Sorbitol Modulates Resistance to <i>Alternaria alternata</i> by Regulating the Expression of an <i>NLR</i> Resistance Gene in Apple

Abstract

In plant-microbe interactions, plant sugars produced by photosynthesis are not only a carbon source for pathogens, but may also act as signals that modulate plant defense responses. Here, we report that decreasing sorbitol synthesis in apple (<i>Malus domestica</i>) leaves by antisense suppression of <i>ALDOSE-6-PHOSPHATE REDUCTASE</i> (<i>A6PR</i>) leads to downregulation of 56 <i>NUCLEOTIDE BINDING/LEUCINE-RICH REPEAT</i> (<i>NLR</i>) genes and converts the phenotypic response to <i>Alternaria alternata</i> from resistant to susceptible. We identified a resistance protein encoded by the apple <i>MdNLR16</i> gene and a small protein encoded by the fungal <i>HRIP1</i> gene that interact in both a yeast two-hybrid assay and a bimolecular fluorescence complementation assay. Deletion of <i>HRIP1</i> in <i>A. alternata</i> enables gain of virulence on the wild-type control plant. Overexpression of <i>MdNLR16</i> in two antisense <i>A6PR</i> lines increases resistance, whereas RNAi suppression of <i>MdNLR16</i> in the wild-type control decreases resistance against <i>A. alternata</i> MdWRKY79 transcriptionally regulates <i>MdNLR16</i> by binding to the promoter of <i>MdNLR16</i> in response to sorbitol, and exogenous sorbitol feeding partially restores resistance of the antisense <i>A6PR</i> lines to <i>A. alternata</i> These findings indicate that sorbitol modulates resistance to <i>A. alternata</i> via the MdNLR16 protein that interacts with the fungal effector in a classic gene-for-gene manner in apple.