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Conservation and variation in pair-rule gene expression and function in the intermediate-germ beetle Dermestes maculatus.

ABSTRACT: A set of pair-rule (PR) segmentation genes (PRGs) promotes the formation of alternate body segments in Drosophila melanogaster Whereas Drosophila embryos are long-germ, with segments specified more or less simultaneously, most insects add segments sequentially as the germband elongates. The hide beetle Dermestes maculatus represents an intermediate between short- and long-germ development, ideal for comparative study of PRGs. We show that eight of nine Drosophila PRG orthologs are expressed in stripes in Dermestes Functional results parse these genes into three groups: Dmac-eve, -odd and -run play roles in both germband elongation and PR patterning; Dmac-slp and -prd function exclusively as complementary, classic PRGs, supporting functional decoupling of elongation and segment formation; and orthologs of ftz, ftz-f1, h and opa show more variable function in Dermestes and other species. While extensive cell death generally prefigured Dermestes PRG RNAi-mediated cuticle defects, an organized region with high mitotic activity near the margin of the segment addition zone is likely to have contributed to truncation of eveRNAi embryos. Our results suggest general conservation of clock-like regulation of PR stripe addition in sequentially segmenting species while highlighting regulatory rewiring involving a subset of PRG orthologs.

SUBMITTER: Xiang J

PROVIDER: S-EPMC5769621 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Conservation and variation in pair-rule gene expression and function in the intermediate-germ beetle Dermestes maculatus.

Xiang Jie J Reding Katie K Heffer Alison A Pick Leslie L

Development (Cambridge, England) 20171030 24

A set of pair-rule (PR) segmentation genes (PRGs) promotes the formation of alternate body segments in Drosophila melanogaster Whereas Drosophila embryos are long-germ, with segments specified more or less simultaneously, most insects add segments sequentially as the germband elongates. The hide beetle Dermestes maculatus represents an intermediate between short- and long-germ development, ideal for comparative study of PRGs. We show that eight of nine Drosophila PRG ...[more]

PMID: 29084804

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Project description:BackgroundUnderstanding how genes change during evolution to direct the development of diverse body plans is a major goal of the evo-devo field. Achieving this will require the establishment of new model systems that represent key points in phylogeny. These new model systems must be amenable to laboratory culture, and molecular and functional approaches should be feasible. To date, studies of insects have been best represented by the model system Drosophila melanogaster. Given the enormous diversity represented by insect taxa, comparative studies within this clade will provide a wealth of information about the evolutionary potential and trajectories of alternative developmental strategies.ResultsHere we established the beetle Dermestes maculatus, a member of the speciose clade Coleoptera, as a new insect model system. We have maintained a continuously breeding culture in the lab and documented Dermestes maculatus embryogenesis using nuclear and phalloidin staining. Anterior segments are specified during the blastoderm stage before gastrulation, and posterior segments are added sequentially during germ band elongation. We isolated and studied the expression and function of the pair-rule segmentation gene paired in Dermestes maculatus. In this species, paired is expressed in stripes during both blastoderm and germ band stages: four primary stripes arise prior to gastrulation, confirming an intermediate-germ mode of development for this species. As in other insects, these primary stripes then split into secondary stripes. To study gene function, we established both embryonic and parental RNAi. Knockdown of Dmac-paired with either method resulted in pair-rule-like segmentation defects, including loss of Engrailed expression in alternate stripes.ConclusionsThese studies establish basic approaches necessary to use Dermestes maculatus as a model system. Methods are now available for use of this intermediate-germ insect for future studies of the evolution of regulatory networks controlling insect segmentation, as well as of other processes in development and homeostasis. Consistent with the role of paired in long-germ Drosophila and shorter-germ Tribolium, paired functions as a pair-rule segmentation gene in Dermestes maculatus. Thus, paired retains pair-rule function in insects with different modes of segment addition.

Dataset Information

Conservation and variation in pair-rule gene expression and function in the intermediate-germ beetle Dermestes maculatus.

Publications

Conservation and variation in pair-rule gene expression and function in the intermediate-germ beetle <i>Dermestes maculatus</i>.

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