A Bacterial Effector Hijacks NBR1 to Modulate Both Autophagy and Ubiquitination-Mediated Degradation That Promotes Bacterial Infection.

Autophagy and the ubiquitin/26S proteasome system (UPS) play critical roles in the immune defence of the host against pathogen invasion. As a countermeasure, pathogens deploy effector proteins to subvert or hijack autophagy and UPS processes. However, it is unclear whether and how a single pathogen effector coordinately modulates both proteolytic systems. Here, we identified a RING finger E3 ligase of Citrus sinensis, CsRHY1A, that directly interacts with SDE4405, an effector protein from Candidatus Liberibacter asiaticus (CLas), the causal agent of citrus Huanglongbing (HLB). CsRHY1A ubiquitinated SDE4405 at Lys87 and Lys92, causing SDE4405 degradation via the 26S proteasome. Furthermore, SDE4405 targeted the ubiquitin-associated (UBA) domain of the autophagic receptor NEIGHBOR OF BRCA1 (CsNBR1) and competitively disrupted CsRHY1A-mediated degradation by decreasing the ubiquitination of SDE4405. Lys87 and Lys92 of SDE4405 were required for its interactions with CsRHY1A and CsNBR1 and were essential for CsNBR1-dependent stabilisation of SDE4405. SDE4405 also inhibited the binding of CsNBR1 to CsATG8s, suppressing CsNBR1-mediated selective autophagic degradation of CLas effector protein SDE1. These findings reveal the sophisticated strategy of bacteria to counteract both autophagy and proteasome-dependent degradation, providing opportunities for developing HLB-resistant citrus varieties.