Regulation of Body Pigmentation by the Abdominal-B Hox Protein and Its Gain and Loss in Drosophila Evolution

Howard Hughes Medical Institute and Laboratory of Molecular Biology, University of Wisconsin, 1525 Linden Drive, Madison, WI 53706, USA.
Cell (Impact Factor: 32.24). 07/2006; 125(7):1387-99. DOI: 10.1016/j.cell.2006.04.043
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Hox genes have been implicated in the evolution of many animal body patterns, but the molecular events underlying trait modification have not been elucidated. Pigmentation of the posterior male abdomen is a recently acquired trait in the Drosophila melanogaster lineage. Here, we show that the Abdominal-B (ABD-B) Hox protein directly activates expression of the yellow pigmentation gene in posterior segments. ABD-B regulation of pigmentation evolved through the gain of ABD-B binding sites in a specific cis-regulatory element of the yellow gene of a common ancestor of sexually dimorphic species. Within the melanogaster species group, male-specific pigmentation has subsequently been lost by at least three different mechanisms, including the mutational inactivation of a key ABD-B binding site in one lineage. These results demonstrate how Hox regulation of traits and target genes is gained and lost at the species level and have general implications for the evolution of body form at higher taxonomic levels.

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    • "Evolutionary modification of this developmental process in different animal lineages has given rise to the vast diversity of body form and function observed across the Metazoa today. Many evolutionary changes to genes have been documented including gene duplications (Brooke et al. 1998; Putnam et al. 2008), coding sequence alterations (Fondon and Garner 2004), and modifications to gene expression (Jeong et al. 2006). Although much focus has been on the evolution of cis-regulatory elements that affect gene expression (Putnam et al. 2008; Chan et al. 2010), there are also trans-acting factors that should not be overlooked. "
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    ABSTRACT: MicroRNAs (miRNAs) are involved in post-transcriptional regulation of gene expression l regulation of gene expressionvelopment to reory genese likely false positives. too approximate.rgence times that I cited init. Since several miRNAs are known to affect the stability or translation of developmental regulatory genes, the origin of novel miRNAs may have contributed to the evolution of developmental processes and morphology. Lepidoptera (butterflies and moths) is a species-rich clade with a well-established phylogeny and abundant genomic resources, thereby representing an ideal system in which to study miRNA evolution. We sequenced small RNA libraries from developmental stages of two divergent lepidopterans, Cameraria ohridella (Horse chestnut Leafminer) and Pararge aegeria (Speckled Wood butterfly), discovering 90 and 81 conserved miRNAs respectively, and many species-specific miRNA sequences. Mapping miRNAs onto the lepidopteran phylogeny reveals rapid miRNA turnover and an episode of miRNA fixation early in lepidopteran evolution, implying that miRNA acquisition accompanied the early radiation of the Lepidoptera. One lepidopteran-specific miRNA gene, miR-2768, is located within an intron of the homeobox gene invected, involved in insect segmental and wing patterning. We identified cubitus interruptus (ci) as a likely direct target of miR-2768, and validated this suppression using a luciferase assay system. We propose a model by which miR-2768 modulates expression of ci in the segmentation pathway and in patterning of lepidopteran wing primordia. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Molecular Biology and Evolution 01/2015; 32(5). DOI:10.1093/molbev/msv004 · 9.11 Impact Factor
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    • "In the posterior abdominal segments of females, Abd-B and a female-isoform of Dsx directly activate bab expression, and then Bab represses yellow expression [39], [41]. In those of males, Abd-B and a male-isoform of Dsx repress bab expression, resulting in the male- and segment-specific patterns of yellow expression [39], [41]. Suppressive regulations of bab with sexually dimorphic pigmentation would have independently occurred several times, at least within the genus Drosophila [42], [43]. "
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    ABSTRACT: Most hymenopteran species exhibit conspicuous sexual dimorphism due to ecological differences between the sexes. As hymenopteran genomes, under the haplodiploid genetic system, exhibit quantitative differences between sexes while remaining qualitatively identical, sexual phenotypes are assumed to be expressed through sex-specific gene usage. In the present study, the molecular basis for expression of sexual dimorphism in a queenless ant, Diacamma sp., which exhibits a distinct color dimorphism, was examined. Worker females of the species appear bluish-black, while winged males exhibit a yellowish-brown body color. Initially, observations of the pigmentation processes during pupal development revealed that black pigmentation was present in female pupae but not in males, suggesting that sex-specific melanin synthesis was responsible for the observed color dimorphism. Therefore, five orthologs of the genes involved in the insect melanin synthesis (yellow, ebony, tan, pale and dopa decarboxylase) were subcloned and their spatiotemporal expression patterns were examined using real-time quantitative RT-PCR. Of the genes examined, yellow, which plays a role in black melanin synthesis in insects, was expressed at higher levels in females than in males throughout the entire body during the pupal stage. RNA interference of yellow was then carried out in order to determine the gene function, and produced females with a more yellowish, brighter body color similar to that of males. It was concluded that transcriptional regulation of yellow was responsible for the sexual color dimorphism observed in this species.
    PLoS ONE 03/2014; 9(3):e92875. DOI:10.1371/journal.pone.0092875 · 3.23 Impact Factor
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    • "These include direct CRE interactions between Abd-B and the yellow body element CRE (Jeong et al., 2006) and both Abd-B and Dsx with the bab loci dimorphic element CRE (Williams et al., 2008) (Fig. 1B). Repression of yellow (Jeong et al., 2006) and presumably the tan gene expression is mediated by the Bab proteins, but whether regulation is direct or indirect remains unknown. Moreover, no direct regulators of ebony are known. "
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    ABSTRACT: Trait development results from the collaboration of genes interconnected in hierarchical networks that control which genes are activated during the progression of development. While networks are understood to change over developmental time, the alterations that occur over evolutionary times are much less clear. A multitude of transcription factors and a far greater number of linkages between transcription factors and cis-regulatory elements (CREs) have been found to structure well-characterized networks, but the best understood networks control traits that are deeply conserved. Fruit fly abdominal pigmentation may represent an optimal setting to study network evolution, as this trait diversified over short evolutionary time spans. However, the current understanding of the underlying network includes a small set of transcription factor genes. Here, we greatly expand this network through an RNAi-screen of 558 transcription factors. We identified 26 genes, including previously implicated abd-A, Abd-B, bab1, bab2, dsx, exd, hth, and jing, as well as 20 novel factors with uncharacterized roles in pigmentation development. These include genes which promote pigmentation, suppress pigmentation, and some that have either male- or female-limited effects. We show that many of these transcription factors control the reciprocal expression of two key pigmentation enzymes, whereas a subset controls the expression of key factors in a female-specific circuit. We found the pupal Abd-A expression pattern was conserved between species with divergent pigmentation, indicating diversity resulted from changes to other loci. Collectively, these results reveal a greater complexity of the pigmentation network, presenting numerous opportunities to map transcription factor-CRE interactions that structure trait development and numerous candidate loci to investigate as potential targets of evolution.
    Developmental Biology 11/2013; 385(2). DOI:10.1016/j.ydbio.2013.11.013 · 3.55 Impact Factor
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