Investigation of the effectiveness and molecular mechanisms of thiamin priming to control early blight disease in potato

Authors: BERRIAN, TRENTON - Oregon State University; FABIAN, MATTHEW - Oak Ridge Institute For Science And Education (ORISE); ROGAN, CONNER - Oregon State University; ANDERSON, JEFFREY - Oregon State University; Clarke, Christopher; GOVER, AYMERIC - Oregon State University

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/19/2024
Publication Date: 3/19/2025
Citation: Berrian, T., Fabian, M., Rogan, C., Anderson, J., Clarke, C.R., Gover, A. 2025. Investigation of the effectiveness and molecular mechanisms of thiamin priming to control early blight disease in potato. Phytopathology. 115(3):234-246. https://doi.org/10.1094/PHYTO-09-24-0277-R.
DOI: https://doi.org/10.1094/PHYTO-09-24-0277-R

Interpretive Summary: Early blight is a major disease of potato caused by the fungal pathogen Alternaria solani. Sustainable, efficacious, and affordable chemical tools are needed for effective disease management of early blight. Currently available chemical tools for early bight disease management are fungicidal pesticides that are often expensive or environmentally hazardous. An alternative approach for managing foliar diseases is to prime the plant immune system to more effectively ward off pathogens. We tested the efficacy of Thiamin-induced immunity priming for mitigating A. solani disease impact. Thiamin has previously been shown to effectively prime immunity in other plants but has been seldom tested in potato. Foliar sprays with Thiamin shortly before A. solani infection significantly attenuated disease severity. However, the immunity priming induced by Thiamin was short-lived. We also performed the first in-depth investigation of molecular pathways differentially regulated by Thiamin treatment using transcriptomic and metabolomic tools. Potential explanatory effects of Thiamin treatment include differential expression of genes in known plant defense-associated hormone pathways and different accumulation of organic compounds involved in plant metabolism. These data suggest that Thiamin treatments may prime plant immunity responses through redirection of metabolism resources toward plant defenses.

Technical Abstract: In several plant species, thiamin foliar application primes plant immunity and can be effective in controlling various diseases. However, the effectiveness of thiamin against potato pathogens has seldom been investigated. Additionally, the transcriptomics and metabolomics of immune priming by thiamin have not previously been investigated. Here, we tested the effect of thiamin application against Alternaria solani, the causal agent of early blight in potato, and identified associated changes in gene expression and metabolite content. Thiamin applied on foliage at an optimal concentration of 10 mM reduced lesion size by ~33%. However, prevention of lesion growth was temporally limited, as a reduction of lesion size occurred when leaves were inoculated 4 h, but not 24 h, following thiamin treatment. Additionally, the effect of thiamin on lesion size was restricted to the application site and was not systemic. RNA-seq analysis showed that thiamin affected the expression of 308 genes involved in the synthesis of salicylic acid, secondary metabolites, fatty acid, chitin, primary metabolism, and photosynthesis. Genes in these pathways were also amongst the thousands of genes differentially regulated in the response to the pathogen alone, though they were often more differentially expressed and enriched when thiamin and the pathogen were combined. Thiamin also delayed the downregulation of photosynthesis-associated genes in plants inoculated with A. solani. Metabolite analyses revealed that thiamin treatment in the absence of a pathogen decreased the amounts of several organic compounds involved in the citric acid cycle. We hypothesize that thiamin primes plant defenses through perturbation of primary metabolism.