Lr34/Yr18/Sr57/Pm38 confers broad-spectrum resistance to fungal diseases via transport of sinapyl alcohol for cell wall lignification in wheat

Widely known pleiotropic adult plant resistance (PAPR) gene, Lr34 encodes an ATP-binding cassette transporter and plays an important role in breeding wheat for enhancing resistance against multiple fungal diseases. Despite its recognized significance, the mechanism underlying Lr34 in pathogen defense remains largely elusive. Our study demonstrated that wheat lines harboring the Lr34res allele exhibit thicker cell walls and enhanced resistance to fungal penetration compared to lines lacking Lr34res. Transcriptome and metabolite profiling revealed that the lignin biosynthetic pathway was repressed in lr34 mutants, indicating a disruption in cell wall lignification. Furthermore, our investigation uncovered the hypersensitivity of lr34 mutant lines to sinapyl alcohol, a major monolignol crucial for cell wall lignification. Yeast accumulation and efflux assays confirmed that Lr34 protein functions as a sinapyl alcohol transporter. Both genetic and virus-induced gene silencing (VIGS) experiments revealed that the disease resistance conferred by Lr34 could be enhanced with the addition of the TaCOMT-3B gene, which is responsible for biosynthesis of sinapyl alcohol. Collectively, our findings provide novel insights into the role of Lr34 in disease resistance, through mediating sinapyl alcohol transport and cell wall deposition. Moreover, TaCOMT-3B plays a synergistic role in the Lr34 facilitated defensive lignification in adult wheat plants against multiple fungal pathogens.