Spatiotemporal patterns of wheat response to Pyrenophora tritici-repentis in asymptomatic regions revealed by transcriptomic and X-ray fluorescence microscopy analyses.

Abstract

Pathogen attacks elicit dynamic and widespread molecular responses in plants. While our understanding of plant responses has advanced considerably, little is known of the molecular responses in the asymptomatic "green" regions (AGR) adjoining lesions. Here, we explore gene expression data and high-resolution elemental imaging to report the spatiotemporal changes in the AGR of susceptible and moderately resistant wheat cultivars infected with a necrotrophic fungal pathogen, Pyrenophora tritici-repentis (Ptr). We show, with improved spatiotemporal resolution, that calcium oscillations are modified in the susceptible cultivar, resulting in "frozen" host defence signals at the mature disease stage, and silencing of the host's recognition and defence mechanisms which would otherwise protect it from further attacks. In contrast, Ca accumulation and heightened defence response was observed in the moderately resistant cultivar in the later stage of disease development. Furthermore, in the susceptible interaction, the AGR was unable to recover post disease disruption. Our targeted sampling technique also enabled detection of eight previously predicted proteinaceous effectors in addition to the known ToxA effector. Collectively, our results highlight the benefits of spatially resolved molecular analysis and nutrient mapping to provide high-resolution spatiotemporal snapshots of host-pathogen interactions, paving the way for detangling complex disease interactions in plants.