Succinic Semialdehyde Promotes Prosurvival Capability of Agrobacterium tumefaciens

Abstract

Succinic semialdehyde (SSA), an important metabolite of ␥-aminobutyric acid (GABA), is a ligand of the repressor AttJ regulating the expression of the attJ-attKLM gene cluster in the plant pathogen Agrobacterium tumefaciens. While the response of A. tumefaciens to GABA and the function of attKLM have been extensively studied, genetic and physiological responses of A. tumefaciens to SSA remain unknown. In combination with microarray and genetic approaches, this study sets out to explore new roles of the SSA-AttJKLM regulatory mechanism during bacterial infection. The results showed that SSA plays a key role in regulation of several bacterial activities, including C 4 -dicarboxylate utilization, nitrate assimilation, and resistance to oxidative stress. Interestingly, while the SSA relies heavily on the functional AttKLM in mediating nitrate assimilation and oxidative stress resistance, the compound could regulate utilization of C 4 -dicarboxylates independent of AttJKLM. We further provide evidence that SSA controls C 4 -dicarboxylate utilization through induction of an SSA importer and that disruption of attKLM attenuates the tumorigenicity of A. tumefaciens. Taken together, these findings indicate that SSA could be a potent plant signal which, together with AttKLM, plays a vital role in promoting the bacterial prosurvival abilities during infection. IMPORTANCE Agrobacterium tumefaciens is a plant pathogen causing crown gall diseases and has been well known as

The biotroph Agrobacterium tumefaciens thrives in tumors by exploiting a wide spectrum of plant host metabolites

“…In the host plant, GABA is mainly produced from glutamate (by GABA decarboxylase) and then degraded into SSA (by GABA transaminase), which is in turn converted into succinate (by SSA dehydrogenase) or GHB (by GHB reductase) (Bown & Shelp, ). SSA is a toxic metabolite provoking an oxidative stress in plants and other organisms and microorganisms, including A. tumefaciens (Bouché et al ., ; Ludewig et al ., ; Wang et al ., ). In plant tumors, A. tumefaciens may exploit plant GABA and GHB as N and C sources but has to face toxic SSA – either exogenous SSA resulting from plant metabolism or endogenous SSA as an intermediate of the A. tumefaciens GABA and GHB degradation pathways.…”

“…In culture assays, Wang et al . () showed that a pre‐exposure of A. tumefaciens to extracellular SSA induces an oxidative stress response and increases resistance of A. tumefaciens to hydrogen peroxide. Noticeably, this effect was lost in a blcABC KO‐mutant (Wang et al ., ).…”

“…() showed that a pre‐exposure of A. tumefaciens to extracellular SSA induces an oxidative stress response and increases resistance of A. tumefaciens to hydrogen peroxide. Noticeably, this effect was lost in a blcABC KO‐mutant (Wang et al ., ). Our study showed that a blc KO‐mutant was impaired for inducing tumors on tomato stems, as well as colonizing plant tumors and competing with a wild‐type strain in the plant tumors.…”

Agrobacteria reprogram virulence gene expression by controlled release of host-conjugated signals

“…The PCR product was digested by BamHI and cloned in pLAFR3, and the resultant construct pLA- sghA was verified by sequencing before transformation into A. tumefaciens by electroporation (15). Deletion of SghR, SghA, and its double deletion were performed according to Wang et al (36).…”

The versatile GABA in plants

“…63 In nitric oxide (NO)-induced chilling tolerance, NO treatment increased the activities of diamine oxidase, polyamine oxidase and glutamate decarboxylase while reducing GABA-T activity to lower levels, which altogether resulted in GABA accumulation. 64,65…”