Transcriptomic and metabolomic analyses reveal defense mechanism in ‘Beta’ grapevine root border cells under ρ-hydroxybenzoic acid stress

Autotoxins are a major cause of grapevine replant disease. Root border cells (RBCs) of ‘Beta’ grapevine seedlings were selected to investigate the mechanism underlying the changes in the composition of grapevine root secretions mediated by autotoxins ρ-hydroxybenzoic acid (4-HBA) and their effect on harmful soil fungi (Fusarium solani). The results showed that, compared with control, the root length and number of RBCs were increased under 50 μg·mL–1 4-HBA treatment but inhibited under 200 μg·mL–1 treatment (T200), and no significant difference was found under 100 μg·mL–1 treatment (T100). In the T100 vs CK group, RBCs enhanced metabolites involved in the respiratory pathway and released carbon source substances, such as saccharides and organic acids. In addition, most metabolites of the flavonoid biosynthesis pathway and gallic acid (GA) of tannins were abundant in the RBC mucilage possibly due to the action of shikimate dehydrogenase (SDH). In the T200 vs CK group, abundance of some metabolites of the respiratory pathway decreased, and dihydroquercetin (DHQ), catechin (C), epicatechin gallate (ECG), quercetin derivative, and hesperetin derivative abundances of flavonoid biosynthesis pathway were inhibited possibly due to the declined expression level of PAL and CHS genes. Tannins [such as GA and ellagic acid (EA)] were also decreased in the mucilage of RBCs. Plate confrontation experiments showed that flavonoids [C, DHQ, and naringenin (NAR)] and tannin (GA) inhibited the growth of Fusarium solani to some extent. RBCs may also resist 4-HBA stress by increasing the expression level of lignin synthesis and SOD genes. Our research indicates that RBCs and their mucilage play an important role in protecting the root tips of grapevine against 4-HBA stress.