Genome-wide DNA mutations in Arabidopsis plants after multigenerational exposure to high temperatures

Zhaogeng Lu,Li Wang,Chenwu Xu,Yingfang Zhu,Siwei Xiao,Biao Jin,Shoudong Zhang,Wensi Ke,Nianjun Teng,Hon-Ming Lam,Jinxing Lin,Jiawen Cui

doi:10.1186/s13059-021-02381-4

Abstract

BackgroundElevated temperatures can cause physiological, biochemical, and molecular responses in plants that can greatly affect their growth and development. Mutations are the most fundamental force driving biological evolution. However, how long-term elevations in temperature influence the accumulation of mutations in plants remains unknown.ResultsMultigenerational exposure of Arabidopsis MA (mutation accumulation) lines and MA populations to extreme heat and moderate warming results in significantly increased mutation rates in single-nucleotide variants (SNVs) and small indels. We observe distinctive mutational spectra under extreme and moderately elevated temperatures, with significant increases in transition and transversion frequencies. Mutation occurs more frequently in intergenic regions, coding regions, and transposable elements in plants grown under elevated temperatures. At elevated temperatures, more mutations accumulate in genes associated with defense responses, DNA repair, and signaling. Notably, the distribution patterns of mutations among all progeny differ between MA populations and MA lines, suggesting that stronger selection effects occurred in populations. Methylation is observed more frequently at mutation sites, indicating its contribution to the mutation process at elevated temperatures. Mutations occurring within the same genome under elevated temperatures are significantly biased toward low gene density regions, special trinucleotides, tandem repeats, and adjacent simple repeats. Additionally, mutations found in all progeny overlap significantly with genetic variations reported in 1001 Genomes, suggesting non-uniform distribution of de novo mutations through the genome.ConclusionCollectively, our results suggest that elevated temperatures can accelerate the accumulation, and alter the molecular profiles, of DNA mutations in plants, thus providing significant insight into how environmental temperatures fuel plant evolution.

Highlights

Elevated temperatures can cause physiological, biochemical, and molecular responses in plants that can greatly affect their growth and development
We found significantly increased mutation rates, along with distinct mutation spectra, mutated genes, and mutation bias, under elevated temperature conditions, providing insights into plant molecular evolution under environmental warming
mutation accumulation (MA) experiments and whole-genome sequencing We conducted long-term MA experiments on A. thaliana in both single-seed descent lineages and populations grown under Control, Heat, and Warming conditions (Fig. 1a, b)

Summary

Introduction

Elevated temperatures can cause physiological, biochemical, and molecular responses in plants that can greatly affect their growth and development. Given the effectiveness of this experimental system, MA experiments combined with whole-genome sequencing technology have been extensively conducted to investigate spontaneous mutation rates and spectra in multiple eukaryotic species, including Chlamydomonas reinhardtii [14, 15], Drosophila melanogaster [16,17,18], Caenorhabditis elegans [19, 20], Escherichia coli [1, 21], Saccharomyces cerevisiae [22], and Arabidopsis thaliana [23] These MA studies have provided important reference data for estimating overall spontaneous mutation rates and the patterns underlying the molecular evolution of various species

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