A strategy for mapping bicoid on the phylogenetic tree.
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Biomedical subjects
Publications and source records attributed to U Schmidt-Ott.
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In Drosophila, the establishment of the larval head and thorax depends on the transcription factors BICOID and HUNCHBACK, and on signalling mediated by the receptor tyrosine kinase TORSO. Genetic experiments described in two recent papers(1, 2) demonstrate that these factors can, to a large extent, replace each other, revealing a surprising degree of plasticity in establishing larval anterior structures. The commutability of developmental factors might in part reflect the evolutionary history of the system. BioEssays 23:8-11, 2001.
The Drosophila gene bicoid functions at the beginning of a gene cascade that specifies anterior structures in the embryo. Its transcripts are localized at the anterior pole of the oocyte, giving rise to a Bicoid protein gradient, which regulates the spatially restricted expression of target genes along the anterior-posterior axis of the embryo in a concentration-dependent manner. The morphogen function of Bicoid requires the coactivity of the zinc finger transcription factor Hunchback, which is expressed in a Bicoid-dependent fashion in the anterior half of the embryo. Whereas hunchback is conserved throughout insects, bicoid homologs are known only from cyclorrhaphan flies. Thus far, identification of hunchback and bicoid homologs rests only on sequence comparison. In this study, we used double-stranded RNA interference (RNAi) to address the function of bicoid and hunchback homologs in embryos of the lower cyclorrhaphan fly Megaselia abdita (Phoridae). Megaselia-hunchback RNAi causes hunchback-like phenotypes as observed in Drosophila, but Megaselia-bicoid RNAi causes phenotypes different from corresponding RNAi experiments in Drosophila and bicoid mutant embryos. Megaselia-bicoid is required not only for the head and thorax but also for the development of four abdominal segments. This difference between Megaselia and Drosophila suggests that the range of functional bicoid activity has been reduced in higher flies.
In developing insect eggs the cells of the blastoderm adopt either an embryonic or an extraembryonic fate. The extraembryonic tissue consists of epithelia, termed amnion and serosa, which wrap the germ band embryo. The serosa develops directly from part of the blastoderm and surrounds the embryo as well as the yolk. The amnion develops from the margins of the germ band and in most insect species generates a transient ventral cavity for the developing embryo. The amniotic cavity and the serosa have been reduced in the course of dipteran evolution. The insect order of Diptera includes the paraphyletic Nematocera, including gnats and mosquitoes, and the more derived monophyletic Brachycera, the true flies. Nematocera develop within an amniotic cavity and the surrounding serosa, whereas cyclorrhaphan Brachycera do not. This observation implies that the amnion and serosa have been reduced before the radiation of the monophyletic cyclorrhaphan flies. Here I show that an amniotic cavity is formed during embryogenesis of the horsefly Haematopota pluvialis (Tabanidae) and the dancefly Empis livida (Empididae). The results suggest that extraembryonic tissue was reduced in the stem lineage of cyclorrhaphan flies, with consequences for the molecular basis of pattern formation along the anterior-posterior axis of the embryo.
The Drosophila gene bicoid functions as the anterior body pattern organizer of Drosophila. Embryos lacking maternally expressed bicoid fail to develop anterior segments including head and thorax. In wild-type eggs, bicoid mRNA is localized in the anterior pole region and the bicoid protein forms an anterior-to-posterior concentration gradient. bicoid activity is required for transcriptional activation of zygotic segmentation genes and the translational suppression of uniformly distributed maternal caudal mRNA in the anterior region of the embryo. caudal genes as well as other homeobox genes or members of the Drosophila segmentation gene cascade have been found to be conserved in animal evolution. In contrast, bicoid homologs have been identified only in close relatives of the schizophoran fly Drosophila. This poses the question of how the bicoid gene evolved and adopted its unique function in organizing anterior-posterior polarity. We have cloned bicoid from a basal cyclorrhaphan fly, Megaselia abdita (Phoridae, Aschiza), and show that the gene originated from a recent duplication of the direct homolog of the vertebrate gene Hox3, termed zerknüllt, which specifies extraembryonic tissues in insects.
The gene Toll (Tl) encodes a maternally supplied interleukin 1 receptor-related transmembrane protein, a key component required to establish dorsoventral polarity in the Drosophila embryo. We have isolated Tl homologs of a primitive dipteran, Clogmia albipunctata, and of the beetle Tribolium castaneum. Tribolium Tl protein (Tl) lacks sequences in the C-terminal portion of the cytoplasmic domains that are conserved in the dipteran homologs. The Tl homolog of Tribolium mediates the ventralizing activity when expressed as a gain-of-function variant in transgenic Drosophila, indicating that the sequences conserved in the Diptera are not essential for Tl signaling. In contrast to Drosophila where Tl gene expression occurs maternally and supplies uniformly distributed Tl in the egg membrane, Tl transcripts form a ventral-to-dorsal gradient in the Tribolium blastoderm stage embryo. This localized expression pattern of Tl transcripts, as compared with the strong maternal and ubiquitous expression in Drosophila and Clogmia embryos, suggests that dorsoventral patterning in long-germ band and short-germ band insects involves the same components but different modes of their action.
The anterior determinant bicoid (bcd) of Drosophila is a homeodomain protein. It forms an anterior-to-posterior gradient in the embryo and activates, in a concentration-dependent manner, several zygotic segmentation genes during blastoderm formation. Its posterior counterpart, the homeodomain transcription factor caudal (cad), forms a concentration gradient in the opposite direction, emanating from evenly distributed messenger RNA in the egg. In embryos lacking bcd activity as a result of mutation, the cad gradient fails to form and cad becomes evenly distributed throughout the embryo. This suggests that bcd may act in the region-specific control of cad mRNA translation. Here we report that bcd binds through its homeodomain to cad mRNA in vitro, and exerts translational control through a bcd-binding region of cad mRNA.
The development of the insect head tagma involves massive rearrangements and secondary fusions of segment anlagen during embryogenesis. Due to the lack of reliable morphological markers, the number, identity, and sequence of the head segments, particularly in the pregnathal region, are still a matter of ongoing debates. We examined the complex array of internal structures of the embryonic Drosophila melanogaster head such as the sensory structures and nerves of the peripheral and stomatogastric nervous systems, and we used embryonic head mutations causing a lack of overlapping segment anlagen to unravel the segmental identity and the sequence of the neural elements. Our results provide evidence for seven distinct segments in the Drosophila head, each characterized by a specific set of sensory neurons, consistent with the proposal that insects, myriapods, and crustaceans share a monophyletic evolutionary tree from a common annelid-like ancestor.
Based on the expression pattern of the segment polarity genes engrailed and wingless during the embryonic development of the larval head, we found evidence that the head of Drosophila consists of remnants of seven segments (4 pregnathal and 3 gnathal) all of which contribute cells to neuromeres in the central nervous system. Until completion of germ band retraction, the four pregnathal segment remnants and their corresponding neuromeres become arranged in an S-shape. We discuss published evidence for seven head segments and morphogenetic movements during head formation in various insects (and crustaceans).