The plant signal salicylic acid shuts down expression of the vir regulon and activates quormone-quenching genes in Agrobacterium

Abstract

Agrobacterium tumefaciens is capable of transferring and integrating an oncogenic T-DNA (transferred DNA) from its tumor-inducing (Ti) plasmid into dicotyledonous plants. This transfer requires that the virulence genes (vir regulon) be induced by plant signals such as acetosyringone in an acidic environment. Salicylic acid (SA) is a key signal molecule in regulating plant defense against pathogens. However, how SA influences Agrobacterium and its interactions with plants is poorly understood. Here we show that SA can directly shut down the expression of the vir regulon. SA specifically inhibited the expression of the Agrobacterium virA/G two-component regulatory system that tightly controls the expression of the vir regulon including the repABC operon on the Ti plasmid. We provide evidence suggesting that SA attenuates the function of the VirA kinase domain. Independent of its effect on the vir regulon, SA up-regulated the attKLM operon, which functions in degrading the bacterial quormone N-acylhomoserine lactone. Plants defective in SA accumulation were more susceptible to Agrobacterium infection, whereas plants overproducing SA were relatively recalcitrant to tumor formation. Our results illustrate that SA, besides its well known function in regulating plant defense, can also interfere directly with several aspects of the Agrobacterium infection process.two-component system ͉ tumorigenesis ͉ defense response ͉ rhizosphere ͉ plant-microbe interaction

Agrobacterium tumefaciensPromotes Tumor Induction by Modulating Pathogen Defense inArabidopsis thaliana

“…Instead, SA may exert a direct effect on the Agrobacterium's virulence machinery. This was also supported by our findings and those of others (Yuan et al, 2007) that mutant plants with low SA levels promote, whereas those with high SA levels inhibit, tumor growth ( Figure 7A). Furthermore, constitutively high levels of SA and PR gene expression interfered with the expression of oncogenes, since the cpr5 mutant expressed only very low numbers of ipt transcripts at 6 d postinoculation compared with wild-type plants (Figure 8).…”

“…The elevated auxin levels at 6 d postinoculation and in tumors may promote agrobacteria invasion by suppression of SA-mediated host defenses. Recently it has been shown that SA has an inhibitory effect on virulence of agrobacteria (Yuan et al, 2007;Anand et al, 2008). SA directly inhibits the expression of the vir regulon of the Ti plasmid that is essential for the transfer and integration of the T-DNA into the host genome.…”

“…Levels of SA, however, accumulate to those seen in wild-type plants in response to infection by various pathogens. Previous studies have uncovered a role for SA on Agrobacterium by inhibiting vir gene induction (Yuan et al, 2007, Anand et al, 2008 and thereby affecting agrobacterial virulence. By contrast, defense reactions against many necrotrophic fungi do not involve SA, but rely on ET and JA accumulation and signaling.…”

Exploiting Quorum Sensing To Confuse Bacterial Pathogens

“…AttM appears to contribute to bacterial fitness within the plant tumor (63) and may also function in interkingdom signaling between the plant and the bacterium. Salicylic acid and the nonprotein amino acid GABA, both naturally found in plants, have been shown to induce attM expression (97)(98)(99), and overexpression of either of these compounds in plants increases the plant's resistance to A. tumefaciens infection (97,98). Additionally, proline, which is a competitive antagonist of GABA import into Agrobacterium, accumulates in plant gall tumors, where it may function to limit GABA-induced AHL degradation (100).…”

In silico characterization of three two-component systems of Ehrlichia canis and evaluation of a natural plant-derived inhibitor

“…This pair of TCSs can sense the presence of phenolic compounds released by wounded plants, thereby triggering the activation of several genes involved in tumor induction (Lin et al, 2008). Conversely, (2H)-1,4-benzoxazin-3(4H)-one (BOA) and salicylic acid (SA), two plant phenolic compounds, can inhibit A. tumefaciens infection by blocking the expression of VirA/VirG (Zhang et al, 2000;Yuan et al, 2007).…”