Bacterial Acetyltransferase Effector AopP2 Primes Effector-Triggered Immunity in Watermelon by Acetylating a Conserved Transcription Factor.

Abstract

Bacterial fruit blotch (BFB), caused by Paracidovorax citrulli (Pc), threatens global watermelon production, yet genetic resistance remains scarce. This study investigates the potential of non-adapted interaction triggered by Paracidovorax avenae (Pa), a maize pathogen, to combat BFB in watermelon. We demonstrate that Pa strain ATCC 19860 elicits a hypersensitive response (HR) in watermelon via its type III secretion system (T3SS), inducing effector-triggered immunity (ETI). To rapidly screen for Pa type III effectors (T3Es) related to ETI, the nonpathogenic Pseudomonas fluorescens Effector-to-Host Analyzer (EtHAn) strain was used for transient expression of T3Es in watermelon. Among 13 candidate T3Es, the acetyltransferase AopP2 emerged as a potent inducer of programmed cell death (PCD) in watermelon, dependent on its enzymatic activity. AopP2 suppresses reactive oxygen species (ROS) bursts, salicylic acid (SA) signalling, while stabilizing the transcription factor ClTFIIB2 via acetylation, thereby activating ETI. Silencing ClTFIIB2 compromised both basal resistance to Pc and AopP2-induced PCD, whereas transient ClTFIIB2 expression via the EtHAn system enhanced resistance to Pc and AopP2-induced PCD. Notably, pretreatment with low-dose AopP2 primed watermelon defences, significantly reducing Pc proliferation. This study demonstrates that AopP2 suppresses pattern-triggered immunity (PTI) via CITFIIB2 acetylation while triggering ETI, revealing a conserved immune node exploitable for engineering resistance in watermelon. Our findings highlight the potential of non-adapted pathogen effectors as tools for activating ETI to identify disease resistance genes, and provide the first evidence of ClTFIIB2's critical role in watermelon immunity, offering novel strategies for BFB management.