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Gene Repositioning Is Under Constraints After Evolutionary Conserved Gene Neighborhood Separate.

ABSTRACT: Genes are not randomly distributed on eukaryotic chromosomes. Some neighboring genes show order conservation among species, while some neighboring genes separate during evolution even though their neighborhoods are conserved in some species. Here, I investigated whether after-separation gene repositioning is under natural selection for evolutionary conserved gene neighborhoods compared with nonconserved neighborhoods. After separation, genes with conserved neighborhoods show low-expression divergence between the after-separation species and the before-separation species. After genes separate from their conserved gene neighbors, their after-separation gene neighbors tend to show coexpression and coprotein complex with their before-separation gene neighbors. These results indicate evolutionary constraints on the selection of neighboring genes after evolutionary conserved gene neighborhoods separate.

SUBMITTER: Dai Z

PROVIDER: S-EPMC6785632 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Gene Repositioning Is Under Constraints After Evolutionary Conserved Gene Neighborhood Separate.

Dai Zhiming Z

Frontiers in genetics 20191003

Genes are not randomly distributed on eukaryotic chromosomes. Some neighboring genes show order conservation among species, while some neighboring genes separate during evolution even though their neighborhoods are conserved in some species. Here, I investigated whether after-separation gene repositioning is under natural selection for evolutionary conserved gene neighborhoods compared with nonconserved neighborhoods. After separation, genes with conserved neighborhoods show low-expression diver ...[more]

PMID: 31632448

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Project description:BACKGROUND: The structure of regulatory networks remains an open question in our understanding of complex biological systems. Interactions during complete viral life cycles present unique opportunities to understand how host-parasite network take shape and behave. The Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV) is a large double-stranded DNA virus, whose genome may encode for 152 open reading frames (ORFs). Here we present the analysis of the ordered cascade of the AgMNPV gene expression. RESULTS: We observed an earlier onset of the expression than previously reported for other baculoviruses, especially for genes involved in DNA replication. Most ORFs were expressed at higher levels in a more permissive host cell line. Genes with more than one copy in the genome had distinct expression profiles, which could indicate the acquisition of new functionalities. The transcription gene regulatory network (GRN) for 149 ORFs had a modular topology comprising five communities of highly interconnected nodes that separated key genes that are functionally related on different communities, possibly maximizing redundancy and GRN robustness by compartmentalization of important functions. Core conserved functions showed expression synchronicity, distinct GRN features and significantly less genetic diversity, consistent with evolutionary constraints imposed in key elements of biological systems. This reduced genetic diversity also had a positive correlation with the importance of the gene in our estimated GRN, supporting a relationship between phylogenetic data of baculovirus genes and network features inferred from expression data. We also observed that gene arrangement in overlapping transcripts was conserved among related baculoviruses, suggesting a principle of genome organization. CONCLUSIONS: Albeit with a reduced number of nodes (149), the AgMNPV GRN had a topology and key characteristics similar to those observed in complex cellular organisms, which indicates that modularity may be a general feature of biological gene regulatory networks.

Project description:BackgroundHeterochromatin has been reported to be a major silencing compartment during development and differentiation. Prominent heterochromatin compartments are located at the nuclear periphery and inside the nucleus (e.g., pericentric heterochromatin). Whether the position of a gene in relation to some or all heterochromatin compartments matters remains a matter of debate, which we have addressed in this study. Answering this question demanded solving the technical challenges of 3D measurements and the large-scale morphological changes accompanying cellular differentiation.ResultsHere, we investigated the proximity effects of the nuclear periphery and pericentric heterochromatin on gene expression and additionally considered the effect of neighboring genomic features on a gene's nuclear position. Using a well-established myogenic in vitro differentiation system and a differentiation-independent heterochromatin remodeling system dependent on ectopic MeCP2 expression, we first identified genes with statistically significant expression changes by transcriptional profiling. We identified nuclear gene positions by 3D fluorescence in situ hybridization followed by 3D distance measurements toward constitutive and facultative heterochromatin domains. Single-cell-based normalization enabled us to acquire morphologically unbiased data and we finally correlated changes in gene positioning to changes in transcriptional profiles. We found no significant correlation of gene silencing and proximity to constitutive heterochromatin and a rather unexpected inverse correlation of gene activity and position relative to facultative heterochromatin at the nuclear periphery.ConclusionIn summary, our data question the hypothesis of heterochromatin as a general silencing compartment. Nonetheless, compared to a simulated random distribution, we found that genes are not randomly located within the nucleus. An analysis of neighboring genomic context revealed that gene location within the nucleus is rather dependent on CpG islands, GC content, gene density, and short and long interspersed nuclear elements, collectively known as RIDGE (regions of increased gene expression) properties. Although genes do not move away/to the heterochromatin upon up-/down-regulation, genomic regions with RIDGE properties are generally excluded from peripheral heterochromatin. Hence, we suggest that individual gene activity does not influence gene positioning, but rather chromosomal context matters for sub-nuclear location.

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Gene Repositioning Is Under Constraints After Evolutionary Conserved Gene Neighborhood Separate.

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Gene Repositioning Is Under Constraints After Evolutionary Conserved Gene Neighborhood Separate.

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