Evolution and Plasticity of the Transcriptome Under Temperature Fluctuations in the Fungal Plant Pathogen Zymoseptoria tritici.

Arthur J Jallet,Arnaud Le Rouzic,Anne Genissel

doi:10.3389/fmicb.2020.573829

Abstract

Most species live in a variable environment in nature. Yet understanding the evolutionary processes underlying molecular adaptation to fluctuations remains a challenge. In this study we investigate the transcriptome of the fungal wheat pathogen Zymoseptoria tritici after experimental evolution under stable or fluctuating temperature, by comparing ancestral and evolved populations simultaneously. We found that temperature regimes could have a large and pervasive effect on the transcriptome evolution, with as much as 38% of the genes being differentially expressed between selection regimes. Although evolved lineages showed different changes of gene expression based on ancestral genotypes, we identified a set of genes responding specifically to fluctuation. We found that transcriptome evolution in fluctuating conditions was repeatable between parallel lineages initiated from the same genotype for about 60% of the differentially expressed genes. Further, we detected several hotspots of significantly differentially expressed genes in the genome, in regions known to be enriched in repetitive elements, including accessory chromosomes. Our findings also evidenced gene expression evolution toward a gain of robustness (loss of phenotypic plasticity) associated with the fluctuating regime, suggesting robustness is adaptive in changing environment. This work provides valuable insight into the role of transcriptional rewiring for rapid adaptation to abiotic changes in filamentous plant pathogens.

Highlights

One remaining challenge in evolutionary genetics is to understand the role of regulatory variation in adaptation
The role of transposable elements in regulating gene expression evolution in Eukaryotes has been well documented. These results suggest that further investigations are needed to identify the causal factors –TE themselves, epigenetic regulation, or single nucleotide polymorphism (SNP)/indels– that are associated with the evolution of gene expression level
Our findings demonstrate substantial evolution of gene expression under fluctuating temperature with striking differences between genetic backgrounds

Summary

Introduction

One remaining challenge in evolutionary genetics is to understand the role of regulatory variation in adaptation. The number of genes showing significant differences between ancestral and evolved lineages with a fold-changed > 2 is considered (stable at 17◦C, stable at 23◦C and fluctuating between 17◦C and 23◦C). Significant change in expression compared to the ancestor was highly correlated in parallel lineages for each genetic background with a large proportion (nearly 60%) of common genes between the two independently evolved lines (568 out of 907 Differentially Expressed Genes (DEGs) for MGGP01, and 366 out of 638 DEGs for MGGP44 when considering genes with a fold change greater than two) (Figure 3). We focused our attention on this set of genes, assuming that parallel evolutionary change could be the consequence of adaptive evolution in fluctuating environments.

Methods

Results

Discussion

Conclusion