The <i>Cephaleuros</i> spp. Causing Red Rust Disease in Oolong Tea ( <i>Camellia sinensis</i> ): Genetic Diversity, Pathogenicity, and Host Defense

Red rust disease, caused by the algal pathogen <i>Cephaleuros</i> spp., poses an increasingly significant threat to oolong tea (<i>Camellia sinensis</i>) cultivation. Currently, however, effective management is hindered by a lack of species-specific diagnostic methods and limited analysis of host-response physiological changes. In this study, the region-wide survey was conducted, species-specific molecular diagnostics, multi-scale microscopy, and host biochemical analysis (pigments and antioxidants) were utilized to investigate <i>Cephaleuros</i> diversity, invasion biology, and host responses in oolong tea. Across 785 composite leaf samples, the overall <i>Cephaleuros</i> positivity rate was 30.19%, with incidence significantly higher detection rate in Chaozhou, Guangdong (46.59%) than in Fujian (7.58%). Genotyping via psaA-targeted qPCR revealed strikingly distinct regional distributions: <i>C. parasiticus</i> was predominantly detected in Chaozhou (95.3%), whereas <i>C. virescens</i> was the only identified species in Fujian, with no mixed infections identified. Histological analysis of Chaozhou samples revealed subepidermal thalli beneath both leaf surfaces, accompanied by palisade/spongy necrosis, which suggested deeper tissue invasion by <i>C. parasiticus</i>. To characterize host responses, we quantified photosynthetic pigments and antioxidant enzymes in lesion centers and margins across representative cultivars. In green-leaf cultivars, infection was generally associated with decreases in chlorophyll a and b (with significance varying by cultivar), whereas carotenoid responses were modest and cultivar dependent. In contrast, two etiolated mutants exhibited significant increases in chlorophyll a (2.0-3.7-fold) and carotenoids (~1.5-1.6-fold), and anthocyanin increased by ~62% in the etiolated Juduozai mutant. Antioxidant enzyme activity was spatially structured, with peroxidase (POD) and catalase (CAT) strongly induced at lesion margins (POD increase 39-248%), while lesion centers exhibited reduced activity (5-41%). Superoxide dismutase (SOD) showed a modest increase at the lesion margins (increase 18-31%). A composite "reaction index" (POD+SOD at lesion margins) was used to classify cultivars into high and moderate response categories. These findings provide new insights into the ecological dynamics and host responses associated with Cephaleuros infection in oolong tea and highlight the potential for using these indicators in cultivar selection and disease management strategies.