The origins of the Drosophila leg revealed by the cis-regulatory architecture of the Distalless gene

The origins of the Drosophila leg revealed by the cis-regulatory architecture of the Distalless gene

Daniel J. McKay, Carlos Estella and Richard S. Mann

Development 136, 61-71 (2009) doi: doi: 10.1242/dev.02997510.1242/dev.029975

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Limb development requires the elaboration of a proximodistal (PD) axis,
which forms orthogonally to previously defined dorsoventral (DV) and
anteroposterior (AP) axes. In arthropods, the PD axis of the adult leg is
subdivided into two broad domains, a proximal coxopodite and a distal
telopodite. We show that the progressive subdivision of the PD axis into these
two domains occurs during embryogenesis and is reflected in the cis-regulatory
architecture of the Distalless (Dll) gene. Early
Dll expression, governed by the Dll304 enhancer, is in cells
that can give rise to both domains of the leg as well as to the entire dorsal
(wing) appendage. A few hours after Dll304 is activated, the activity
of this enhancer fades, and two later-acting enhancers assume control over
Dll expression. The LT enhancer is expressed in cells that
will give rise to the entire telopodite, and only the telopodite. By contrast,
cells that activate the DKO enhancer will give rise to a
leg-associated larval sensory structure known as the Keilin’s organ (KO).
Cells that activate neither LT nor DKO, but had activated
Dll304, will give rise to the coxopodite. In addition, we describe
the trans-acting signals controlling the LT and DKO
enhancers, and show, surprisingly, that the coxopodite progenitors begin to
proliferate ~24 hours earlier than the telopodite progenitors. Together, these findings provide a complete and high-resolution fate map of the Drosophila appendage primordia, linking the primary domains to
specific cis-regulatory elements in Dll.

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