Stress-Driven Transposable Element De-repression Dynamics and Virulence Evolution 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. Plant pathogens are excellent models to dissect the impact of stress on TEs. The process of plant infection induces stress for the pathogen, and virulence factors (i.e., effectors) located in TE-rich regions become expressed. To dissect TE de-repression dynamics and contributions to virulence, we analyzed the TE expression landscape of four strains of the major wheat pathogen Zymoseptoria 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 miniature inverted-repeat transposable element and long terminal repeat-Gypsy element, 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 under stress. Gene expression profiles under stress varied significantly depending on the proximity to the closest TEs and genomic defenses against TEs were largely ineffective to prevent de-repression. Next, we analyzed the locus encoding the Avr3D1 effector. We show that the insertion and subsequent silencing of TEs in close proximity likely contributed to reduced expression and virulence on a specific wheat cultivar. The complexity of TE responsiveness to stress across genetic backgrounds and genomic locations demonstrates substantial intraspecific genetic variation to control TEs with consequences for virulence.

A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici

“…Overall, more than 70% of the TE families have non-zero transcription levels. This is consistent with recent findings of pervasive transcription of TEs in the Z. tritici genome under nutrient stress and during infection [45]. We find that the largest TE family, an unclassified LTR identified as RLX_LARD_Thrym, was the most transcribed with an average log 10 CPM4 .2 (Fig.…”

“…Genome expansions may also be triggered by TE mobilization. Stressors such as host defences during infection cause substantial TE derepression across the Z. tritici genome [45]. Taken together, TE dynamics and large effective population sizes likely constitute the proximate and ultimate drivers of pangenome size evolution.…”

“…For isolates 1A5, 1E4, 3D1 and 3D7, RNA sequencing experiments on minimal media were performed by [45,67]. Raw reads were retrieved from the NCBI Short Read Archive accession number SRP077418.…”

Genomic rearrangements generate hypervariable mini-chromosomes in host-specific lineages of the blast fungus

“…Repeats facilitate genomic rearrangements, such as interchromosomal translocations, in several plant pathogenic fungi [6,11,20,62,63]. Under stress conditions, specific classes of transposable elements can get activated and induce genomic rearrangements [64]. Interestingly, Peng et al [56] observed that the B71 mini-chromosome contains more active repeats than core chromosomes based on lower rates of repeat-induced point (RIP) mutations.…”

Advances in understanding the evolution of fungal genome architecture

“…Mobilization of transposable elements throughout the genome can mediate hypermutation at a larger scale than the single-nucleotide polymorphism changes in mismatch repair and DNA polymerase mutants. Within the past year, two studies have reported instances of hypermutation via mobilization of transposons under stress conditions, illustrating that host infection can trigger transposition in the human pathogen Cryptococcus deneoformans and in the plant pathogen Zymoseptoria tritici 51 , 52 . Another study has also characterized the evolutionary dynamics and genomic impacts of similar bursts of transposon expansion within the genomes of Microbotryum species 53 .…”