'Candidatus Liberibacter asiaticus' secretory protein SDE5640 activates host autophagy dependent on PSMD10 to mediate PBA1 degradation.

The ubiquitin proteasome system (UPS) and autophagy cooperatively orchestrate plant immune homeostasis, while diverse phytopathogens deploy secreted effectors to disrupt their crosstalk for successful colonization. Proteaphagy, the autophagic turnover of intact 26S proteasome holoenzymes, is a conserved stress response co-opted by Pseudomonas syringae effector HopM1 to cripple host proteolysis. However, how the Huanglongbing (HLB) pathogen 'Candidatus Liberibacter asiaticus' (CLas) simultaneously manipulates UPS and autophagy to subvert citrus immunity remains largely uncharacterized. Here, we functionally characterize the secreted CLas effector SDE5640, which exacerbates HLB susceptibility in sweet orange (Citrus sinensis). SDE5640 directly binds the 19S proteasome chaperone CsPSMD10, whose homodimerization via Cys163/Cys190 disulfide bonds is required for immune suppression. CsPSMD10 overexpression enhances citrus susceptibility to CLas, whereas the dimerization-deficient CsPSMD10-C190S mutant confers robust HLB resistance. Mechanistically, CsPSMD10 targets CsATG8 isoforms for UPS-dependent degradation to restrain autophagic flux; SDE5640 competitively occupies the Ank2/Ank3 domains of CsPSMD10 to disrupt CsPSMD10-CsATG8c complexes, thereby stabilizing CsATG8c and triggering autophagy dependent on CsPSMD10. Moreover, SDE5640-induced autophagy drives selective autophagic degradation of the 20S proteasome catalytic subunit CsPBA1, which ultimately disrupts cellular proteasome activity and attenuates salicylic acid-mediated citrus immunity. Collectively, our findings identify a novel SDE5640-CsPSMD10-CsATG8c-CsPBA1 regulatory cascade, illustrating how a single CLas effector synchronously rewires the UPS-autophagy crosstalk to facilitate pathogen proliferation.