A homolog of the Arabidopsis TIME FOR COFFEE gene is involved in nonhost resistance to wheat stem rust in Brachypodium distachyon

Authors: DELLA COLETTA, RAFAEL - University Of Minnesota; LAVELL, ANASTASIYA - University Of Minnesota; Garvin, David

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/28/2021
Publication Date: 11/16/2021
Citation: Della Coletta, R., Lavell, A.A., Garvin, D.F. 2021. A homolog of the Arabidopsis TIME FOR COFFEE gene is involved in nonhost resistance to wheat stem rust in Brachypodium distachyon. Molecular Plant-Microbe Interactions. 34(11):1298-1306. https://doi.org/10.1094/MPMI-06-21-0137-R.
DOI: https://doi.org/10.1094/MPMI-06-21-0137-R

Interpretive Summary: Nonhost resistance is a biological phenomenon that holds promise as a strategy to control existing and emerging plant diseases that threaten global production of many crop species. One such example is wheat stem rust, with new races emerging that can overcome the existing resistance in most wheat varieties. However, the promise of employing nonhost resistance for protecting wheat against this disease requires a deeper understanding of its molecular and biochemical components, which are poorly understood. In this study, the model grass Brachypodium distachyon (Brachypodium), a nonhost of wheat stem rust, was mutagenized to identify a mutant that had lost its nonhost resistance to wheat stem rust. Genetic studies indicated that a single mutated locus is responsible for its susceptible phenotype. Genomic and bioinformatic analysis was employed to determine that the causal mutation is a single nucleotide deletion in a gene that, in the model plant Arabidopsis thaliana, acts as a sentinel to maintain the correct level of a protein that is a critical regulator of the jasmonic acid pathway. This hormone pathway plays a central role in inducible defense responses against many plant pathogens. It also can be manipulated by some pathogens to block a separate pathway, the salicylic acid pathway, from conferring resistance to another group of pathogens. We propose a model by which the loss of nonhost resistance in the mutant is likely due to the overaccumulation of the key jasmonic acid pathway regulatory protein, because the mutated gene can no longer accurately control levels of this protein. This in turns would have the potential to block a salicylic acid pathway defense response to wheat stem rust. This implies that the salicylic acid pathway is an important contributor to nonhost resistance to wheat stem rust in Brachypodium, and that positively modulating levels of this pathway may be a potential strategy for enhancing resistance to wheat stem rust in cereal crops.

Technical Abstract: Plants resist infection by pathogens using both preexisting barriers and inducible defense responses. Inducible responses are governed in a complex manner by various hormone signaling pathways. The relative contribution of hormone signaling pathways to nonhost resistance to pathogens is not well understood. In this study, we examined the molecular basis of disrupted nonhost resistance to two fungal Puccinia species of the genus that cause stem rust of wheat and timothy in an induced mutant of the model grass Brachypodium distachyon. Through bioinformatic analysis, a 1 base pair deletion in the mutant genotype was identified that introduces a premature stop codon in the gene Bradi1g24100, which is a homolog of the Arabidopsis thaliana gene TIME FOR COFFEE (TIC). In Arabidopsis, TIC is central to the regulation of the circadian clock and plays a crucial role in jasmonate signaling by attenuating levels of the transcription factor protein MYC2, and its mutational disruption results in enhanced susceptibility to the hemi-biotroph Pseudomonas syringae. Our similar finding for an obligate biotroph suggests that the biochemical role of TIC in mediating disease resistance to biotrophs is conserved in grasses, and that the ability to correctly modulate the jasmonate signaling pathway during infection by Puccinia species is essential for nonhost resistance to stem rust in B. distachyon.