In a previous study, tomato race 3 (T3) strains of Xanthomonas perforans became predominant in fields containing both X. euvesicatoria and X. perforans races T1 and T3, respectively. This apparent ability to take over fields led to the discovery that there are three bacteriocin-like compounds associated with T3 strains. Bacterial spot of tomatoes and peppers is caused by Xanthomonas campestris pv. vesicatoria. Pohronezny and Volin (34) estimated that as high as 50% loss of marketable fruit was due to bacterial spot on tomatoes. Control of bacterial spot of tomato is difficult when high temperatures and high moisture exist. Bactericides, such as fixed coppers and streptomycin, have provided the primary means of control (30,45,46); however, streptomycin-resistant mutants and copper-tolerant strains became prevalent on treated plants (46). Marco and Stall (30) showed that many Xanthomonas euvesicatoria strains were tolerant of copper and addition of mancozeb to copper sprays improved control of the copper-tolerant strains (6, 30). However, they also showed that this treatment is insufficient when conditions favorable for disease development exist.On tomato, three races, designated tomato race 1 (T1), T2, and T3, were identified based on their reaction on three tomato genotypes (25,26, 44). Recent reclassification of the xanthomonads associated with bacterial spot of tomato has changed the species classification of these races. Currently, T1 strains are classified as X. euvesicatoria, T2 strains are classified as X. vesicatoria, and T3 strains are now classified as Xanthomonas perforans (24). T1 and T2 were first identified in 1990 (55) and are distributed worldwide (3), although only T1 strains were present in Florida until the early 1990s. In 1991, T3 appeared in Florida fields (26) and eventually predominated (22). This new race had antagonistic activity toward T1 strains (8) and was determined to be a new group designated group C (23). Genetically, T3 strains are most closely related to T1 strains based on DNA similarity values (23).In a previous study, wild type (WT) T3 strains were shown to be antagonistic toward WT T1 strains (8). Tudor-Nelson et al. (52) identified three cosmid clones, designated BCN-A, BCN-B, and BCN-C, which were found to confer the ability to inhibit a sensitive T1 strain in plate assays. These compounds were determined to have narrow inhibition spectra and fit the definition of a bacteriocin described by Reeves (36) based on the following criteria: (i) the presence of a biologically active protein moiety, (ii) inducibility with mitomycin C, and (iii) non-self inhibition (52). The three clones isolated by TudorNelson et al. (52) were unique in activity and specificity based on differential inhibition of selected sensitive T1 and T2 strains (52). It has been speculated that the bacteriocins may confer in part or completely this competitive advantage.Of the bacteriocins which have been well characterized in
A bacteriocin-producing strain of the bacterial spot of tomato plant pathogen, Xanthomonas perforans, with attenuated pathogenicity was deployed for biocontrol of a bacteriocin-sensitive strain of the genetically closely related bacterial spot of tomato plant pathogen, X. euvesicatoria. The attenuated mutant (91-118⌬opgH⌬bcnB) of X. perforans was tested in leaf tissue and shown to significantly inhibit internal populations of the wild-type X. euvesicatoria strain although significantly less than the wild-type 91-118 strain, whereas in a phyllosphere inhibition assay, the mutant strain reduced epiphytic populations comparably to 91-118. Thus, the attenuated mutant limited the sensitive bacterium more efficiently on the leaf surface than inside the leaf. In field experiments, weekly application of 91-118⌬opgH⌬bcnB significantly reduced X. euvesicatoria populations compared to the growers' standard control (copper hydroxide and mancozeb applied weekly and acibenzolar-Smethyl applied every 2 weeks). The biological control agent, 91-118⌬opgH⌬bcnB, applied every 2 weeks also significantly reduced X. euvesicatoria populations in one season but was not significantly different from the growers' standard control. Potentially, attenuated pathogenic strains could be deployed as biological control agents in order to improve disease control of foliar plant pathogens.Bacterial spot of tomato is incited by several Xanthomonas spp., including Xanthomonas euvesicatoria, X. perforans, and X. vesicatoria (13). On tomato plants, three races, designated tomato race 1 (T1), T2, and T3, were originally identified based on their reactions on three tomato genotypes (22,23,33,37). These races, T1, T2, and T3, are principally members of X. euvesicatoria, X. vesicatoria, and X. perforans, respectively. Control of bacterial spot of tomato is extremely difficult when moderate-to-high temperatures and high moisture conditions exist. The disease causes significant damage to the crop, resulting in major losses (27). Management is primarily limited to bactericides, such as fixed coppers (3,20,32); however, copper-tolerant strains have become prevalent (31, 32) and chemical control alone is insufficient to control the disease under optimal weather conditions. Additionally, the use of copper compounds has led to soil contamination in some instances (16).Recently, there has been increased interest in integrated biological control strategies for bacterial diseases (5,7,11,19,23). However, optimization of biocontrol agents for consistent disease suppression for many bacterial diseases has been difficult. Studies are increasing our understanding of the ecology of nonpathogenic saprophytes as biocontrol agents, but their selection is limited to labor-intensive protocols. New biological control strategies are currently being sought, including the use of bacteriocins, bacteriophages, and attenuated plant pathogens (4,5,7,9,11,23,26,35,38).For many years, only X. euvesicatoria (T1) was present on tomato plants in Florida. In 1991, X. perforans (T3) appeare...
Bacterial spot is a destructive disease of tomato in Florida that prior to the early 1990s was caused by Xanthomonas euvesicatoria. X. perforans was first identified in Florida in 1991 and by 2006 was the only xanthomonad associated with bacterial spot disease in tomato. The ability of an X. perforans strain to outcompete X. euvesicatoria both in vitro and in vivo was at least in part associated with the production of three bacteriocins designated Bcn-A, Bcn-B, and Bcn-C. The objective of this study was to characterize the genetic determinants of these bacteriocins. Bcn-A activity was confined to one locus consisting of five ORFs of which three (ORFA, ORF2 and ORF4) were required for bacteriocin activity. The fifth ORF is predicted to encode an immunity protein to Bcn-A based on in vitro and in vivo assays. The first ORF encodes Bcn-A, a 1,398 amino acid protein, which bioinformatic analysis predicts to be a member of the RHS family of toxins. Based on results of homology modeling, we hypothesize that the amino terminus of Bcn-A interacts with a protein in the outer membrane of X. euvesicatoria. The carboxy terminus of the protein may interact with an as yet unknown protein(s) and puncture the X. euvesicatoria membrane, thereby delivering the accessory proteins into the target and causing cell death. Bcn-A appears to be activated upon secretion based on cell fractionation assays. The other two loci were each shown to be single ORFs encoding Bcn-B and Bcn-C. Both gene products possess homology toward known proteases. Proteinase activity for both Bcn-B and Bcn-C was confirmed using a milk agar assay. Bcn-B is predicted to be an ArgC-like serine protease, which was confirmed by PMSF inhibition of proteolytic activity, whereas Bcn-C has greater than 50% amino acid sequence identity to two zinc metalloproteases.
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