Responses to temperature shocks in Zymoseptoria tritici reveal specific transcriptional reprogramming and novel candidate genes for thermal adaptation

Abstract

Pathogens responses to sudden temperature fluctuations, spanning various temporal scales, are critical determinants of their survival, growth, reproduction, and homeostasis. Here, we combined phenotyping, transcriptomics, and genome-wide association approaches to investigate how the wheat pathogen Zymoseptoria tritici responds to and recovers from temperature shocks. Survival emerged as the most significantly affected trait immediately following temperature shocks across 122 geographically diverse strains. In contrast, post-recovery phenotypic traits, including growth rate and melanization, showed no significant deviations from control conditions. Transcriptomic analyses of a reference strain revealed temperature stress-specific gene expression patterns, with genes involved in protein folding, redox homeostasis, membrane stabilization, and cell-wall remodeling playing central roles in the response. A multi-reference k-mer genome-wide association study (GWAS) identified six loci significantly associated with cold shock responses. Among these, two loci emerged as strong candidates for near-freezing temperature adaptation, including a 60S ribosomal protein gene involved in protein synthesis and stress recovery, and an NADH oxidoreductase gene implicated in redox homeostasis and oxidative stress tolerance. These findings shed light on the distinct molecular strategies Z. tritici employs to adapt to temperature stress and provide novel insights into fungal resilience under dynamic environmental conditions. Author summaryTemperature fluctuations, an inherent aspect of natural environments, are increasingly exacerbated by climate change, intensifying challenges for organisms to maintain homeostasis amid more frequent and severe extreme weather events. This study reveals distinct phenotypic, transcriptomic, and genetic mechanisms underlying Z. triticis responses to short-term temperature shocks. Survival-related phenotypic traits were significantly reduced by heat and cold shocks, while other traits measured after a recovery period demonstrated the resilience of Z. tritici strains to temperature stress, reflecting efficient recovery mechanisms. Transcriptomic analyses uncovered temperature-specific gene expression patterns, emphasizing unique regulatory strategies, which mostly return to baseline levels after a recovery period. The discovery of novel loci associated with cold shock responses provides valuable insights into the genetic basis of resilience to short-term temperature stress, offering a foundation for future research on pathogen adaptation to fluctuating environments.