Dataset Information

Complex chromosomal neighborhood effects determine the adaptive potential of a gene under selection.

ABSTRACT: How the organization of genes on a chromosome shapes adaptation is essential for understanding evolutionary paths. Here, we investigate how adaptation to rapidly increasing levels of antibiotic depends on the chromosomal neighborhood of a drug-resistance gene inserted at different positions of the Escherichia coli chromosome. Using a dual-fluorescence reporter that allows us to distinguish gene amplifications from other up-mutations, we track in real-time adaptive changes in expression of the drug-resistance gene. We find that the relative contribution of several mutation types differs systematically between loci due to properties of neighboring genes: essentiality, expression, orientation, termination, and presence of duplicates. These properties determine rate and fitness effects of gene amplification, deletions, and mutations compromising transcriptional termination. Thus, the adaptive potential of a gene under selection is a system-property with a complex genetic basis that is specific for each chromosomal locus, and it can be inferred from detailed functional and genomic data.

SUBMITTER: Steinrueck M

PROVIDER: S-EPMC5526668 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Complex chromosomal neighborhood effects determine the adaptive potential of a gene under selection.

Steinrueck Magdalena M Guet Călin C CC

eLife 20170725

How the organization of genes on a chromosome shapes adaptation is essential for understanding evolutionary paths. Here, we investigate how adaptation to rapidly increasing levels of antibiotic depends on the chromosomal neighborhood of a drug-resistance gene inserted at different positions of the <i>Escherichia coli</i> chromosome. Using a dual-fluorescence reporter that allows us to distinguish gene amplifications from other up-mutations, we track in real-time adaptive changes in expression of ...[more]

PMID: 28738969

Similar Datasets

Project description:Recently diverged species typically have incomplete reproductive barriers, allowing introgression of genetic material from one species into the genomic background of the other. The role of natural selection in preventing or promoting introgression remains contentious. Because of genomic co-adaptation, some chromosomal fragments are expected to be selected against in the new background and resist introgression. In contrast, natural selection should favor introgression for alleles at genes evolving under multi-allelic balancing selection, such as the MHC in vertebrates, disease resistance, or self-incompatibility genes in plants. Here, we test the prediction that negative, frequency-dependent selection on alleles at the multi-allelic gene controlling pistil self-incompatibility specificity in two closely related species, Arabidopsis halleri and A. lyrata, caused introgression at this locus at a higher rate than the genomic background. Polymorphism at this gene is largely shared, and we have identified 18 pairs of S-alleles that are only slightly divergent between the two species. For these pairs of S-alleles, divergence at four-fold degenerate sites (K = 0.0193) is about four times lower than the genomic background (K = 0.0743). We demonstrate that this difference cannot be explained by differences in effective population size between the two types of loci. Rather, our data are most consistent with a five-fold increase of introgression rates for S-alleles as compared to the genomic background, making this study the first documented example of adaptive introgression facilitated by balancing selection. We suggest that this process plays an important role in the maintenance of high allelic diversity and divergence at the S-locus in flowering plant families. Because genes under balancing selection are expected to be among the last to stop introgressing, their comparison in closely related species provides a lower-bound estimate of the time since the species stopped forming fertile hybrids, thereby complementing the average portrait of divergence between species provided by genomic data.

Project description:BACKGROUND: Molecular lock-and-key systems are common among reproductive proteins, yet their evolution remains a major puzzle in evolutionary biology. In the Brassicaceae, the genes encoding self-incompatibility have been identified, but technical challenges currently prevent detailed analyses of the molecular interaction between the male and female components. In the present study, we investigate sequence polymorphism in the female specificity determinant SRK of Arabidopsis halleri from throughout Europe. Using a comparative approach based on published SRK sequences in A. lyrata and Brassica, we track the signature of frequency-dependent selection acting on these genes at the codon level. Using simulations, we evaluate power and accuracy of our approach and estimate the proportion of codon sites involved in the molecular interaction. RESULTS: We identified several members of the S-gene family, together with 22 putative S-haplotypes. Linkage to the S-locus and the presence of a kinase domain were formally demonstrated for four and six of these haplotypes, respectively, and sequence polymorphism was extremely high. Twenty-five codons showed signs of positive selection in at least one species, and clustered significantly (but not exclusively) within hypervariable regions. We checked that this clustering was not an artifact due to variation in evolution rate at synonymous sites. Simulations revealed that the analysis was highly accurate, thus providing a reliable set of candidates for future functional analyses, but with an overall power not higher than 60 %. Assuming similar power, we infer from our results that about 23% of all codons in the S-domain may actually be involved in recognition. Interestingly, while simulations demonstrated that this comparison remained reliable even at very high levels of divergence, codons identified in Brassica had higher posterior rates of non-synonymous to synonymous substitutions than codons identified in A. halleri or A. lyrata, possibly suggesting more intense selection in Brassica. CONCLUSION: The signature of balancing selection can be identified reliably at the codon level even in cases of very high sequence divergence, provided that a sufficiently large set of sequences are analyzed. Altogether, our results indicate that a large proportion of codons may be involved in recognition and confirm the particular importance of hypervariable regions. The more intense signature of positive selection detected in Brassica suggests that allelic diversification in this genus was very recent, possibly following a recent demographic bottleneck.

Dataset Information

Complex chromosomal neighborhood effects determine the adaptive potential of a gene under selection.

Publications

Complex chromosomal neighborhood effects determine the adaptive potential of a gene under selection.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure