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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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C. salei CsASH2 and T. castaneum ase can both rescue the bristle phenotype in D. melanogaster ase1 mutants. (A) Bar chart showing the extent to which Dm-ase, Tc-ase and CsASH2 can rescue the phenotype when ectopically expressed (hsp70Gal4 > UAS Dm-sc/Dm-ase/Tc-ase/CsASH2). In contrast, Dm-sc enhances the ase1 phenotype (hsp70Gal4 > UAS Dm-sc). The number of bristles affected is given on the x-axis. Error bars indicate the standard error of the mean (see Additional file 1 for details). (B-G) Abnormally differentiated bristles (asterisks) on the anterior wing margin are shown for the genotypes indicated (genotypes as in (A)). The number of abnormal bristles is enhanced in (D) and reduced in (F, E, G). (H-K) Detail of the abnormalities at higher magnification.
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Figure 3: C. salei CsASH2 and T. castaneum ase can both rescue the bristle phenotype in D. melanogaster ase1 mutants. (A) Bar chart showing the extent to which Dm-ase, Tc-ase and CsASH2 can rescue the phenotype when ectopically expressed (hsp70Gal4 > UAS Dm-sc/Dm-ase/Tc-ase/CsASH2). In contrast, Dm-sc enhances the ase1 phenotype (hsp70Gal4 > UAS Dm-sc). The number of bristles affected is given on the x-axis. Error bars indicate the standard error of the mean (see Additional file 1 for details). (B-G) Abnormally differentiated bristles (asterisks) on the anterior wing margin are shown for the genotypes indicated (genotypes as in (A)). The number of abnormal bristles is enhanced in (D) and reduced in (F, E, G). (H-K) Detail of the abnormalities at higher magnification.

Mentions: Flies lacking ase function exhibit only a mild phenotype because activity of ac, sc and senseless compensates for most of the defects [11,13,29,30]. However, one defect is specific to ase: differentiation of the stout mechanosensory bristles of the triple row of bristles on the anterior wing margin is impaired [11,13]. In ase1 mutant flies these bristles show variable defects that include a split shaft, two to three shafts arising from a single socket, an empty socket or a complete duplication (Figure 3H-K). When over-expressed, Dm-ase, but neither Dm-ac nor Dm-sc, has been shown to rescue these defects [11,13]. We found that CsASH2, as well as Tc-ase, display a rescuing activity comparable to that of Dm-ase (Figure 3A-G). The number of defective bristles in ase1 flies is reduced from an average of 9.7 to 2.5, 4.9 and 3.9 in flies expressing Dm-ase, Tc-ase and CsASH2, respectively (Figure 3A-G; Additional file 1). CsASH2 can therefore substitute for functions specific to Dm-ase, which suggests that it might carry out precursor-specific ase-like functions in the spider.


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)

C. salei CsASH2 and T. castaneum ase can both rescue the bristle phenotype in D. melanogaster ase1 mutants. (A) Bar chart showing the extent to which Dm-ase, Tc-ase and CsASH2 can rescue the phenotype when ectopically expressed (hsp70Gal4 > UAS Dm-sc/Dm-ase/Tc-ase/CsASH2). In contrast, Dm-sc enhances the ase1 phenotype (hsp70Gal4 > UAS Dm-sc). The number of bristles affected is given on the x-axis. Error bars indicate the standard error of the mean (see Additional file 1 for details). (B-G) Abnormally differentiated bristles (asterisks) on the anterior wing margin are shown for the genotypes indicated (genotypes as in (A)). The number of abnormal bristles is enhanced in (D) and reduced in (F, E, G). (H-K) Detail of the abnormalities at higher magnification.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: C. salei CsASH2 and T. castaneum ase can both rescue the bristle phenotype in D. melanogaster ase1 mutants. (A) Bar chart showing the extent to which Dm-ase, Tc-ase and CsASH2 can rescue the phenotype when ectopically expressed (hsp70Gal4 > UAS Dm-sc/Dm-ase/Tc-ase/CsASH2). In contrast, Dm-sc enhances the ase1 phenotype (hsp70Gal4 > UAS Dm-sc). The number of bristles affected is given on the x-axis. Error bars indicate the standard error of the mean (see Additional file 1 for details). (B-G) Abnormally differentiated bristles (asterisks) on the anterior wing margin are shown for the genotypes indicated (genotypes as in (A)). The number of abnormal bristles is enhanced in (D) and reduced in (F, E, G). (H-K) Detail of the abnormalities at higher magnification.
Mentions: Flies lacking ase function exhibit only a mild phenotype because activity of ac, sc and senseless compensates for most of the defects [11,13,29,30]. However, one defect is specific to ase: differentiation of the stout mechanosensory bristles of the triple row of bristles on the anterior wing margin is impaired [11,13]. In ase1 mutant flies these bristles show variable defects that include a split shaft, two to three shafts arising from a single socket, an empty socket or a complete duplication (Figure 3H-K). When over-expressed, Dm-ase, but neither Dm-ac nor Dm-sc, has been shown to rescue these defects [11,13]. We found that CsASH2, as well as Tc-ase, display a rescuing activity comparable to that of Dm-ase (Figure 3A-G). The number of defective bristles in ase1 flies is reduced from an average of 9.7 to 2.5, 4.9 and 3.9 in flies expressing Dm-ase, Tc-ase and CsASH2, respectively (Figure 3A-G; Additional file 1). CsASH2 can therefore substitute for functions specific to Dm-ase, which suggests that it might carry out precursor-specific ase-like functions in the spider.

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
Related in: MedlinePlus