Suppression of host salicylic acid defense by a phloem-colonizing pathogen effector in citrus Huanglongbing

Citrus Huanglongbing (HLB), caused by Candidatus Liberibacter asiaticus (CLas), severely threatens citrus production. Here, we identify Sec-delivered effector 10 (SDE10), a key effector from CLas, whose ectopic expression in citrus mimics HLB symptoms. Genetic and biochemical analyses demonstrate that SDE10 suppresses salicylic acid (SA)-mediated defense by inhibiting xylem cysteine peptidase 2 (CsXCP2). CsXCP2 positively regulates SA homeostasis through two activity-dependent mechanisms. First, it processes pathogenesis-related 1 (CsPR1) to generate cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins (CAP)-derived peptide 9 (CsCAPE9), which activates SA-mediated defense and significantly reduces CLas titers under both greenhouse and field conditions. Second, it degrades the CLas-derived SA hydroxylase (SahA), thereby preventing SA signaling disruption. Notably, engineered CsXCP2 variants that evade SDE10 binding while retaining moderate activity can counteract SDE10-mediated defense suppression. Collectively, our findings delineate a sophisticated molecular arms race between CLas virulence strategies and citrus immune countermeasures centered on SA signaling modulation, providing a mechanistic foundation for breeding HLB-resistant citrus varieties.