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An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian.

Ayyar S, Negre B, Simpson P, Stollewerk A - BMC Biol. (2010)

Bottom Line: The SOPEs of the spider Cupiennius salei and the insect Tribolium castaneum are shown to be functional in transgenic Drosophila.This would place the origin of this regulatory sequence as far back as the last common ancestor of the Arthropoda, that is, in the Cambrian, 550 million years ago.The SOPE is not detectable by inter-specific sequence comparison, raising the possibility that other ancient regulatory modules in invertebrates might have escaped detection.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.

ABSTRACT

Background: An increasing number of publications demonstrate conservation of function of cis-regulatory elements without sequence similarity. In invertebrates such functional conservation has only been shown for closely related species. Here we demonstrate the existence of an ancient arthropod regulatory element that functions during the selection of neural precursors. The activity of genes of the achaete-scute (ac-sc) family endows cells with neural potential. An essential, conserved characteristic of proneural genes is their ability to restrict their own activity to single or a small number of progenitor cells from their initially broad domains of expression. This is achieved through a process called lateral inhibition. A regulatory element, the sensory organ precursor enhancer (SOPE), is required for this process. First identified in Drosophila, the SOPE contains discrete binding sites for four regulatory factors. The SOPE of the Drosophila asense gene is situated in the 5' UTR.

Results: Through a manual comparison of consensus binding site sequences we have been able to identify a SOPE in UTR sequences of asense-like genes in species belonging to all four arthropod groups (Crustacea, Myriapoda, Chelicerata and Insecta). The SOPEs of the spider Cupiennius salei and the insect Tribolium castaneum are shown to be functional in transgenic Drosophila. This would place the origin of this regulatory sequence as far back as the last common ancestor of the Arthropoda, that is, in the Cambrian, 550 million years ago.

Conclusions: The SOPE is not detectable by inter-specific sequence comparison, raising the possibility that other ancient regulatory modules in invertebrates might have escaped detection.

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Conserved domains of the arthropod ASH and Ase proteins. Alignment of the bHLH domain, Ase motif and carboxy-terminal motif of ASH and Ase. Am, Apis mellifera; Cs, Cupiennius salei; Dm, Drosophila melanogasster; Dp, Daphnia pulex; Gm, Glomeris marginata; Sm, Strigamia maritima; Tc, Tribolium castaneum.
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Figure 1: Conserved domains of the arthropod ASH and Ase proteins. Alignment of the bHLH domain, Ase motif and carboxy-terminal motif of ASH and Ase. Am, Apis mellifera; Cs, Cupiennius salei; Dm, Drosophila melanogasster; Dp, Daphnia pulex; Gm, Glomeris marginata; Sm, Strigamia maritima; Tc, Tribolium castaneum.

Mentions: In order to classify proneural and precursor-specific genes in other arthropod groups, we applied the above criteria to recently published sequences. Two ASH genes were described in the crustacean Triops longicaudatus [24]. The authors show that the deduced amino acid sequence of Tl-ASH1 bears the ASH carboxy-terminal domain, while this sequence is not conserved in Tl-ASH2. We identified the Ase motif in Tl-ASH2, confirming that this gene is in fact an asense orthologue (Figure 1). Furthermore, we detected single ASH and ase orthologues, Dpu-ASH and Dpu-ase, in the Daphnia pulex genome (Daphnia Genome Consortium), which can clearly be distinguished by the presence of the respective domains (Figure 1). The spider Cupiennius salei (chelicerate) displays two ASH orthologues [23] but sequence analysis does not unambiguously distinguish a bona fide ase gene in this species. The carboxy-terminal domain of CsASH1 displays a greater similarity to that of insect and crustacean ASH proteins (56% amino acid identity) than does that of CsASH2 (30%). However, neither CsASH1 nor CsASH2 contain the five amino acid motif characteristic of Ase (Figure 1). A single orthologue has been identified in each of the myriapods Glomeris marginata [26] and Strigamia maritima (Strigamia Genome Project, Human Genome Sequencing Consortium, Baylor College). We are confident that there is only a single copy present in the S. maritima genome (see Materials and methods). They show 50% and 62% identity with the insect ASH carboxy-terminal domain, respectively, and 78% identity with the carboxy-terminal domain of CsASH1. They lack the Ase-specific motif and would appear to be ASH genes.


An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian.

Ayyar S, Negre B, Simpson P, Stollewerk A - BMC Biol. (2010)

Conserved domains of the arthropod ASH and Ase proteins. Alignment of the bHLH domain, Ase motif and carboxy-terminal motif of ASH and Ase. Am, Apis mellifera; Cs, Cupiennius salei; Dm, Drosophila melanogasster; Dp, Daphnia pulex; Gm, Glomeris marginata; Sm, Strigamia maritima; Tc, Tribolium castaneum.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2958161&req=5

Figure 1: Conserved domains of the arthropod ASH and Ase proteins. Alignment of the bHLH domain, Ase motif and carboxy-terminal motif of ASH and Ase. Am, Apis mellifera; Cs, Cupiennius salei; Dm, Drosophila melanogasster; Dp, Daphnia pulex; Gm, Glomeris marginata; Sm, Strigamia maritima; Tc, Tribolium castaneum.
Mentions: In order to classify proneural and precursor-specific genes in other arthropod groups, we applied the above criteria to recently published sequences. Two ASH genes were described in the crustacean Triops longicaudatus [24]. The authors show that the deduced amino acid sequence of Tl-ASH1 bears the ASH carboxy-terminal domain, while this sequence is not conserved in Tl-ASH2. We identified the Ase motif in Tl-ASH2, confirming that this gene is in fact an asense orthologue (Figure 1). Furthermore, we detected single ASH and ase orthologues, Dpu-ASH and Dpu-ase, in the Daphnia pulex genome (Daphnia Genome Consortium), which can clearly be distinguished by the presence of the respective domains (Figure 1). The spider Cupiennius salei (chelicerate) displays two ASH orthologues [23] but sequence analysis does not unambiguously distinguish a bona fide ase gene in this species. The carboxy-terminal domain of CsASH1 displays a greater similarity to that of insect and crustacean ASH proteins (56% amino acid identity) than does that of CsASH2 (30%). However, neither CsASH1 nor CsASH2 contain the five amino acid motif characteristic of Ase (Figure 1). A single orthologue has been identified in each of the myriapods Glomeris marginata [26] and Strigamia maritima (Strigamia Genome Project, Human Genome Sequencing Consortium, Baylor College). We are confident that there is only a single copy present in the S. maritima genome (see Materials and methods). They show 50% and 62% identity with the insect ASH carboxy-terminal domain, respectively, and 78% identity with the carboxy-terminal domain of CsASH1. They lack the Ase-specific motif and would appear to be ASH genes.

Bottom Line: The SOPEs of the spider Cupiennius salei and the insect Tribolium castaneum are shown to be functional in transgenic Drosophila.This would place the origin of this regulatory sequence as far back as the last common ancestor of the Arthropoda, that is, in the Cambrian, 550 million years ago.The SOPE is not detectable by inter-specific sequence comparison, raising the possibility that other ancient regulatory modules in invertebrates might have escaped detection.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.

ABSTRACT

Background: An increasing number of publications demonstrate conservation of function of cis-regulatory elements without sequence similarity. In invertebrates such functional conservation has only been shown for closely related species. Here we demonstrate the existence of an ancient arthropod regulatory element that functions during the selection of neural precursors. The activity of genes of the achaete-scute (ac-sc) family endows cells with neural potential. An essential, conserved characteristic of proneural genes is their ability to restrict their own activity to single or a small number of progenitor cells from their initially broad domains of expression. This is achieved through a process called lateral inhibition. A regulatory element, the sensory organ precursor enhancer (SOPE), is required for this process. First identified in Drosophila, the SOPE contains discrete binding sites for four regulatory factors. The SOPE of the Drosophila asense gene is situated in the 5' UTR.

Results: Through a manual comparison of consensus binding site sequences we have been able to identify a SOPE in UTR sequences of asense-like genes in species belonging to all four arthropod groups (Crustacea, Myriapoda, Chelicerata and Insecta). The SOPEs of the spider Cupiennius salei and the insect Tribolium castaneum are shown to be functional in transgenic Drosophila. This would place the origin of this regulatory sequence as far back as the last common ancestor of the Arthropoda, that is, in the Cambrian, 550 million years ago.

Conclusions: The SOPE is not detectable by inter-specific sequence comparison, raising the possibility that other ancient regulatory modules in invertebrates might have escaped detection.

Show MeSH