Field pathogenomics and evolutionary conservation unveil CRISPR-targetable susceptibility genes for wheat blast resistance

Abstract

Abstract Wheat blast, caused by Magnaporthe oryzae pathotype Triticum (MoT), threatens global wheat production, yet durable resistance mechanisms remain elusive. Current strategies relying on race-specific resistance genes or fungicides are vulnerable to pathogen evolution and inefficacy. Here, we investigated field-derived transcriptomes from the 2016 Bangladesh wheat blast epidemic, a catastrophic event devastating all local varieties to identify host susceptibility ( S ) genes co-opted by MoT. By analyzing RNA-seq data from infected and healthy plants across geographically distinct regions, we pinpointed 273 consistently upregulated wheat genes, enriched in defense-related pathways. Ortholog analysis with rice, a model for blast resistance, identified three conserved susceptibility ( S )-gene candidates: TaSULTR3-3B (an ortholog of a rice bacterial blight susceptibility gene), TaSTP3-4D (associated with stripe rust), and TaMLO1-5A (a wheat powdery mildew susceptibility gene). While all three candidates exhibited significant expression correlation with M. oryzae Triticum (MoT) effectors in field-derived samples, in planta spike assays revealed distinct expression dynamics. Only TaMLO1-5A was significantly upregulated in the susceptible cultivar BARI Gom 26 following MoT inoculation, with no induction observed in the resistant cultivar S-615 (carrying Rmg8 ). Conversely, TaSULTR3-3B and TaSTP3-4D did not show significant induction under the specific conditions and time points of the in planta spike assays. This discrepancy potentially arises from tissue-specific regulation (spike vs. leaf), environmental variations, or differences in sampling time points between the field and greenhouse experiments. Disruption of such S genes, validated in other cereals for durable resistance, offers a transformative strategy to engineer non-race-specific wheat blast resilience. Our findings shift the paradigm from transient resistance genes to foundational susceptibility networks, proposing CRISPR-based editing of the candidate gene as an actionable target. This approach, resilient to pathogen evolution, could preempt epidemics in climate-vulnerable regions, safeguarding global wheat security. By bridging field pathogenomics and evolutionary genomics, we provide a roadmap for sustainable disease management in an era of expanding fungal threats.