Evaluation of the Role of Functional Constraints on the Integrity of an Ultraconserved Region in the Genus Drosophila
ABSTRACT Why gene order is conserved over long evolutionary timespans remains elusive. A common interpretation is that gene order conservation might reflect the existence of functional constraints that are important for organismal performance. Alteration of the integrity of genomic regions, and therefore of those constraints, would result in detrimental effects. This notion seems especially plausible in those genomes that can easily accommodate gene reshuffling via chromosomal inversions since genomic regions free of constraints are likely to have been disrupted in one or more lineages. Nevertheless, no empirical test has been performed to this notion. Here, we disrupt one of the largest conserved genomic regions of the Drosophila genome by chromosome engineering and examine the phenotypic consequences derived from such disruption. The targeted region exhibits multiple patterns of functional enrichment suggestive of the presence of constraints. The carriers of the disrupted collinear block show no defects in their viability, fertility, and parameters of general homeostasis, although their odorant perception is altered. This change in odorant perception does not correlate with modifications of the level of expression and sex bias of the genes within the genomic region disrupted. Our results indicate that even in highly rearranged genomes, like those of Diptera, unusually high levels of gene order conservation cannot be systematically attributed to functional constraints, which raises the possibility that other mechanisms can be in place and therefore the underpinnings of the maintenance of gene organization might be more diverse than previously thought.
SourceAvailable from: Tatyana D Kolesnikova[Show abstract] [Hide abstract]
ABSTRACT: Drosophila chromosomes are organized into distinct domains differing in their predominant chromatin composition, replication timing and evolutionary conservation. We show on a genome-wide level that genes whose order has remained unaltered across 9 Drosophila species display late replication timing and frequently map to the regions of repressive chromatin. This observation is consistent with the existence of extensive domains of repressive chromatin that replicate extremely late and have conserved gene order in the Drosophila genome. We suggest that such repressive chromatin domains correspond to a handful of regions that complete replication at the very end of S phase. We further demonstrate that the order of genes in these regions is rarely altered in evolution. Substantial proportion of such regions significantly coincide with large synteny blocks. This indicates that there are evolutionary mechanisms maintaining the integrity of these late-replicating chromatin domains. The synteny blocks corresponding to the extremely late-replicating regions in the D. melanogaster genome consistently display two-fold lower gene density across different Drosophila species.PLoS ONE 12/2013; 8(12):e83319. DOI:10.1371/journal.pone.0083319 · 3.53 Impact Factor
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ABSTRACT: Many late replicating regions are under-replicated in polytene chromosomes of Drosophila melanogaster. These regions contain silenced chromatin and overlap long syntenic blocks of conserved gene order in drosophilids. In this report we show that in D. melanogaster the under-replicated regions are enriched with fast evolving genes lacking homologs in distant species such as mosquito or human, indicating that the phylogenetic conservation of genes correlates with replication timing and chromatin status. Drosophila genes without human homologs located in the under-replicated regions have higher non-synonymous substitution rate and tend to encode shorter proteins when compared to those in the adjacent regions. At the same time, the under-replicated regions are enriched with ultra-conserved elements and highly conserved noncoding sequences, especially in introns of very long genes indicating the presence of an extensive regulatory network that may be responsible for the conservation of gene order in these regions. The regions have a modest preference for long noncoding RNAs but are depleted for snoRNAs, miRNAs and tRNAs. Our results demonstrate that the under-replicated regions have a specific genic composition and distinct pattern of evolution.Genome Biology and Evolution 07/2014; 6(8). DOI:10.1093/gbe/evu156 · 4.53 Impact Factor
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ABSTRACT: Many biological processes depend on very few copies of intervening elements, which makes such processes particularly susceptible to the stochastic fluctuations of these elements. The intrinsic stochasticity of certain processes is propagated across bio-logical levels, causing genotype-and environment-independent biological variation which might permit populations to better cope with variable environments. Biolog-ical variations of stochastic nature might also allow the accumulation of variations at the genetic level that are hidden from natural selection, which might have a great potential for population diversification. The study of any mechanism that resulted in the modulation of stochastic variation is, therefore, of potentially wide interest. I propose that sex might be an important modulator of the stochastic variation in gene expression, i.e., gene expression noise. Based on known associations between diVerent patterns of gene expression variation, I hypothesize that in metazoans the gene expression noise might be generally larger in heterogametic than in homoga-metic individuals. I directly tested this hypothesis by comparing putative genotype-and environment-independent variations in gene expression between females and males of Drosophila melanogaster strains. Also, considering the potential eVect of the propagation of gene expression noise across biological levels, I indirectly tested the existence of a metazoan sexual dimorphism in gene expression noise by analyzing putative genotype-and environment-independent variation in phenotypes related to interaction with the environment in D. melanogaster strains and metazoan species. The results of these analyses are consistent with the hypothesis that gene expression is generally noisier in heterogametic than in homogametic individuals. Further analyses and discussion of existing literature permits the speculation that the sexual dimorphism in gene expression noise is ultimately based on the nuclear dynamics in gametogenesis and very early embryogenesis of sex-specific chromosomes, i.e., Y and W chromosomes.