Stress-driven transposable element de-repression dynamics in a fungal pathogen

Abstract

Transposable elements (TEs) are drivers of genome evolution and affect the expression landscape of the host genome. Stress is a major factor inducing TE activity, however the regulatory mechanisms underlying de-repression are poorly understood. Key unresolved questions are whether different types of stress differentially induce TE activity and whether different TEs respond differently to the same stress. Plant pathogens are excellent models to dissect the impact of stress on TEs, because lifestyle transitions on and off the host impose exposure to a variety of stress conditions. We analyzed the TE expression landscape of four well-characterized strains of the major wheat pathogenZymoseptoria tritici. We experimentally exposed strains to nutrient starvation and host infection stress. Contrary to expectations, we show that the two distinct conditions induce the expression of different sets of TEs. In particular, the most highly expressed TEs, including MITE and LTR-Gypsyelements, show highly distinct de-repression across stress conditions. Both the genomic context of TEs and the genetic background stress (i.e.different strains harboring the same TEs) were major predictors of de-repression dynamics under stress. Genomic defenses inducing point mutations in repetitive regions were largely ineffective to prevent TE de-repression. Consistent with TE de-repression being governed by epigenetic effects, we found that gene expression profiles under stress varied significantly depending on the proximity to the closest TEs. The unexpected complexity in TE responsiveness to stress across genetic backgrounds and genomic locations shows that species harbor substantial genetic variation to control TEs.

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogen Verticillium dahliae

“…Environmental changes can alter suppression mechanisms and drive a de-repression of TEs (Bouvet, et al 2008;Carr, et al 2010;Fouche, et al 2020). We observed TE expression upon changes in environmental conditions, i.e.…”

“…For further analysis, we considered only MS media for in vitro and in planta comparisons. Single-end sequencing reads of three biological replicates per condition were mapped to V. dahliae strain JR2 genome assembly (Faino, et al 2015) using STAR v.2.4.2.a, allowing multiple mapped reads with the following settings: --outFilterMultimapNmax 100 --winAnchorMultimapNmax 200 --outSAMtype BAM Unsorted --outFilterMismatchNmax 3 (Jin, et al 2015;Jin and Hammell 2018;Fouche, et al 2020). The bam files were sorted by read name with samtools v.1.2 and the transcriptional activity level was quantified using TEcount from the TEtrancripts package 2.2.1 (Jin, et al 2015), with the following parameters: --stranded no -mode multi, -iteration 1000.…”

A dispensable paralog of succinate dehydrogenase subunit C mediates standing resistance towards a subclass of SDHI fungicides in Zymoseptoria tritici

“…The molecular characterization of promoter insertions in other SHA-SDHIs-resistant isolates may therefore permit the discovery of additional mobile elements. In addition, the SHA-SDHIs sensitivity shift conferred by a de novo TE insertion in the promoter of a strain with low alt-SDHC protein expression may enable the selection of de novo insertions in directed evolution experiments [44]. As such the promoter of ZtSDHC3 and cognate SHA-SDHIs resistance may constitute a valuable system for the study of active TEs in Z. tritici.…”

A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen

“…We analyzed variation in TE copy numbers across families and found 483 that the expansions were mostly driven by Gypsy elements including the families Luna, Sol and 484 Venus, the Copia family Deimos and the LINE family Lucy (Figure 6C; Supplementary Figures S4-485 6). We also found a burst specific to the two North American populations in Helitron elements 486 (Ada), an increase specific to Swiss populations in LINE elements, and an increase in Analyses of sequence similarities and transcriptional activity suggest that several TE families are 532 actively creating new copies in the Z. tritici genome (Dhillon et al, 2014;Fouché et al, 2019). The 533 26 transposition activity in a genome and counter-acting purifying selection is expected to establish an 534 equilibrium over time (Charlesworth & Charlesworth, 1983).…”

“…Transposition activity of TEs also had a genome-wide impact on gene expression profiles during 121 infection (Fouché et al, 2019). The compact genome of ~39 Mb is completely assembled and 122 contains ~17% TEs (Goodwin et al, 2011;Dhillon et al, 2014).…”