Gene expression of functionally-related genes coevolves across fungal species: detecting coevolution of gene expression using phylogenetic comparative methods

Cope, Alexander L.; O’Meara, Brian C.; Gilchrist, Michael A.

doi:10.1186/s12864-020-6761-3

Title: Gene expression of functionally-related genes coevolves across fungal species: detecting coevolution of gene expression using phylogenetic comparative methods

Journal Article · Wed May 20 00:00:00 EDT 2020 · BMC Genomics

DOI:https://doi.org/10.1186/s12864-020-6761-3· OSTI ID:1815917

^[1]; O’Meara, Brian C. ^[2]; Gilchrist, Michael A. ^[3]

Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
Univ. of Tennessee, Knoxville, TN (United States). Dept. of Ecology and Evolutionary Biology; Univ. of Tennessee, Knoxville, TN (United States). Mathematical and Biological Synthesis
Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Ecology and Evolutionary Biology; Univ. of Tennessee, Knoxville, TN (United States). Mathematical and Biological Synthesis

Researchers often measure changes in gene expression across conditions to better understand the shared functional roles and regulatory mechanisms of different genes. Analogous to this is comparing gene expression across species, which can improve our understanding of the evolutionary processes shaping the evolution of both individual genes and functional pathways. One area of interest is determining genes showing signals of coevolution, which can also indicate potential functional similarity, analogous to co-expression analysis often performed across conditions for a single species. However, as with any trait, comparing gene expression across species can be confounded by the non-independence of species due to shared ancestry, making standard hypothesis testing inappropriate. We compared RNA-Seq data across 18 fungal species using a multivariate Brownian Motion phylogenetic comparative method (PCM), which allowed us to quantify coevolution between protein pairs while directly accounting for the shared ancestry of the species. Our work indicates proteins which physically-interact show stronger signals of coevolution than randomly-generated pairs. Interactions with stronger empirical and computational evidence also showing stronger signals of coevolution. We examined the effects of number of protein interactions and gene expression levels on coevolution, finding both factors are overall poor predictors of the strength of coevolution between a protein pair. Simulations further demonstrate the potential issues of analyzing gene expression coevolution without accounting for shared ancestry in a standard hypothesis testing framework. Furthermore, our simulations indicate the use of a randomly-generated null distribution as a means of determining statistical significance for detecting coevolving genes with phylogenetically-uncorrected correlations, as has previously been done, is less accurate than PCMs, although is a significant improvement over standard hypothesis testing. These methods are further improved by using a phylogenetically-corrected correlation metric. Our work highlights potential benefits of using PCMs to detect gene expression coevolution from high-throughput omics scale data. This framework can be built upon to investigate other evolutionary hypotheses, such as changes in transcription regulatory mechanisms across species.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1815917

Journal Information:: BMC Genomics, Vol. 21, Issue 1; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Additional file 1 of Gene expression of functionally-related genes coevolves across fungal species: detecting coevolution of gene expression using phylogenetic comparative methods Cope, Alexander L.; O’Meara, Brian C.; Gilchrist, Michael A. https://doi.org/10.6084/m9.figshare.12344681 The current record is supplemented by this text	text	January 2020
Gene expression of functionally-related genes coevolves across fungal species: detecting coevolution of gene expression using phylogenetic comparative methods Cope, Alexander L.; O’Meara, Brian C.; Gilchrist, Michael A. https://doi.org/10.6084/m9.figshare.c.4986869 The current record is supplemented by this collection	collection	January 2020
Additional file 1 of Gene expression of functionally-related genes coevolves across fungal species: detecting coevolution of gene expression using phylogenetic comparative methods Cope, Alexander L.; O’Meara, Brian C.; Gilchrist, Michael A. https://doi.org/10.6084/m9.figshare.12344681.v1 The current record is supplemented by this text	text	January 2020

Title: Gene expression of functionally-related genes coevolves across fungal species: detecting coevolution of gene expression using phylogenetic comparative methods

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