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Recombinational micro-evolution of functionally different metallothionein promoter alleles from Orchesella cincta.

ABSTRACT: BACKGROUND:Metallothionein (mt) transcription is elevated in heavy metal tolerant field populations of Orchesella cincta (Collembola). This suggests that natural selection acts on transcriptional regulation of mt in springtails at sites where cadmium (Cd) levels in soil reach toxic values This study investigates the nature and the evolutionary origin of polymorphisms in the metallothionein promoter (pmt) and their functional significance for mt expression. RESULTS:We sequenced approximately 1600 bp upstream the mt coding region by genome walking. Nine pmt alleles were discovered in NW-European populations. They differ in the number of some indels, consensus transcription factor binding sites and core promoter elements. Extensive recombination events between some of the alleles can be inferred from the alignment. A deviation from neutral expectations was detected in a cadmium tolerant population, pointing towards balancing selection on some promoter stretches. Luciferase constructs were made from the most abundant alleles, and responses to Cd, paraquat (oxidative stress inducer) and moulting hormone were studied in cell lines. By using paraquat we were able to dissect the effect of oxidative stress from the Cd specific effect, and extensive differences in mt induction levels between these two stressors were observed. CONCLUSION:The pmt alleles evolved by a number of recombination events, and exhibited differential inducibilities by Cd, paraquat and molting hormone. In a tolerant population from a metal contaminated site, promoter allele frequencies differed significantly from a reference site and nucleotide polymorphisms in some promoter stretches deviated from neutral expectations, revealing a signature of balancing selection. Our results suggest that the structural differences in the Orchesella cincta metallothionein promoter alleles contribute to the metallothionein -over-expresser phenotype in cadmium tolerant populations.

SUBMITTER: Janssens TK

PROVIDER: S-EPMC1913499 | biostudies-literature | 2007 Jun

REPOSITORIES: biostudies-literature

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Recombinational micro-evolution of functionally different metallothionein promoter alleles from Orchesella cincta.

Janssens Thierry K S TK Mariën Janine J Cenijn Peter P Legler J J van Straalen Nico M NM Roelofs Dick D

BMC evolutionary biology 20070611

<h4>Background</h4>Metallothionein (mt) transcription is elevated in heavy metal tolerant field populations of Orchesella cincta (Collembola). This suggests that natural selection acts on transcriptional regulation of mt in springtails at sites where cadmium (Cd) levels in soil reach toxic values This study investigates the nature and the evolutionary origin of polymorphisms in the metallothionein promoter (pmt) and their functional significance for mt expression.<h4>Results</h4>We sequenced app ...[more]

PMID: 17562010

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Project description:BackgroundIn Drosophila and many other insects, the Hox genes Ultrabithorax (Ubx) and abdominal-A (abd-A) suppress limb formation on most or all segments of the abdomen. However, a number of basal hexapod lineages retain multiple appendages on the abdomen. In the collembolans or springtails, three abdominal segments develop specialized organs that originate from paired appendage primordia which fuse at the midline: the first abdominal segment bears the collophore (ventral tube), involved in osmoregulation; the fourth segment bears the furca, the leaping organ, and the third segment bears the retinaculum, which retains the furca at rest. Ubx and abd-A are known to be expressed in the springtail abdomen, but what role they play in specifying these distinct abdominal appendages is not known. This is largely because no genetic model has been established in collembolans or any other non-insect hexapod.ResultsWe have developed a convenient method for laboratory culture of the collembolan Orchesella cincta on defined media, a method for in-situ hybridization to embryos and a procedure for gene knockdown by parental injection of double-stranded RNA (RNAi). We show that Orchesella Ubx transcripts are detectable in the first to third abdominal segments, and abd-A transcripts in the second to fourth segments. Knockdown of Oc-Ubx leads to the homeotic transformation of the collophore into a pair of walking legs (a more anterior identity) but the retinaculum into a furca (a more posterior identity). Knockdown of Oc-abd-A leads to the transformation of the retinaculum into a collophore and of the furca into legs (both anterior transformations). Simultaneous silencing of both Oc-Ubx and Oc-abd-A transformed all three of these appendages into paired legs, but did not cause appendages to develop on the second, or on the most posterior abdominal segments.ConclusionsWe conclude that, in Orchesella, Oc-Ubx alone specifies the collophore on the first and Oc-abd-A alone specifies the furca on the fourth abdominal segment. Oc-Ubx and Oc-abd-A function together, apparently combinatorially, to specify the retinaculum on the third segment. The efficiency of RNAi in Orchesella makes this an attractive model for further genetic studies of development and physiology in basal hexapods.

Project description:Although human bitter taste perception is hypothesized to be a dietary adaptation, little is known about genetic signatures of selection and patterns of bitter taste perception variability in ethnically diverse populations with different diets, particularly from Africa. To better understand the genetic basis and evolutionary history of bitter taste sensitivity, we sequenced a 2,975 bp region encompassing TAS2R38, a bitter taste receptor gene, in 611 Africans from 57 populations in West Central and East Africa with diverse subsistence patterns, as well as in a comparative sample of 132 non-Africans. We also examined the association between genetic variability at this locus and threshold levels of phenylthiocarbamide (PTC) bitterness in 463 Africans from the above populations to determine how variation influences bitter taste perception. Here, we report striking patterns of variation at TAS2R38, including a significant excess of novel rare nonsynonymous polymorphisms that recently arose only in Africa, high frequencies of haplotypes in Africa associated with intermediate bitter taste sensitivity, a remarkably similar frequency of common haplotypes across genetically and culturally distinct Africans, and an ancient coalescence time of common variation in global populations. Additionally, several of the rare nonsynonymous substitutions significantly modified levels of PTC bitter taste sensitivity in diverse Africans. While ancient balancing selection likely maintained common haplotype variation across global populations, we suggest that recent selection pressures may have also resulted in the unusually high level of rare nonsynonymous variants in Africa, implying a complex model of selection at the TAS2R38 locus in African populations. Furthermore, the distribution of common haplotypes in Africa is not correlated with diet, raising the possibility that common variation may be under selection due to their role in nondietary biological processes. In addition, our data indicate that novel rare mutations contribute to the phenotypic variance of PTC sensitivity, illustrating the influence of rare variation on a common trait, as well as the relatively recent evolution of functionally diverse alleles at this locus.

Dataset Information

Recombinational micro-evolution of functionally different metallothionein promoter alleles from Orchesella cincta.

Publications

Recombinational micro-evolution of functionally different metallothionein promoter alleles from Orchesella cincta.

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