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The embryonic expression pattern of a second, hitherto unrecognized, paralog of the pair-rule gene sloppy-paired in the beetle Tribolium castaneum.

ABSTRACT: In the fly Drosophila melanogaster, a hierarchic segmentation gene cascade patterns the anterior-posterior body axis of the developing embryo. Within this cascade, the pair-rule genes (PRGs) transform the more uniform patterning of the higher-level genes into a metameric pattern that first represents double-segmental units, and then, in a second step, represents a true segmental pattern. Within the PRG network, primary PRGs regulate secondary PRGs that are directly involved in the regulation of the next lower level, the segment-polarity genes (SPGs). While the complement of primary PRGs is different in Drosophila and the beetle Tribolium, another arthropod model organism, both paired (prd) and sloppy-paired (slp), acts as secondary PRGs. In earlier studies, the interaction of PRGs and the role of the single slp ortholog in Tribolium have been investigated in some detail revealing conserved and diverged aspects of PRG function. In this study, I present the identification and the analysis of embryonic expression patterns of a second slp gene (called slp2) in Tribolium. While the previously identified gene, slp, is expressed in a typical PRG pattern, expression of slp2 is more similar to that of the downstream-acting SPGs, and shows expression similarities to slp2 in Drosophila. The previously reported differences between the function of slp in Drosophila and Tribolium may partially account for the function of the newly identified second slp paralog in Tribolium, and it may therefore be advised to conduct further studies on PRG function in the beetle.

SUBMITTER: Janssen R

PROVIDER: S-EPMC7260273 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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The embryonic expression pattern of a second, hitherto unrecognized, paralog of the pair-rule gene sloppy-paired in the beetle Tribolium castaneum.

Janssen Ralf R

Development genes and evolution 20200520 3

In the fly Drosophila melanogaster, a hierarchic segmentation gene cascade patterns the anterior-posterior body axis of the developing embryo. Within this cascade, the pair-rule genes (PRGs) transform the more uniform patterning of the higher-level genes into a metameric pattern that first represents double-segmental units, and then, in a second step, represents a true segmental pattern. Within the PRG network, primary PRGs regulate secondary PRGs that are directly involved in the regulation of ...[more]

PMID: 32430691

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Project description:BackgroundThe Drosophila larval head is evolutionarily derived at the genetic and morphological level. In the beetle Tribolium castaneum, development of the larval head more closely resembles the ancestral arthropod condition. Unlike in Drosophila, a knirps homologue (Tc-kni) is required for development of the antennae and mandibles. However, published Tc-kni data are restricted to cuticle phenotypes and Tc-even-skipped and Tc-wingless stainings in knockdown embryos. Hence, it has remained unclear whether the entire antennal and mandibular segments depend on Tc-kni function, and whether the intervening intercalary segment is formed completely. We address these questions with a detailed examination of Tc-kni function.ResultsBy examining the expression of marker genes in RNAi embryos, we show that Tc-kni is required only for the formation of the posterior parts of the antennal and mandibular segments (i.e. the parasegmental boundaries). Moreover, we find that the role of Tc-kni is distinct in these segments: Tc-kni is required for the initiation of the antennal parasegment boundary, but only for the maintenance of the mandibular parasegmental boundary. Surprisingly, Tc-kni controls the timing of expression of the Hox gene Tc-labial in the intercalary segment, although this segment does form in the absence of Tc-kni function. Unexpectedly, we find that the pair-rule gene Tc-even-skipped helps set the posterior boundary of Tc-kni expression in the mandible. Using the mutant antennaless, a likely regulatory Null mutation at the Tc-kni locus, we provide evidence that our RNAi studies represent a Null situation.ConclusionsTc-kni is required for the initiation of the antennal and the maintenance of the mandibular parasegmental boundaries. Tc-kni is not required for specification of the anterior regions of these segments, nor the intervening intercalary segment, confirming that Tc-kni is not a canonical 'gap-gene'. Our finding that a gap gene orthologue is regulated by a pair rule gene adds to the view that the segmentation gene hierarchies differ between Tribolium and Drosophila upstream of the pair rule gene level. In Tribolium, as in Drosophila, head and trunk segmentation gene networks cooperate to pattern the mandibular segment, albeit involving Tc-kni as novel component.

Project description:UNLABELLED: BACKGROUND:The biting mandible of the arthropods is thought to have evolved in the ancestor of the insects, crustaceans and myriapods: the Mandibulata. A unique origin suggests a common set of developmental genes will be required to pattern the mandible in different arthropods. To date we have functional studies on patterning of the mandibular segment of Drosophila melanogaster showing in particular the effects of the gene cap'n'collar (cnc), however, the dipteran head is far from representative of insects or of more distantly related mandibulates; Drosophila does not even possess a mandibular appendage. To study the development of a more representative insect mandible, we chose the red flour beetle Tribolium castaneum and investigated the function of the Tribolium orthologs of cap'n'collar (Tc-cnc) and the Hox gene Deformed (Tc-Dfd). In order to determine the function of Tc-cnc and Tc-Dfd, transcripts were knocked down by maternal RNA interference (RNAi). The effects of gene knockdown were examined in the developing embryos and larvae. The effect of Tc-cnc and Tc-Dfd knockdown on the expression of other genes was determined by using in situ hybridization on Tribolium embryos. RESULTS:Our analyses show that Tc-cnc is required for specification of the identity of the mandibular segment of Tribolium and differentiates the mandible from maxillary identity. Loss of Tc-cnc function results in a transformation of the mandible to maxillary identity as well as deletion of the labrum. Tc-Dfd and the Tribolium homolog of proboscipedia (Tc-mxp?=?maxillopedia), Hox genes that are required to pattern the maxillary appendage, are expressed in a maxilla-like manner in the transformed mandible. Tribolium homologs of paired (Tc-prd) and Distal-less (Tc-Dll) that are expressed in the endites and telopodites of embryonic appendages are also expressed in a maxilla-like manner in the transformed mandible.We also show that Tc-Dfd is required to activate the collar of Tc-cnc expression in the mandibular segment but not the cap expression in the labrum. Tc-Dfd is also required for the activation of Tc-prd in the endites of the mandible and maxillary appendages. CONCLUSIONS:Tc-cnc is necessary for patterning the mandibular segment of Tribolium. Together, Tc-cnc and Tc-Dfd cooperate to specify mandibular identity, as in Drosophila. Expression patterns of the homologs of cnc and Dfd are conserved in mandibulate arthropods suggesting that the mandible specifying function of cnc is likely to be conserved across the mandibulate arthropods.

Dataset Information

The embryonic expression pattern of a second, hitherto unrecognized, paralog of the pair-rule gene sloppy-paired in the beetle Tribolium castaneum.

Publications

The embryonic expression pattern of a second, hitherto unrecognized, paralog of the pair-rule gene sloppy-paired in the beetle Tribolium castaneum.

Similar Datasets

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