Mitonuclear mismatch alters nuclear gene expression in naturally introgressed Rhinolophus bats

Yuting Ding,Wenli Chen,Stephen J Rossiter,Xiuguang Mao,Qianqian Li

doi:10.1186/s12983-021-00424-x

Abstract

BackgroundMitochondrial function involves the interplay between mitochondrial and nuclear genomes. Such mitonuclear interactions can be disrupted by the introgression of mitochondrial DNA between taxa or divergent populations. Previous studies of several model systems (e.g. Drosophila) indicate that the disruption of mitonuclear interactions, termed mitonuclear mismatch, can alter nuclear gene expression, yet few studies have focused on natural populations.ResultsHere we study a naturally introgressed population in the secondary contact zone of two subspecies of the intermediate horseshoe bat (Rhinolophus affinis), in which individuals possess either mitonuclear matched or mismatched genotypes. We generated transcriptome data for six tissue types from five mitonuclear matched and five mismatched individuals. Our results revealed strong tissue-specific effects of mitonuclear mismatch on nuclear gene expression with the largest effect seen in pectoral muscle. Moreover, consistent with the hypothesis that genes associated with the response to oxidative stress may be upregulated in mitonuclear mismatched individuals, we identified several such gene candidates, including DNASE1L3, GPx3 and HSPB6 in muscle, and ISG15 and IFI6 in heart.ConclusionOur study reveals how mitonuclear mismatch arising from introgression in natural populations is likely to have fitness consequences. Underlying the processes that maintain mitonuclear discordance is a step forward to understand the role of mitonuclear interactions in population divergence and speciation.

Highlights

Mitochondrial function involves the interplay between mitochondrial and nuclear genomes
Consistent with this, the ML tree based on sequences of concatenated 13 protein-coding genes (PCGs) and principal component analysis (PCA) based on SNPs from the whole mitogenome strongly supported the classification of five mismatched individuals with macrurus (Additional file 1: Figure S1b, Additional file 2: S2b)
The results of the PCA and sliding-window Fst analysis supported the overall similarity across the nuclear genome between these two groups (Additional file 2: Figure S2c and Additional file 2: Figure S2e) and our recent study based on a wider range of sampling indicated that no nuclear DNA introgression had occurred between the two subspecies following mitochondrial DNA (mtDNA) introgression [37]

Summary

Introduction

Mitochondrial function involves the interplay between mitochondrial and nuclear genomes. Few studies have directly investigated the impact of mitonuclear mismatch on fitness in natural populations (but see [10, 24]), largely because it is difficult to compare the fitness of individuals with different combinations of mitochondrial and nuclear genotypes. Only a few studies have used comparative transcriptomics to investigate the effects of mitonuclear interactions on gene expression, and most such studies focused on the model organism Drosophila [25,26,27] Most of these studies indicated that mtDNA variation could alter nuclear gene expression, when individuals with mismatched mitonuclear genomes are placed under stress (e.g. hypoxic conditions). As far as we know, few such studies have been performed in naturally introgressed populations [28, 29], which are critical to understand how individuals with mismatched mitonuclear genotypes have evolved to cope with mitochondrial dysfunction, such as reduced ATP production [30] and elevated oxidative damage [31, 32]

Methods

Results

Discussion

Conclusion