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1.
Curr Biol ; 19(24): 2057-65, 2009 Dec 29.
Article in English | MEDLINE | ID: mdl-20005109

ABSTRACT

BACKGROUND: The vast diversity in morphology of insect wings provides an excellent model to study morphological evolution. The best-described wing modification is the specification of halteres in Drosophila by a Hox-dependent mechanism, in which a Hox gene affects the expression of genes important for wing development to modify the resulting structure. We have previously shown that highly modified beetle elytra are Hox-free structures despite their divergent morphology, suggesting another mode of evolutionary modification. RESULTS: To understand how elytra have evolved without Hox input, we have analyzed wing development in a coleopteran, Tribolium castaneum. Based on Drosophila mutant phenotypes, we first hypothesized that changes in the wing gene network might have contributed to elytral evolution. However, we found that the wing gene network defined in Drosophila is largely conserved in Tribolium and is also used to pattern the elytra. Instead, we found evidence that the exoskeleton formation has been co-opted downstream of the conserved wing gene network multiple times. We also show evidence that one of these co-options happened prior to the others, suggesting that repeated co-options may have strengthened an advantageous trait. In addition, we found that the Tribolium apterous genes are not only essential for exoskeletalization of the elytra but also are required for the proper identity of the hindwing-an unexpected role that we find to be conserved in Drosophila. CONCLUSIONS: Our findings suggest that elytral evolution has been achieved by co-opting a beneficial trait several times while conserving the main framework of wing patterning genes.


Subject(s)
Animal Structures/anatomy & histology , Biological Evolution , Gene Expression Regulation/physiology , Gene Regulatory Networks/genetics , Morphogenesis/physiology , Tribolium/anatomy & histology , Wings, Animal/anatomy & histology , Animal Structures/physiology , Animals , Gene Expression Regulation/genetics , Genes, Insect/genetics , Insect Proteins/metabolism , Pigmentation/genetics , Pigmentation/physiology , RNA Interference , Tribolium/genetics , Wings, Animal/physiology
2.
Dev Genes Evol ; 219(1): 45-51, 2009 Jan.
Article in English | MEDLINE | ID: mdl-19030877

ABSTRACT

The morphology of insect antennae varies widely among species, but our understanding of antennal development comes almost solely from studies of one species-the fruit fly, Drosophila melanogaster. Moreover, this knowledge applies mostly to adult structures, since Drosophila lacks external larval appendages. In contrast to Drosophila, the red flour beetle, Tribolium castaneum, has both larval and adult antennae, which are very different from one another in morphology. Thus, Tribolium provides an ideal system to compare modes of antennal development both within and between species. Here, we report that the Tribolium ortholog of spineless (Tc-ss) is required in both the larval and adult antennae. Knockdown of Tc-ss by RNAi during either larval or imaginal development causes transformation of the distal portion of the antennae to legs. Thus, the function of ss is conserved between Drosophila and Tribolium with respect to adult antennal specification and also between Tribolium larval and adult antennal development. The similarity of the Tc-ss RNAi phenotype to that of a classically described Tribolium mutation, antennapedia (ap) (of no relationship to the Drosophila Hox gene of the same name), led us to characterize the original ap mutation and two newly identified ap alleles. Our mapping and phenotypic data suggest that Tc-ss is the best candidate for the ap locus. These results represent a first step in characterizing larval and adult antennal patterning in Tribolium, which should provide important insights into the evolution of insect antennal development.


Subject(s)
Insect Proteins/genetics , Receptors, Aryl Hydrocarbon/genetics , Tribolium/growth & development , Tribolium/genetics , Animals , Gene Expression Regulation, Developmental , Gene Knockdown Techniques , Larva/growth & development
3.
Dev Genes Evol ; 218(3-4): 127-39, 2008 Apr.
Article in English | MEDLINE | ID: mdl-18392875

ABSTRACT

The remarkable conservation of Hox clusters is an accepted but little understood principle of biology. Some organizational constraints have been identified for vertebrate Hox clusters, but most of these are thought to be recent innovations that may not apply to other organisms. Ironically, many model organisms have disrupted Hox clusters and may not be well-suited for studies of structural constraints. In contrast, the red flour beetle, Tribolium castaneum, which has a long history in Hox gene research, is thought to have a more ancestral-type Hox cluster organization. Here, we demonstrate that the Tribolium homeotic complex (HOMC) is indeed intact, with the individual Hox genes in the expected colinear arrangement and transcribed from the same strand. There is no evidence that the cluster has been invaded by non-Hox protein-coding genes, although expressed sequence tag and genome tiling data suggest that noncoding transcripts are prevalent. Finally, our analysis of several mutations affecting the Tribolium HOMC suggests that intermingling of enhancer elements with neighboring transcription units may constrain the structure of at least one region of the Tribolium cluster. This work lays a foundation for future studies of the Tribolium HOMC that may provide insights into the reasons for Hox cluster conservation.


Subject(s)
Conserved Sequence , Genes, Homeobox , Multigene Family , Tribolium/genetics , Animals , Embryo, Nonmammalian , Evolution, Molecular , Gene Expression Profiling , Gene Expression Regulation, Developmental , Genes, Insect , Genetic Speciation , Homeodomain Proteins/genetics , Insect Proteins/genetics , Mutation , Oligonucleotide Array Sequence Analysis , Tribolium/embryology
4.
Dev Genes Evol ; 218(3-4): 141-52, 2008 Apr.
Article in English | MEDLINE | ID: mdl-18392876

ABSTRACT

The Drosophila teashirt gene acts in concert with the homeotic selector (Hox) genes to specify trunk (thorax and abdomen) identity. There has been speculation that this trunk-specifying function might be very ancient, dating back to the common ancestor of insects and vertebrates. However, other evidence suggests that the role of teashirt in trunk identity is not well conserved even within the Insecta. To address this issue, we have analyzed the function of Tc-tiotsh, the lone teashirt family member in the red flour beetle, Tribolium castaneum. Although Tc-tiotsh is important for aspects of both embryonic and imaginal development including some trunk features, we find no evidence that it acts as a trunk identity gene. We discuss this finding in the context of recent insights into the evolution and function of the Drosophila teashirt family genes.


Subject(s)
Body Patterning/genetics , Genes, Insect/physiology , Tribolium/embryology , Tribolium/genetics , Amino Acid Sequence , Animals , Cloning, Molecular , Drosophila/genetics , Drosophila Proteins/genetics , Embryo, Nonmammalian , Genes, Homeobox , Insect Proteins/metabolism , Molecular Sequence Data , Multigene Family/physiology , Phylogeny , Repressor Proteins/genetics , Sequence Homology , Thorax/embryology , Thorax/metabolism , Tissue Distribution , Transcription Factors/genetics
5.
Nature ; 452(7190): 949-55, 2008 Apr 24.
Article in English | MEDLINE | ID: mdl-18362917

ABSTRACT

Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.


Subject(s)
Genes, Insect/genetics , Genome, Insect/genetics , Tribolium/genetics , Animals , Base Composition , Body Patterning/genetics , Cytochrome P-450 Enzyme System/genetics , DNA Transposable Elements/genetics , Growth and Development/genetics , Humans , Insecticides/pharmacology , Neurotransmitter Agents/genetics , Oogenesis/genetics , Phylogeny , Proteome/genetics , RNA Interference , Receptors, G-Protein-Coupled/genetics , Receptors, Odorant/genetics , Repetitive Sequences, Nucleic Acid/genetics , Taste/genetics , Telomere/genetics , Tribolium/classification , Tribolium/embryology , Tribolium/physiology , Vision, Ocular/genetics
6.
Genetics ; 174(1): 297-307, 2006 Sep.
Article in English | MEDLINE | ID: mdl-16849608

ABSTRACT

In insects, the boundary between the embryonic head and thorax is formed by the dorsal ridge, a fused structure composed of portions of the maxillary and labial segments. However, the mechanisms that promote development of this unusual structure remain a mystery. In Drosophila, mutations in the Hox genes Sex combs reduced and Deformed have been reported to cause abnormal dorsal ridge formation, but the significance of these abnormalities is not clear. We have identified three mutant allele classes of Cephalothorax, the Tribolium castaneum (red flour beetle) ortholog of Sex combs reduced, each of which has a different effect on dorsal ridge development. By using Engrailed expression to monitor dorsal ridge development in these mutants, we demonstrate that Cephalothorax promotes the fusion and subsequent dorsolateral extension of the maxillary and labial Engrailed stripes (posterior compartments) during dorsal ridge formation. Molecular and genetic analysis of these alleles indicates that the N terminus of Cephalothorax is important for the fusion step, but is dispensable for Engrailed stripe extension. Thus, we find that specific regions of Cephalothorax are required for discrete steps in dorsal ridge formation.


Subject(s)
Drosophila Proteins/genetics , Drosophila Proteins/physiology , Genes, Insect/physiology , Transcription Factors/genetics , Transcription Factors/physiology , Tribolium/embryology , Tribolium/genetics , Alleles , Amino Acid Sequence , Animals , Animals, Genetically Modified , Base Sequence , Embryo, Nonmammalian , Gene Expression Regulation, Developmental , Head/embryology , Homeodomain Proteins/genetics , Homeodomain Proteins/metabolism , Homozygote , Insect Proteins/genetics , Insect Proteins/metabolism , Models, Biological , Molecular Sequence Data , Mutation , Phenotype , Protein Structure, Tertiary , Thorax/embryology , Tribolium/metabolism
7.
Nature ; 433(7026): 643-7, 2005 Feb 10.
Article in English | MEDLINE | ID: mdl-15703749

ABSTRACT

The two pairs of wings that are characteristic of ancestral pterygotes (winged insects) have often undergone evolutionary modification. In the fruitfly, Drosophila melanogaster, differences between the membranous forewings and the modified hindwings (halteres) depend on the Hox gene Ultrabithorax (Ubx). The Drosophila forewings develop without Hox input, while Ubx represses genes that are important for wing development, promoting haltere identity. However, the idea that Hox input is important to the morphologically specialized wing derivatives such as halteres, and not the more ancestral wings, requires examination in other insect orders. In beetles, such as Tribolium castaneum, it is the forewings that are modified (to form elytra), while the hindwings retain a morphologically more ancestral identity. Here we show that in this beetle Ubx 'de-specializes' the hindwings, which are transformed to elytra when the gene is knocked down. We also show evidence that elytra result from a Hox-free state, despite their diverged morphology. Ubx function in the hindwing seems necessary for a change in the expression of spalt, iroquois and achaete-scute homologues from elytron-like to more typical wing-like patterns. This counteracting effect of Ubx in beetle hindwings represents a previously unknown mode of wing diversification in insects.


Subject(s)
Gene Expression Regulation , Insect Proteins/metabolism , Tribolium/growth & development , Tribolium/genetics , Wings, Animal/growth & development , Wings, Animal/metabolism , Animals , Genes, Insect/genetics , Homeodomain Proteins/genetics , Homeodomain Proteins/metabolism , Insect Proteins/genetics , Molecular Sequence Data , Morphogenesis/genetics , Mutation/genetics , Phenotype , RNA Interference , Transcription Factors/genetics , Transcription Factors/metabolism
8.
Dev Genes Evol ; 214(11): 575-8, 2004 Nov.
Article in English | MEDLINE | ID: mdl-15365833

ABSTRACT

We report here on the use of RNA interference (RNAi) to create pupal and adult loss-of-function phenotypes in the red flour beetle, Tribolium castaneum, by injection of double-stranded RNA (dsRNA) into late instar larvae (we refer to this method as larval RNAi). RNAi is well-established as a useful method to mimic loss-of-function phenotypes in many organisms including insects. However, with a few exceptions (such as in the fruit fly Drosophila melanogaster), RNAi analysis has usually been limited to studies of embryogenesis. Here we demonstrate that injection of green fluorescent protein (GFP) dsRNA into the larval body cavity can inhibit GFP expression beginning shortly after injection and continuing through pupal and adult stages. RNAi analysis of the Tc-achaete-scute-homolog (Tc-ASH) revealed that larval RNAi can induce morphological defects in adult beetles, and also that larval RNAi affects the entire body rather than being localized near the site of injection. The larval RNAi technique will be useful to analyze gene functions in post-embryonic development, giving us the opportunity to study the molecular basis of adult morphological diversity in various organisms.


Subject(s)
RNA Interference/physiology , Tribolium/growth & development , Animals , Animals, Genetically Modified/genetics , Animals, Genetically Modified/growth & development , Genes, Reporter , Larva/genetics , Larva/growth & development , Pupa/genetics , Pupa/metabolism , Tribolium/genetics
9.
Genet Res ; 82(3): 155-61, 2003 Dec.
Article in English | MEDLINE | ID: mdl-15134194

ABSTRACT

The red flour beetle, Tribolium castaneum, has been selected for whole genome shotgun sequencing in the next year. In this minireview, we discuss some of the genetic and genomic tools and biological properties of Tribolium that have established its importance as an organism for agricultural and biomedical research as well as for studies of development and evolution. A Tribolium genomic database, Beetlebase, is being constructed to integrate genetic, genomic and biological data as it becomes available.


Subject(s)
Genome , Tribolium/genetics , Animals , Biological Evolution , Databases as Topic , Tribolium/embryology
10.
Mol Phylogenet Evol ; 24(3): 384-7, 2002 Sep.
Article in English | MEDLINE | ID: mdl-12220981

ABSTRACT

Evidence from Drosophila suggests that Hox genes not only specify regional identity, but have the additional function of repressing antennal development within their normal domains. This is dramatically demonstrated by a series of Hox mutants in the red flour beetle, Tribolium castaneum, and is likely an ancient function of Hox genes in insects.


Subject(s)
Coleoptera/embryology , Coleoptera/genetics , Homeodomain Proteins/genetics , Homeodomain Proteins/physiology , Tribolium/genetics , Animals , Body Patterning , Evolution, Molecular , Mutation , Phenotype
11.
Genetics ; 160(3): 1067-74, 2002 Mar.
Article in English | MEDLINE | ID: mdl-11901122

ABSTRACT

The homeotic selector genes of the red flour beetle, Tribolium castaneum, are located in a single cluster. We have sequenced the region containing the homeotic selector genes required for proper development of the head and anterior thorax, which is the counterpart of the ANTC in Drosophila. This 280-kb interval contains eight homeodomain-encoding genes, including single orthologs of the Drosophila genes labial, proboscipedia, Deformed, Sex combs reduced, fushi tarazu, and Antennapedia, as well as two orthologs of zerknüllt. These genes are all oriented in the same direction, as are the Hox genes of amphioxus, mice, and humans. Although each transcription unit is similar to its Drosophila counterpart in size, the Tribolium genes contain fewer introns (with the exception of the two zerknüllt genes), produce shorter mRNAs, and encode smaller proteins. Unlike the ANTC, this region of the Tribolium HOMC contains no additional genes.


Subject(s)
Drosophila Proteins , Drosophila melanogaster/genetics , Genes, Homeobox , Homeodomain Proteins/genetics , Nuclear Proteins , Transcription Factors , Tribolium/genetics , Amino Acid Sequence , Animals , Antennapedia Homeodomain Protein , Chromosomes, Artificial, Bacterial , Molecular Sequence Data , Polymorphism, Genetic , Repressor Proteins/genetics , Sequence Alignment , Sequence Analysis, DNA , Sequence Homology
12.
Genetics ; 160(1): 225-34, 2002 Jan.
Article in English | MEDLINE | ID: mdl-11805058

ABSTRACT

The use of eye-color mutants and their corresponding genes as scorable marker systems has facilitated the development of transformation technology in Drosophila and other insects. In the red flour beetle, Tribolium castaneum, the only currently available system for germline transformation employs the exogenous marker gene, EGFP, driven by an eye-specific promoter. To exploit the advantages offered by eye-pigmentation markers, we decided to develop a transformant selection system for Tribolium on the basis of mutant rescue. The Tribolium orthologs of the Drosophila eye-color genes vermilion (tryptophan oxygenase) and cinnabar (kynurenine 3-monooxygenase) were cloned and characterized. Conceptual translations of Tc vermilion (Tcv) and Tc cinnabar (Tccn) are 71 and 51% identical to their respective Drosophila orthologs. We used RNA interference (RNAi) to show that T. castaneum larvae lacking functional Tcv or Tccn gene products also lack the pigmented eyespots observed in wild-type larvae. Five available eye-color mutations were tested for linkage to Tcv or Tccn via recombinational mapping. No linkage was found between candidate mutations and Tccn. However, tight linkage was found between Tcv and the white-eye mutation white, here renamed vermilion(white) (v(w)). Molecular analysis indicates that 80% of the Tcv coding region is deleted in v(w) beetles. These observations suggest that the Tribolium eye is pigmented only by ommochromes, not pteridines, and indicate that Tcv is potentially useful as a germline transformation marker.


Subject(s)
Drosophila Proteins , Eye Color/genetics , Eye Proteins , Mixed Function Oxygenases/genetics , Tribolium/genetics , Tryptophan Oxygenase/genetics , Animals , Cloning, Molecular , Genes, Insect , Humans , Insect Proteins , Kynurenine 3-Monooxygenase , Larva/genetics , Molecular Sequence Data , Mutation , Sequence Analysis, DNA , Sequence Homology , Transformation, Genetic , Tribolium/enzymology
13.
Wilehm Roux Arch Dev Biol ; 192(2): 103-107, 1983 Mar.
Article in English | MEDLINE | ID: mdl-28305504

ABSTRACT

Drosophila cell lines have provided popular material for study of the mechanisms by which steroid hormones regulate cellular events. Previous investigations at the organismic or organ level have suggested that ecdysteroids are bound by a cytoplasmic receptor, and that the resulting complex translocates to the nucleus where it results in active transcription of a few genes. The protein products of these primary responding genes then modulate a larger series of secondary transcriptional changes. In cultured cells, other investigators have detected the hormonally-induced synthesis of only 4-5 new polypeptides through 72 h of treatment. Although these proteins may represent the gene products associated with the primary response, this small number of changes is surprising in view of the rapid morphological alteration of the cells and changes in such surface-mediated behavior as substrate adhesion and agglutinability observed within the same time interval. In this report, we show that lactoperoxidase-catalyzed radioiodination followed by 2-dimensional polyacrylamide gel electrophoresis and autoradiography provide an effective protocol for visualizing cell surface proteins of a Drosophila cell line. Among the more than 175 labeled species detected, comparisons of control cells with those treated by 20-hydroxyecdysone for 72 h shows at least 27 differences. We interpret these differences as the result of the secondary transcriptional response to the hormone.

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