Ubiquitin Receptor RPN13-Mediated “<i>Candidatus</i> <i>Liberibacter asiaticus</i>” Virulence Effector Degradation to Positively Regulate Immunity

Ubiquitin-proteasome is a conserved mechanism that regulates cellular responses and disease resistance in plants. However, the regulation role of ubiquitin-proteasome in the pathogenicity of "<i>Candidatus</i> <i>Liberibacter asiaticus</i>" (<i>C</i>Las), the causal agent of citrus Huanglongbing, one of the most serious citrus diseases, remains poorly defined. In this study, we identified a <i>C</i>Las effector, SDE5640 (CLIBASIA_05640), which downregulates salicylic acid signaling pathway genes and partial 26S proteasome genes in SDE5640-transgenic citrus shoots. SDE5640 suppresses proteasome activity to promote bacterial infection. Intriguingly, RPN13, a known component of the proteasome, was first identified as a new ubiquitin receptor. Overexpression of <i>NbRPN13</i> leads to the degradation of SDE5640 via the 26S proteasome system. We further revealed that SDE5640 can be ubiquitinated <i>in planta</i> and that NbRPN13 promotes the degradation of SDE5640 by binding to ubiquitinated SDE5640. Furthermore, transient coexpression of SDE5640 and <i>CsRPN13</i> enhances citrus resistance against <i>Xanthomonas</i>. Together, these results demonstrate that RPN13 recognizes the ubiquitination site of SDE5640 and specifically degrades it using the ubiquitin-proteasome system, which provides evidence for the role of ubiquitin-proteasome in <i>C</i>Las-citrus interactions.