Derepression of BRANCHED1-Controlled Sucrose Hydrolysis Drives Bud Outgrowth and Phytoplasma-Induced Symptoms in Ziziphus jujuba

Sugar metabolism and signalling play major roles in the early events of axillary bud outgrowth by repressing BRANCHED 1 (BRC1) expression. However, whether BRC1 controls sugar metabolism during the cessation of axillary bud growth remains unknown. In previous research it was shown that jujube witches' broom (JWB) phytoplasma effectors SJP1 and SJP2-mediated ZjBRC1 degradation induced lateral main bud (LMB) outgrowth in Ziziphus jujuba. Here, we found that derepression of ZjBRC1-suppressed sucrose hydrolysis drove JWB phytoplasma-induced LMB outgrowth. ZjBRC1 complementation repressed axillary bud outgrowth in the Arabidopsis brc1-2 mutant by increasing sucrose accumulation. ZjBRC1 directly bound to and downregulated the promoter activities of the vacuolar invertase ZjVIN2, the neural or alkaline invertase ZjCIN9 and the sucrose synthase ZjSUSY5, contributing to sucrose accumulation. Fusing the SRDX repression domain to the C terminus of ZjBRC1 (ZjBRC1-SRDX) counteracted the repression and promoted sucrose hydrolysis in jujube calli. Compared with the control, JWB phytoplasma infection reduced the sucrose content and ZjBRC1 accumulation in growing LMBs, which was consistent with the results of the decapitation treatment. The effector SJP2 disrupted the balance between sucrose homeostasis and growth cessation, resulting in a shortened and repeated bud break-active growth cycle of LMBs in transgenic jujube plants. In this study we propose a potential model for JWB phytoplasma-mediated LMB outgrowth in which ZjBRC1 regulates sugar metabolism and signalling in a negative feedback loop in Ziziphus jujuba.