Odd-paired controls frequency doubling inDrosophilasegmentation by altering the pair-rule gene regulatory network

Abstract

The Drosophila embryo transiently exhibits a double-segment periodicity, defined by the expression of seven 'pair-rule' genes, each in a pattern of seven stripes. At gastrulation, interactions between the pair-rule genes lead to frequency doubling and the patterning of 14 parasegment boundaries. In contrast to earlier stages of Drosophila anteroposterior patterning, this transition is not well understood. By carefully analysing the spatiotemporal dynamics of pairrule gene expression, we demonstrate that frequency-doubling is precipitated by multiple coordinated changes to the network of regulatory interactions between the pair-rule genes. We identify the broadly expressed but temporally patterned transcription factor, Odd-paired (Opa/ Zic), as the cause of these changes, and show that the patterning of the even-numbered parasegment boundaries relies on Opa-dependent regulatory interactions. Our findings indicate that the pair-rule gene regulatory network has a temporally modulated topology, permitting the pair-rule genes to play stage-specific patterning roles.

Speed regulation of genetic cascades allows for evolvability in the body plan specification of insects

“…The gap gene gt is also regulated by two enhancers in Drosophila, one enhancer for initialization and the other for stabilization (52). Furthermore, two genetic programs have recently been implicated to be involved in regulating pair-rule genes in Drosophila (53,54).…”

Two pair‐rule responsive enhancers regulate wingless transcription in the Drosophila blastoderm embryo

“…The seven‐stripe pattern of Prd spans the posterior border of the even numbered parasegments with strong expression in cells comprising the even numbered wg stripes and the adjacent en expressing cells that identify the anterior of the odd parasegments. This initial pattern also changes over time with an anterior broadening of the stripes followed by loss of Prd expression in cells expressing the primary stripes of Odd and the emergence of secondary Prd stripes that span the anterior border of the even numbered parasegments . The response of the wg3613u‐lacZ reporter does not match the response of wg to either loss‐of or gain‐of‐function manipulations in prd activity.…”

“…For example, Prd levels stay high in cells 1 and 8, the primary stripes of Prd expression, expression in cells 6 and 7 is reduced, and expression of secondary stripes appears in cells 4 and 5. This interpretation incorporates observations as described 33 Opa is a gray rectangle, expressed at the same level in both parasegments, Runt is a yellow trapezoid expressed in varying levels integrated over time in cells 3-6, Eve is a blue triangle, Ftz is a purple triangle, Odd is represented by orange triangles (primary stripes) or orange rectangles (secondary stripes), Prd is a light pink irregular shape with primary stripes in cells 8 and 1 and secondary expression throughout the even parasegment, stronger slp1 even numbered stripes are light blue squares, and weaker odd numbered stripes are shorter light blue rectangles. Endogenous wg expression in cells 4 and 8 is depicted below in black.…”

“…27 Recent work indicates Opa is especially important in the timely regulation of the secondary stripes of the pair-rule genes prd and odd, which in turn is critical for establishing the expression of juxtaposed wg and en stripes. 33 In light of Opa's role in wg and slp1 activation, we sought to investigate how Opa acts on the wg enhancers identified in this study.…”

“…This initial pattern also changes over time with an anterior broadening of the stripes followed by loss of Prd expression in cells expressing the primary stripes of Odd and the emergence of secondary Prd stripes that span the anterior border of the even numbered parasegments. 3,33 The response of the wg3613u-lacZ reporter does not match the response of wg to either loss-of or gain-of-function manipulations in prd activity. As described previously, 16 expression of the even numbered wg stripes is markedly reduced in prd mutant embryos ( Figure 4F).…”