MdXERICO negatively regulates salt tolerance in apple through ubiquitination and degradation of MdJAZ10

Abstract

The growth, development, and yield of the globally important economic crop, apple, are severely restricted by soil salinisation, which is driven by multiple environmental and human factors. Thus, breeding salt-tolerant apple varieties by deciphering key salt-stress response mechanisms is crucial for sustainable production. Although RING-H2-type E3 ubiquitin ligases play vital roles in plant adaptation to salt stress, their regulatory functions in apple remain incompletely understood. In this study, we identified MdXERICO, a RING-H2-type E3 ubiquitin ligase from apple, which was significantly induced by salt stress. Functional analysis revealed that MdXERICO negatively regulates apple salt tolerance, whereas its overexpression enhanced salt sensitivity, as evidenced by severe leaf wilting, reduced root activity, increased relative electrolyte leakage, accumulation of malondialdehyde, impaired photosynthetic capacity, and compromised antioxidant defense. However, silencing of MdXERICO improved salt tolerance. Further mechanistic investigation demonstrated that the MdXERICO protein interacts with MdJAZ10, a salt-stress-responsive positive regulator, both in vivo and in vitro. MdXERICO mediates ubiquitination and degradation of MdJAZ10 via the 26S proteasome pathway, while MdJAZ10 positively regulates apple salt tolerance by enhancing the expression of ion transport-related genes, such as MdSOS1, MdSOS2, MdSOS3, MdNHX1, MdHKT1, and MdHKT2 to maintain sodium-potassium homeostasis. In addition, silencing MdJAZ10 in the MdXERICO-Ri2 background weakens the salt tolerance of these plants. Therefore, our findings have uncovered a novel MdXERICO-MdJAZ10 regulatory module, in which MdXERICO negatively modulates apple salt tolerance by targeting MdJAZ10 for ubiquitin-dependent degradation, thereby suppressing the expression of ion-transport-related genes and disrupting sodium-potassium balance. This study provides new insights into the ubiquitination-mediated salt stress response mechanism in apple and identifies potential candidate genes for salt-tolerant breeding.