Integrated transcriptome and hormone dynamics uncover biphasic defense responses in sugar beet infected by Cercospora beticola

Abstract

Cercospora leaf spot (CLS), caused by the hemibiotrophic fungus Cercospora beticola , is a destructive foliar disease that threatens sugar beet production worldwide. Despite its economic significance, the molecular interaction between sugar beet and C. beticola is poorly understood. We report integrated time-resolved transcriptomics and hormone profiling of CLS infection spanning the asymptomatic and symptomatic phases. Our data revealed broad transcriptional changes, with defense and hormone-related processes being most altered. We detected transcriptional signatures consistent with activation of pathogen-associated molecular pattern- and effector-triggered immunity, along with differential expression of genes encoding putative receptor-like kinases and receptor-like proteins as well as nucleotide-binding (NB) leucine‑rich repeat (LRR) receptors (NLRs). Defense activation was evident as early as 3 days post-inoculation (dpi), including upregulation of pathogenesis-related proteins, genes related to systemic acquired resistance, and the hypersensitive response (HR). At 7 dpi, several biological processes, including defense response, showed overall downregulation, suggesting a pathogen-mediated suppression of transcriptional responses. During the symptomatic phase, defense-related genes—particularly those associated with HR and numerous putative NLRs—were induced again, illustrating a bi-phasic regulation pattern. Cis-element enrichment analysis showed significant overrepresentation of defense-related WRKY and AT-hook motif nuclear-localized protein binding motifs within the protomers of genes upregulated from 11 to 25 dpi. Parallel quantification of major phytohormones demonstrated stage-dependent modulation of infection-related hormone groups across the infection cycle. Our analysis revealed that a susceptible sugar beet genotype mounts an early and transient defense response against C. beticola , which appears to be pathogen-suppressed but later reactivated during symptom development. By integrating time-resolved transcriptome analysis and hormone profiling, our study links major defense transcriptional programs and phytohormone dynamics, providing a comprehensive view of sugar beet responses to CLS that complements and extends previous genotype-focused work.