Unlocking the genetic control of early seedling resistance to wheat powdery mildew through microphenomics.

BACKGROUND: Powdery mildew is one of the most devastating diseases affecting wheat-growing areas worldwide. The most effective strategy for managing this disease is through the cultivation of resistant genotypes. RESULTS: In this study, early resistance was assessed in a set of 197 spring wheat genotypes using a novel Microphenomics approach. Parameters measured using this technique were: the number of micro-colonies 48 h post-infection (N48), the median colony area 72 h post-infection (M72), and the area under the disease progress curve (AUDPC). No significant correlations were found among these parameters. Single-locus and multi-locus GWAS revealed 57, 61, and 57 significant markers associated with N48, M72, and AUDPC, respectively. These markers were located within 29, 42, and 34 genes, respectively. Gene enrichment analysis uncovered 17 biological processes (BP), 13 cellular components, and one molecular function pathway. The 17 BP pathways formed a single network controlled by five gene models. Eight genotypes were identified as highly resistant based on all evaluation parameters. CONCLUSION: Microphenomics is a cutting-edge technique that facilitates large-scale quantification of the early, often critical stages of plant-pathogen interactions, providing unprecedented insights into the infection process and enabling the discovery of new resistance mechanisms. SL and ML-GWAS, along with gene enrichment analysis, provided a deeper understanding of the genetic control of WPM early resistance. Genotypes from Oman and the UK were particularly notable as good sources for improving early resistance to wheat powdery mildew due to their superior response and the high genetic distance between them and the German genotypes. © 2025 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.