Dual impact of ambient pH on the virulence of Phytophthora nicotianae and resistance in tobacco.

key messageAmbient pH affects the virulence of Phytophthora nicotianae and activates NtFERL2 to enhance the resistance of tobacco to Phytophthora nicotianae. Tobacco is a globally important economic crop and plays a crucial role in agricultural production and rural development. Tobacco black shank, caused by Phytophthora nicotianae, results in severe biomass and yield losses across all major tobacco-growing regions. Variations in soil pH are known to reshape crop-pathogen interactions and pose a threat to productivity, yet how ambient pH affects the occurrence of diseases in plants remains poorly understood. Here, we observed that acidic ambient pH was more conducive to the growth and pathogenicity of P. nicotianae, which was correlated with promoted sporulation and mycelial bulges under laboratory conditions. In tobacco plants, acidic ambient pH increased susceptibility to the pathogen, whereas alkaline pH reduced disease severity. Transcriptome analysis with tobacco plants under different pH regimes for 4 weeks showed that genes involved in the plant-pathogen interaction, oxidative phosphorylation and mitogen-activated protein kinase (MAPK) signaling pathway were differentially expressed. We identified a receptor-like kinase, FERONIA-like 2 (FERL2), as a resistance factor exhibiting pH-dependent expression variations. Overexpression of FERL2 attenuated resistance differences across pH conditions by activating downstream defense signaling pathways, suggesting its essential role in pH-modulated immunity. Our study demonstrates that acidic pH enhances P. nicotianae virulence and compromises resistance, potentially through impairing FERL2-mediated signaling, providing strategic insights for controlling tobacco black shank under varying soil pH conditions.