OryR Is a LuxR-Family Protein Involved in Interkingdom Signaling between PathogenicXanthomonas oryzaepv. oryzae and Rice

Abstract

Xanthomonas oryzae pv. oryzae, the causal agent of bacterial leaf blight in rice, contains a regulator that is encoded in the genome, designated OryR, which belongs to the N-acyl homoserine lactone (AHL)-dependent quorum-sensing LuxR subfamily of proteins. However, we previously reported that X. oryzae pv. oryzae does not make AHLs and does not possess a LuxI-family AHL synthase and that the OryR protein is solubilized by a compound present in rice. In this study we obtained further evidence that OryR interacts with a rice signal molecule (RSM) and that the OryR concentration increases when rice is infected with X. oryzae pv. oryzae. We also describe three OryR target promoters which are regulated differently: (i) the neighboring proline iminopeptidase (pip) virulence gene, which is positively regulated by OryR in the presence of the RSM; (ii) the oryR promoter, which is negatively autoregulated independent of the RSM; and (iii) the 1,4-␤-cellobiosidase cbsA gene, which is positively regulated by OryR independent of the RSM. We also found that the RSM for OryR is small, is not related to AHLs, and is not able to activate the broad-range AHL biosensor Agrobacterium tumefaciens NT1(pZLQR). Furthermore, OryR does not regulate production of the quorum-sensing diffusible signal factor present in the genus Xanthomonas. Therefore, OryR has unique features and is an important regulator involved in interkingdom communication between the host and the pathogen.The species Xanthomonas oryzae includes two pathovars, X. oryzae pv. oryzae and X. oryzae pv. oryzicola, which are pathogens of rice, are closely related, and were initially considered pathovars of Xanthomonas campestris (28). X. oryzae pv. oryzae is a gram-negative rod-shaped bacterium that causes bacterial leaf blight (BLB), one of the most important diseases of rice.

Identification of the Quorum-Sensing Target DNA Sequence andN-Acyl Homoserine Lactone Responsiveness of theBrucella abortus virBpromoter

“…However, no homologues for AHL synthases were found in the genome of Brucella, and the pathway for intrinsic production of the autoinducer by B. melitensis remains unidentified. Thus, although this so-called orphan LuxR regulator conserves an AHL-responsive domain, there is a possibility that VjbR mediates interkingdom communication by detection of signaling molecules from its eukaryotic host, as occurs with OryR from Xanthomonas oryzae (12).…”

A Burkholderia cenocepacia Orphan LuxR Homolog Is Involved in Quorum-Sensing Regulation

“…oryzae, a variety of exogenous AHLs are not sufficient to solubilize the orphan LuxR homolog, OryR; however, solubilization occurs in the presence of a rice signal molecule (19). Furthermore, OryR regulates target genes in the absence or presence of the rice signal molecule (20). Protein solubilization and AHL binding are important factors when workers consider how LuxR regulators exert their effects.…”

Bacterial Subfamily of LuxR Regulators That Respond to Plant Compounds

“…campestris are two LuxR solos of plant-pathogenic species that are homologous to each other and are involved in interkingdom signaling as they respond to a plant compound(s) (15,16,50). Orthologues of OryR and XccR are also present in the genomes of several other plant-associated species of rhizobia and pseudomonads (16,50), indicating that they could represent a new subfamily of LuxR solos. However, there is a lack of information regarding their role in plant-associated biocontrol bacteria, as well as the range/nature of their target genes.…”