Transcriptome Profiling and Functional Analysis ofAgrobacterium tumefaciensReveals a General Conserved Response to Acidic Conditions (pH 5.5) and a Complex Acid-Mediated Signaling Involved inAgrobacterium-Plant Interactions
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ABSTRACTAgrobacterium tumefacienstransferred DNA (T-DNA) transfer requires that the virulence genes (virregulon) on the tumor-inducing (Ti) plasmid be induced by plant phenolic signals in an acidic environment. Using transcriptome analysis, we found that these acidic conditions elicit two distinct responses: (i) a general and conserved response through whichAgrobacteriummodulates gene expression patterns to adapt to environmental acidification and (ii) a highly specialized acid-mediated signaling response involved inAgrobacterium-plant interactions. Overall, 78 genes were induced and 74 genes were repressed significantly under acidic conditions (pH 5.5) compared to neutral conditions (pH 7.0). Microarray analysis not only confirmed previously identified acid-inducible genes but also uncovered many new acid-induced genes which may be directly involved inAgrobacterium-plant interactions. These genes includevirE0,virE1,virH1, andvirH2. Further, thechvG-chvItwo-component system, previously shown to be critical for virulence, was also induced under acid conditions. Interestingly, acidic conditions induced a type VI secretion system and a putative nonheme catalase. We provide evidence suggesting that acid-induced gene expression was independent of the VirA-VirG two-component system. Our results, together with previous data, support the hypothesis that there is three-step sequential activation of thevirregulon. This process involves a cascade regulation and hierarchical signaling pathway featuring initial direct activation of the VirA-VirG system by the acid-activated ChvG-ChvI system. Our data strengthen the notion thatAgrobacteriumhas evolved a mechanism to perceive and subvert the acidic conditions of the rhizosphere to an important signal that initiates and directs the early virulence program, culminating in T-DNA transfer.
