Global expression differences and tissue specific expression differences in rice evolution result in two contrasting types of differentially expressed genes.

Youko Horiuchi,Nori Kurata,Takako Mochizuki,Hironori Fujisawa,Hajime Ohyanagi,Yoshiaki Harushima,Masahiro Fujita

doi:10.1186/s12864-015-2319-1

Abstract

BackgroundSince the development of transcriptome analysis systems, many expression evolution studies characterized evolutionary forces acting on gene expression, without explicit discrimination between global expression differences and tissue specific expression differences. However, different types of gene expression alteration should have different effects on an organism, the evolutionary forces that act on them might be different, and different types of genes might show different types of differential expression between species. To confirm this, we studied differentially expressed (DE) genes among closely related groups that have extensive gene expression atlases, and clarified characteristics of different types of DE genes including the identification of regulating loci for differential expression using expression quantitative loci (eQTL) analysis data.ResultsWe detected differentially expressed (DE) genes between rice subspecies in five homologous tissues that were verified using japonica and indica transcriptome atlases in public databases. Using the transcriptome atlases, we classified DE genes into two types, global DE genes and changed-tissues DE genes. Global type DE genes were not expressed in any tissues in the atlas of one subspecies, however changed-tissues type DE genes were expressed in both subspecies with different tissue specificity. For the five tissues in the two japonica-indica combinations, 4.6 ± 0.8 and 5.9 ± 1.5 % of highly expressed genes were global and changed-tissues DE genes, respectively. Changed-tissues DE genes varied in number between tissues, increasing linearly with the abundance of tissue specifically expressed genes in the tissue. Molecular evolution of global DE genes was rapid, unlike that of changed-tissues DE genes. Based on gene ontology, global and changed-tissues DE genes were different, having no common GO terms. Expression differences of most global DE genes were regulated by cis-eQTLs. Expression evolution of changed-tissues DE genes was rapid in tissue specifically expressed genes and those rapidly evolved changed-tissues DE genes were regulated not by cis-eQTLs, but by complicated trans-eQTLs.ConclusionsGlobal DE genes and changed-tissues DE genes had contrasting characteristics. The two contrasting types of DE genes provide possible explanations for the previous controversial conclusions about the relationships between molecular evolution and expression evolution of genes in different species, and the relationship between expression breadth and expression conservation in evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2319-1) contains supplementary material, which is available to authorized users.

Highlights

Since the development of transcriptome analysis systems, many expression evolution studies characterized evolutionary forces acting on gene expression, without explicit discrimination between global expression differences and tissue specific expression differences
We study differentially expressed (DE) genes among closely related groups that have extensive gene expression atlases, and clarify the characteristics of different types of DE genes and identify the loci regulating the differential expression by using expression quantitative loci analysis data
We investigated the following characteristics of the two types of japonica-indica DE (jiDE) genes in comparison with japonica-indica similarly expressed (jiSE) genes: the number expressed in each homologous tissue; the level of tissue specificity; their molecular evolution; their chromosomal gene distribution; and the kinds of genes enriched in each group

Summary

Introduction

Since the development of transcriptome analysis systems, many expression evolution studies characterized evolutionary forces acting on gene expression, without explicit discrimination between global expression differences and tissue specific expression differences. Recent expression evolution studies have been performed with RNA sequencing (RNA-seq) using high-throughout generation sequencers (reviewed in [9, 10]) Most of these studies (both microarray and RNA-seq) have focused on characterization of the evolutionary forces on gene expression by comparison of expression level variation within species and among species, and evaluate the relative influences of neutral drift, stabilizing selection, directional selection, and balancing selection on gene expression evolution. Since different types of gene expression alteration would result in different effects on an organism, the evolutionary forces that act on them might be different, and different types of genes might show different types of differential expression between species. We study differentially expressed (DE) genes among closely related groups that have extensive gene expression atlases, and clarify the characteristics of different types of DE genes and identify the loci regulating the differential expression by using expression quantitative loci (eQTL) analysis data

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