Decision letter: Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network

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 pair-rule 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.

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Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network

10.1101/052241 ◽

2016 ◽

Cited By ~ 7

Author(s):

Erik Clark ◽

Michael Akam

Keyword(s):

Gene Expression ◽

Transcription Factor ◽

Gene Regulatory Network ◽

Regulatory Network ◽

Frequency Doubling ◽

Anteroposterior Patterning ◽

Regulatory Interactions ◽

Pair Rule Gene ◽

Gene Regulatory ◽

Pair Rule

ABSTRACTThe 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 fourteen parasegment boundaries. In contrast to earlier stages of Drosophila anteroposterior patterning, this transition is not well understood. By carefully analysing the spatiotemporal dynamics of pair-rule 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.

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Author response: Odd-paired controls frequency doubling in Drosophila segmentation by altering the pair-rule gene regulatory network

10.7554/elife.18215.040 ◽

2016 ◽

Cited By ~ 2

Author(s):

Erik Clark ◽

Michael Akam

Keyword(s):

Gene Regulatory Network ◽

Regulatory Network ◽

Frequency Doubling ◽

Author Response ◽

Pair Rule Gene ◽

Gene Regulatory ◽

Pair Rule

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Nasoniasegmentation is regulated by an ancestral insect segmentation regulatory network also present in flies

10.1101/2021.03.23.436706 ◽

2021 ◽

Author(s):

S E Taylor ◽

P K Dearden

Keyword(s):

Gene Regulatory Network ◽

Regulatory Network ◽

Single Gene ◽

Genetic Regulation ◽

Nasonia Vitripennis ◽

Genetic Changes ◽

Parasteatoda Tepidariorum ◽

Simulation Based ◽

Gene Regulatory ◽

Pair Rule

AbstractInsect segmentation is a well-studied and tractable system with which to investigate the genetic regulation of development. Though insects segment their germband using a variety of methods, modelling work implies that a single gene regulatory network can underpin the two main types of insect segmentation. This means limited genetic changes are required to explain significant differences in segmentation mode between different insects. Evidence for this idea is limited toDrosophila melanogaster, Tribolium castaneum, and the spiderParasteatoda tepidariorum, and the nature of the gene regulatory network (GRN) underlying this model has not been tested. Some insects, for exampleNasonia vitripennisandApis melliferasegment progressively, a pattern not examined in studies of this segmentation model, producing stripes at different times throughout the embryo, but not from a segment addition zone.Here we aim to understand the GRNs patterningNasoniausing a simulation-based approach. We found that an existing model ofDrosophilasegmentation (Clark, 2017) can be used to recapitulateNasonia’s progressive segmentation, if provided with altered inputs in the form of expression of the timer genesNν-caudalandNν-odd paired. We also predict limited topological changes to the pair rule network. Together this implies that very limited changes to theDrosophilanetwork are required to simulateNasoniasegmentation, despite the differences in segmentation modes, implying thatNasoniause a very similar version of an ancestral GRN also used byDrosophila.

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