Yang, Zaiyu

SUMMARY 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’ ( C Las) simultaneously manipulates UPS and autophagy to subvert citrus immunity remains largely uncharacterized. Here, we functionally characterize the secreted C Las 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 C Las, 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 C Las effector synchronously rewires the UPS‐autophagy crosstalk to facilitate pathogen proliferation.

ABSTRACT The selective autophagy receptor NEIGHBOUR OF BRCA1 (NBR1) is a key regulator of plant immunity, but its role against bacterial pathogens remains poorly understood. Here, we demonstrated that overexpression of CsNBR1 confers citrus resistance to huanglongbing (HLB) caused by ‘ Candidatus Liberibacter asiaticus’ ( C Las). CsNBR1 can interact with multiple virulence effector proteins of C Las, including SDE5115, SDE1, SDE19 and SDE5, leading to their degradation via the autophagic pathway. In addition, expression of CsNBR1 in Nicotiana benthamiana mitigated the leaf curling and dwarfing phenotypes triggered by SDE1 by reducing the protein content of SDE1. These findings reveal that CsNBR1 positively regulates citrus defence against C Las by degrading its effector proteins via selective autophagy, providing both mechanistic insights and a potential target for resistance breeding.

ABSTRACT Ubiquitin‐proteasome is a conserved mechanism that regulates cellular responses and disease resistance in plants. However, the regulatory role of ubiquitin‐proteasome in the pathogenicity of “ Candidatus Liberibacter asiaticus” ( C Las), the causal agent of citrus huanglongbing (HLB), one of the most serious citrus diseases, remains poorly defined. In this study, we demonstrated that CLIBASIA_04250 (SDE4250) suppresses 26S proteasome activity in citrus, leading to a reduction in salicylic acid (SA) levels and downregulation of SA‐responsive genes. Further investigation revealed that SDE4250 specifically targets the citrus 26S proteasome non‐ATPase regulatory subunit 4 homologue (CsRPN10) and enhances its degradation via the 26S proteasome pathway. Moreover, overexpression of CsRPN10 inhibited C Las proliferation in citrus hairy roots, which was accompanied by a significant accumulation of SA content and upregulation of related defence genes. Collectively, our findings indicate that SDE4250 targets the citrus 26S proteasome to disrupt SA‐mediated citrus immunity.