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Connectivity in gene coexpression networks negatively correlates with rates of molecular evolution in flowering plants.

ABSTRACT: Gene coexpression networks are a useful tool for summarizing transcriptomic data and providing insight into patterns of gene regulation in a variety of species. Though there has been considerable interest in studying the evolution of network topology across species, less attention has been paid to the relationship between network position and patterns of molecular evolution. Here, we generated coexpression networks from publicly available expression data for seven flowering plant taxa (Arabidopsis thaliana, Glycine max, Oryza sativa, Populus spp., Solanum lycopersicum, Vitis spp., and Zea mays) to investigate the relationship between network position and rates of molecular evolution. We found a significant negative correlation between network connectivity and rates of molecular evolution, with more highly connected (i.e., "hub") genes having significantly lower nonsynonymous substitution rates and dN/dS ratios compared to less highly connected (i.e., "peripheral") genes across the taxa surveyed. These findings suggest that more centrally located hub genes are, on average, subject to higher levels of evolutionary constraint than are genes located on the periphery of gene coexpression networks. The consistency of this result across disparate taxa suggests that it holds for flowering plants in general, as opposed to being a species-specific phenomenon.

SUBMITTER: Masalia RR

PROVIDER: S-EPMC5536297 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Connectivity in gene coexpression networks negatively correlates with rates of molecular evolution in flowering plants.

Masalia Rishi R RR Bewick Adam J AJ Burke John M JM

PloS one 20170731 7

Gene coexpression networks are a useful tool for summarizing transcriptomic data and providing insight into patterns of gene regulation in a variety of species. Though there has been considerable interest in studying the evolution of network topology across species, less attention has been paid to the relationship between network position and patterns of molecular evolution. Here, we generated coexpression networks from publicly available expression data for seven flowering plant taxa (Arabidops ...[more]

PMID: 28759647

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Project description:BackgroundTheoretical models and experimental evidence suggest that rates of molecular evolution could be raised in parasitic organisms compared to non-parasitic taxa. Parasitic plants provide an ideal test for these predictions, as there are at least a dozen independent origins of the parasitic lifestyle in angiosperms. Studies of a number of parasitic plant lineages have suggested faster rates of molecular evolution, but the results of some studies have been mixed. Comparative analysis of all parasitic plant lineages, including sequences from all three genomes, is needed to examine the generality of the relationship between rates of molecular evolution and parasitism in plants.ResultsWe analysed DNA sequence data from the mitochondrial, nuclear and chloroplast genomes for 12 independent evolutionary origins of parasitism in angiosperms. We demonstrated that parasitic lineages have a faster rate of molecular evolution than their non-parasitic relatives in sequences for all three genomes, for both synonymous and nonsynonymous substitutions.ConclusionsOur results prove that raised rates of molecular evolution are a general feature of parasitic plants, not confined to a few taxa or specific genes. We discuss possible causes for this relationship, including increased positive selection associated with host-parasite arms races, relaxed selection, reduced population size or repeated bottlenecks, increased mutation rates, and indirect causal links with generation time and body size. We find no evidence that faster rates are due to smaller effective populations sizes or changes in selection pressure. Instead, our results suggest that parasitic plants have a higher mutation rate than their close non-parasitic relatives. This may be due to a direct connection, where some aspect of the parasitic lifestyle drives the evolution of raised mutation rates. Alternatively, this pattern may be driven by an indirect connection between rates and parasitism: for example, parasitic plants tend to be smaller than their non-parasitic relatives, which may result in more cell generations per year, thus a higher rate of mutations arising from DNA copy errors per unit time. Demonstration that adoption of a parasitic lifestyle influences the rate of genomic evolution is relevant to attempts to infer molecular phylogenies of parasitic plants and to estimate their evolutionary divergence times using sequence data.

Dataset Information

Connectivity in gene coexpression networks negatively correlates with rates of molecular evolution in flowering plants.

Publications

Connectivity in gene coexpression networks negatively correlates with rates of molecular evolution in flowering plants.

Similar Datasets

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