Transcription Factor MdbHLH093 Enhances Powdery Mildew Resistance by Promoting Salicylic Acid Signaling and Hydrogen Peroxide Accumulation

Abstract

Powdery mildew is an apple disease caused by the obligate trophic fungus Podosphaera leucotricha. Basic helix–loop–helix (bHLH) transcription factors play important roles in plant development and stress responses, and they have been widely studied in model plants such as Arabidopsis thaliana. However, their role in the stress response of perennial fruit trees remains unclear. Here, we investigated the role of MdbHLH093 in the powdery mildew of apples. The expression of MdbHLH093 was significantly induced during the infection of apples with powdery mildew, and the allogenic overexpression of MdbHLH093 in A. thaliana enhanced the resistance to powdery mildew by increasing the accumulation of hydrogen peroxide (H2O2) and activating the salicylic acid (SA) signaling pathway. The transient overexpression of MdbHLH093 in apple leaves increased the resistance to powdery mildew. Conversely, when MdbHLH093 expression was silenced, the sensitivity of apple leaves to powdery mildew was increased. The physical interaction between MdbHLH093 and MdMYB116 was demonstrated by yeast two-hybrid, bi-molecular fluorescence complementation, and split luciferase experiments. Collectively, these results indicate that MdbHLH093 interacts with MdMYB116 to improve apple resistance to powdery mildew by increasing the accumulation of H2O2 and activating the SA signaling pathway, as well as by providing a new candidate gene for resistance molecular breeding.