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

Abstract

SignificanceBacterial infection has been extensively investigated; however, little is known about how bacterial pathogens timely shut down infecting machinery after successful infections. Here, a previously unknown sucrose–SghR/SghA–SAG–SA signaling axis was identified which controls the timing to shut off bacterial virulence expression and fine-tune host immune response. Sucrose, salicylic acid (SA), and its storage form SAG are small chemicals produced in plants whereas SghR is a bacterial sensor of sucrose and SghA is a bacterial enzyme that releases SA from SAG. Given that SA is an imperative signaling molecule in defense against a variety of microbial pathogens, these results depict a previously unknown 2-way chemical signaling cross-talk during microbe–host coevolution and shed mechanistic insights into host–bacteria interaction.

Structural basis of a novel repressor, SghR, controlling Agrobacterium infection by cross-talking to plants

“…It has also been reported that sucrose plays an important role in wound signaling (11) and endogenous signaling to induce defense responses against pathogens in rice (12). We found that the accumulated sucrose at the wound sites during healing appears to serve as an environmental stimulus involved in the SghR-SghA pair mediating the signaling cross-talk at the late stage of Agrobacterium infection (7).…”

“…The regulation of SghA by SghR SghA, an SA-releasing enzyme, has been implicated in immune response and tumorigenesis during Agrobacterium infection, which is likely relevant to SghR (7). To further reveal that SghA is regulated by SghR and that this pair, SghR-SghA, is involved in regulating plant tumor development, we examined the tumor occurrence and growth on carrot disks that are infected by either WT or deletion mutant Agrobacterium strains (DsghA, DsghR, and DsghRA).…”

“…Independent of VirA/VirG, we have recently found that a pair of novel proteins, SghR and SghA, regulate plant tumor growth through controlled release of the host defense signal salicylic acid (SA) by a previously uncharacterized mechanism. SghA is a glucosidase, controlling the release of SA from its inactive storage form, SA 2-O-b-D-glucoside, in host plants, which then activates plant immune response and shuts down bacterial virulence when the infection is successfully established (7).…”

Structural analysis of rice Os4BGlu18 monolignol β-glucosidase

“…DG is a glucose-like inhibitor that mimiks the expected oxocarbenium ion-like transition state in that the C1 carbon is sp 2 hybridized [ 51 ], and could be observed in the active site pocket. The Os4BGlu18-DG complex structure contains DG in the ring-form in a 4 H 3 / 4 E conformation (Cremer-Pople parameters: φ (°), θ (°), Q : 224.521, 47.426, 0.534 and 227.030, 44.337, 0.524 in molecules A and B, respectively) [ 52 ] via hydrogen bonds with the surrounding residues, as shown in Fig 2A . This DG ring was also observed in Phanerochaete chrysosporium β-glucosidase [ 47 ] and Neotermes koshunensis β-glucosidase [ 48 ], while an open-form was seen in Bacillus polymyxa β-glucosidase [ 49 ].…”

“…respectively) [52] via hydrogen bonds with the surrounding residues, as shown in Fig 2A . This DG ring was also observed in Phanerochaete chrysosporium β-glucosidase [47] and Neotermes koshunensis β-glucosidase [48], while an open-form was seen in Bacillus polymyxa β-glucosidase [49]. In the active site of Os4BGlu18-DG, the O1 atom of DG forms strong hydrogen bonds to E194 Oε2 (2.3 Å) and E408 Oε1 (3.1 Å).…”