From development to biodiversity–Tribolium castaneum, an insect model organism for short germband development

Department of Animal Genetics, Institute for Cell Biology, University of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, Germany.
Development Genes and Evolution (Impact Factor: 2.44). 05/2008; 218(3-4):119-26. DOI: 10.1007/s00427-008-0214-3
Source: PubMed


Insect embryogenesis is best understood in the fruit fly Drosophila. However, Drosophila embryogenesis shows evolutionary-derived features: anterior patterning is controlled by a highly derived Hox gene bicoid, the body segments form almost simultaneously and appendages develop from imaginal discs. In contrast, embryogenesis of the red flour beetle Tribolium castaneum displays typical features in anterior patterning, axis and limb formation shared with most insects, other arthropods as well as with vertebrates. Anterior patterning depends on the conserved homeobox gene orthodenticle, the main body axis elongates sequentially and limbs grow continuously starting from an appendage bud. Thus, by analysing developmental processes in the beetle at the molecular and cellular level, inferences can be made for similar processes in other arthropods. With the completion of sequencing the Tribolium genome, the door is now open for post-genomic studies such as RNA expression profiling, proteomics and functional genomics to identify beetle-specific gene circuits.

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    • "To polarise this comparison, we used the arthropod Tribolium castaneum, for which a high quality genome sequence is available [44]. T. castaneum development is considered less derived than that of the major arthropod model Drosophila melanogaster[45]. The OrthoMCL pipeline accurately clusters orthologous proteins, facilitating the complex task of grouping proteins that are likely to share biological function in divergent organisms [46], and performs better than approaches that simply use domain presence information or aggregative approaches such as psiBLAST [47]. "
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    ABSTRACT: The genetics of development in the nematode Caenorhabditis elegans has been described in exquisitedetail. The phylum Nematoda has two classes: Chromadorea (which includes C. elegans) and theEnoplea. While the development of many chromadorean species resembles closely that of C. elegans,enoplean nematodes show markedly different patterns of early cell division and cell fate assignment.Embryogenesis of the enoplean Romanomermis culicivorax has been studied in detail, but the geneticcircuitry underpinning development in this species has not been explored. We generated a draft genome for R. culicivorax and compared its gene content with that of C. elegans,a second enoplean, the vertebrate parasite Trichinella spiralis, and a representative arthropod,Tribolium castaneum. This comparison revealed that R. culicivorax has retained components of theconserved ecdysozoan developmental gene toolkit lost in C. elegans. T. spiralis has independentlylost even more of this toolkit than has C. elegans. However, the C. elegans toolkit is not simply depauperate, as many novel genes essential for embryogenesis in C. elegans are not found in, or haveonly extremely divergent homologues in R. culicivorax and T. spiralis. Our data imply fundamentaldifferences in the genetic programmes not only for early cell specification but also others such asvulva formation and sex determination. Despite the apparent morphological conservatism, major differences in the molecular logic of developmenthave evolved within the phylum Nematoda. R. culicivorax serves as a tractable system to contrast C. elegans and understand how divergent genomic and thus regulatory backgrounds nevertheless generate a conserved phenotype. The R. culicivorax draft genome will promote use of this species as a research model.
    BMC Genomics 12/2013; 14(1):923. DOI:10.1186/1471-2164-14-923 · 3.99 Impact Factor
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    • "Here, we demonstrate transient labeling methods for strong, homogeneous and persistent expression of fluorescent markers in embryos of the red flour beetle Tribolium castaneum. Tribolium is a well-established arthropod model representing an ideal system with which to study the diversity and evolution of developmental mechanisms (Brown et al., 2009; Schröder et al., 2008). Tribolium is supported by an extensive repertoire of genetic and genomic resources (Beeman et al., 1989; Berghammer et al., 1999; Posnien et al., 2009; Richards et al., 2008; Trauner et al., 2009), but is still lagging behind in imaging resources. "
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    ABSTRACT: Studies on new arthropod models such as the beetle Tribolium castaneum are shifting our knowledge of embryonic patterning and morphogenesis beyond the Drosophila paradigm. In contrast to Drosophila, Tribolium embryos exhibit the short-germ type of development and become enveloped by extensive extra-embryonic membranes, the amnion and serosa. The genetic basis of these processes has been the focus of active research. Here, we complement genetic approaches with live fluorescence imaging of Tribolium embryos to make the link between gene function and morphogenetic cell behaviors during blastoderm formation and differentiation, germband condensation and elongation, and extra-embryonic development. We first show that transient labeling methods result in strong, homogeneous and persistent expression of fluorescent markers in Tribolium embryos, labeling the chromatin, membrane, cytoskeleton or combinations thereof. We then use co-injection of fluorescent markers with dsRNA for live imaging of embryos with disrupted caudal gene function caused by RNA interference. Using these approaches, we describe and compare cell and tissue dynamics in Tribolium embryos with wild-type and altered fate maps. We find that Tribolium germband condensation is effected by cell contraction and intercalation, with the latter being dependent on the anterior-posterior patterning system. We propose that germband condensation drives initiation of amnion folding, whereas expansion of the amniotic fold and closure of the amniotic cavity are likely driven by contraction of an actomyosin cable at the boundary between the amnion and serosa. Our methodology provides a comprehensive framework for testing quantitative models of patterning, growth and morphogenetic mechanisms in Tribolium and other arthropod species.
    Development 08/2013; 140(15):3210-20. DOI:10.1242/dev.096271 · 6.46 Impact Factor
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    • "Because of the cuticular reduction accompanying the process, embryonic head defects can be interpreted only with difficulty in Drosophila. Tribolium exhibits an typical insect larval head with all typical appendages (Klingler 2004; Posnien et al. 2010; Schröder et al. 2008) and markers for specific head regions (Schinko et al. 2008). In addition, the Tribolium model is a representative of the most species-rich metazoan taxon, the Coleoptera, which represent one fourth of all described animals (Hunt et al. 2007), including many important pest species such as the boll weevil, corn rootworm, Colorado potato beetle and comprising species with intriguing evolutionary adaptations like the horns of horned beetles (Moczek et al. 2006). "
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    ABSTRACT: Insect gene function has mainly been studied in the fruit fly Drosophila melanogaster because in this species many techniques and resources are available for gene knock down and the ectopic activation of gene function. However, in order to study biological aspects that are not represented by the Drosophila model, and in order to test to what degree gene functions are conserved within insects and what changes in gene function accompanied the evolution of novel traits, the establishment of respective tools in other insect species is required. While gene knock down can be induced by RNA interference in many insects, methods to misexpress genes are much less developed. In order to allow misexpression of genes in a timely controlled manner in the red flour beetle Tribolium castaneum, we have established a heat shock-mediated misexpression system. We show that endogenous heat shock elements perform better than artificial heat shock elements derived from vertebrates. We carefully determine the optimal conditions for heat shock and define a core promoter for use in future constructs. Finally, using this system, we study the effects of misexpressing the head patterning gene Tc-orthodenticle1 (Tc-otd1), We show that Tc-otd1 suppresses Tc-wingless (Tc-wg) in the trunk and to some degree in the head.
    Development Genes and Evolution 07/2012; 222(5):287-98. DOI:10.1007/s00427-012-0412-x · 2.44 Impact Factor
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Reinhard Schröder