplegic (Dpp) — that pattern appendages by forming gradients.

  • Cells respond to these morphogens by activating different patterns of gene expression, depending on the level of morphogen.

  • Trunk cells become separated from appendage cells by mutual antagonism between Hh/Wg/Dpp at the centre of the disc, and the homeobox genes homothorax (hth) and extradenticle ( exd), at the periphery.

  • The response to the gradient of Wg and Dpp signals generates distinct genetic domains along the proximodistal axis of the appendage: high Wg and Dpp levels in the centre of the disc (which becomes the distal appendage) activate Dll, whereas moderate levels in the intermediate zone (which becomes the more proximal appendage) activate dachshund (dac).

  • Appendage identity is specified by a combination of homeobox gene expression, which specifies the segment, and Dpp or Wg response genes, which specify dorsal or ventral properties.

  • The mechanisms used in Drosophila to segregate the cells fated to form appendages and the genes involved are conserved in vertebrates.

Abstract

Just a glance at the body of the fruitfly Drosophila reveals that it has a main body part — the trunk — and a number of specialized appendages such as legs, wings, halteres and antennae. How do Drosophila appendages develop, what gives each appendage its unique identity, and what can the fruitfly teach us about appendage development in vertebrates?

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Figure 1: Imaginal discs and the structures that develop from them.
Figure 2: Generation of cell affinity differences between anterior and posterior compartment cells in the wing disc.
Figure 3: Gene activity in the leg and wing imaginal disc primordia in a late embryo (stage 14).
Figure 4: Subdivision of the mature leg disc and the adult leg into distinct genetic subdomains.
Figure 5: Specification of appendage identity by the combinatorial contributions of Hox genes and Distal-less and vestigial.

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Acknowledgements

I thank E. Sanchez-Herrero, J. F. de Celis, M. Calleja and D. Duboule for discussions and their comments on the manuscript.

Author information

Authors and Affiliations

  1. Centro de Biología Molecular, Consejo Superior de Investigaciones Cientificas, Universidad Autónoma de Madrid, Madrid, 28049, Spain

    Ginés Morata

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  1. Ginés Morata
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DATABASE LINKS

engrailed

hedgehog

wingless

decapentaplegic

LIM-homeobox

apterous

fringe

Delta

Serrate

Notch

vestigial

Antennapedia Complex

Bithorax Complex

caudal

helix–turn–helix

Distal-less

extradenticle

homothorax

Wnt family

Spitz

escargot

zinc-finger

dachshund

aristaless

Bar

bric a brac

spineless

H15

spalt

brinker

Sex combs reduced

Antp

Ubx

abdominal-A

Abdominal-B

achaete-scute

serum response factor

meis

Pbx1

Snail

FURTHER INFORMATION

Interactive Fly: imaginal discs and tissues

Interactive Fly: the Drosophila leg

Interactive Fly: wing

Homeobox Genes Database

ENCYCLOPEDIA OF LIFE SCIENCES

Vertebrate embryo: limb development

Evolutionary developmental biology: Hox gene evolution

Drosophila embryo: cell signalling and segmental patterning

Glossary

IMAGINAL DISCS

Sac-like structures present in the larvae and composed of cells destined to form the different adult cuticular structures. They are named after the adult part that they make: for example, wing, leg, eye-antennal, genital.

SEGMENT

The insect body is divided along the anteroposterior axis into a number of individual units or segments. This organization is visible in embryos, larvae and adult insects.

LINEAGE

The cellular ancestry of a given structure. Two structures share the same lineage if the progeny of a single cell (a clone) can contribute to both. Otherwise they have different lineages.

CLONAL ANALYSIS

A type of study based on experiments in which individual cells are marked genetically during development. In the final structure the progeny of each of these cells will appear as a group of marked cells — a clone.

HOMEOBOX

A 180-bp sequence present in many developmental genes of animals and plants. It encodes a DNA-binding helix–turn–helix motif, indicating that homeobox-containing gene products function as transcription factors.

SELECTOR GENES

The concept of selector genes is intimately linked to that of compartments — body regions of fixed lineage. Selector genes become activated precisely within compartments, where they 'select' specific developmental routes. Classical examples of selector genes are engrailed, apterous and the BX-C genes.

HALTERE

A small dorsal appendage in the third thoracic segment, thought to be involved in flight control.

LIM DOMAIN

A repeat of about 60 amino acids containing cysteine and histidine residues. It is thought to be involved in protein–protein interactions.

HOMEOTIC MUTATIONS

A class of mutations in which a given organ or a segment develops in the same way as one normally present in another part of the body.

BITHORAX COMPLEX (BX-C) GENES

A group of three adjacent homeotic genes responsible for the identity of part of the thorax and the abdomen of the fly. Together with the antennapedia complex (ANT-C), it forms the Hox gene cluster in Drosophila.

GENETIC DOMAINS

A general term referring to the region of the body where a particular gene is expressed. They are usually visualized using specific antibody, DNA or RNA probes.

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Morata, G. How drosophila appendages develop. Nat Rev Mol Cell Biol 2, 89–97 (2001). https://doi.org/10.1038/35052047

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