Isocitrate lyase promotes Puccinia striiformis f. sp. tritici susceptibility in wheat (Triticum aestivum) by suppressing accumulation of glyoxylate cycle intermediates

SUMMARY Plant fungal parasites manipulate host metabolism to support their own survival. Among the many central metabolic pathways altered during infection, the glyoxylate cycle is frequently upregulated in both fungi and their host plants. Here, we examined the response of the glyoxylate cycle in bread wheat (Triticum aestivum) to infection by the obligate biotrophic fungal pathogen Puccinia striiformis f. sp. tritici (Pst). Gene expression analysis revealed that wheat genes encoding the two unique enzymes of the glyoxylate cycle, isocitrate lyase (TaICL) and malate synthase, diverged in their expression between susceptible and resistant Pst interactions. Focusing on TaICL, we determined that the TaICL B homoeolog is specifically upregulated during early stages of a successful Pst infection. Furthermore, disruption of the B homoeolog alone was sufficient to significantly perturb Pst disease progression. Indeed, Pst infection of the TaICL‐B disruption mutant (TaICL‐BY400*) was inhibited early during initial penetration, with the TaICL‐BY400* line also accumulating high levels of malic acid, citric acid, and aconitic acid. Exogenous application of malic acid or aconitic acid also suppressed Pst infection, with trans‐aconitic acid treatment having the most pronounced effect by decreasing fungal biomass 15‐fold. Thus, enhanced TaICL‐B expression during Pst infection may lower accumulation of malic acid and aconitic acid to promote Pst proliferation. As exogenous application of aconitic acid and malic acid has previously been shown to inhibit other critical pests and pathogens, we propose TaICL as a potential target for disruption in resistance breeding that could have wide‐reaching protective benefits for wheat and beyond. Significance Statement Isocitrate lyase (ICL) is a unique enzyme of the glyoxylate cycle that frequently accumulates in fungi and their host plants. We uncovered a critical role for wheat ICL in supporting Puccinia striiformis f. sp. tritici (Pst) infection. Disruption of ICL function in wheat prevented Pst disease progression, likely due to the accumulation of glyoxylate cycle intermediates that can suppress Pst infection. ICL thus represents a new potential target for disruption in resistance breeding.