The brominated aryl-polyene (xanthomonadin) pigments ofXanthomonas juglandis protect against photobiological damage

Jenkins, Christie L.; Starr, Mortimer P.

doi:10.1007/bf01566872

Cited by 41 publications

(26 citation statements)

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“…However, these results do not preclude the possibility that xanthomonadins may protect against indirect UV damage, mediated by an unknown photosensitizing agent on the leaf surface. Previous studies have indicated that xanthomonadins may protect against visible light damage in the presence of photosensitizers (11,18). In the first study, a single, chemically induced mutant strain of X. juglandis was more sensitive than its parent strain to photosensitizer-mediated photobiological damage.…”

Section: Discussionmentioning

confidence: 99%

“…DF extracellularly restored all of these traits to a pigB mutant strain (4, 15, 16), indicating that DF is needed for xanthomonadin and EPS production, as well as for epiphytic survival and host infection. These results suggest that DF acts as a signal for the initiation of xanthomonadin and EPS production and that xanthomonadins and EPS may play a role in host infection and/or epiphytic survival.The results of other studies suggest an association of xanthomonadins with protection against photobiological damage (11,18). However, these studies were not conducted using modern methods of single gene mutation and chromosomal restoration, from which definitive conclusions can be drawn.…”

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confidence: 99%

“…The results of other studies suggest an association of xanthomonadins with protection against photobiological damage (11,18). However, these studies were not conducted using modern methods of single gene mutation and chromosomal restoration, from which definitive conclusions can be drawn.…”

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confidence: 99%

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Biological Role of Xanthomonadin Pigments in Xanthomonas campestris pv. Campestris

Poplawsky

Urban

Chun

2000

Appl Environ Microbiol

100

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Previous studies have indicated that the yellow pigments (xanthomonadins) produced by phytopathogenicXanthomonas bacteria are unimportant during pathogenesis but may be important for protection against photobiological damage. We used a Xanthomonas campestris pv. campestris parent strain, single-site transposon insertion mutant strains, and chromosomally restored mutant strains to define the biological role of xanthomonadins. Although xanthomonadin mutant strains were comparable to the parent strain for survival when exposed to UV light; after their exposure to the photosensitizer toluidine blue and visible light, survival was greatly reduced. Chromosomally restored mutant strains were completely restored for survival in these conditions. Likewise, epiphytic survival of a xanthomonadin mutant strain was greatly reduced in conditions of high light intensity, whereas a chromosomally restored mutant strain was comparable to the parent strain for epiphytic survival. These results are discussed with respect to previous results, and a model for epiphytic survival of X. campestris pv. campestris is presented.Xanthomonas bacteria are the causal agents of disease on at least 124 monocot and 268 dicot plant hosts (12), and many of them can survive and multiply as epiphytes (8,24). Most Xanthomonas bacteria produce yellow, membrane-bound, brominated aryl-polyene pigments referred to as xanthomonadins (24). Xanthomonadins are unique to Xanthomonas bacteria and serve as useful chemotaxonomic (2, 25) and diagnostic (22) markers. With methods of artificial infection, xanthomonadin-deficient strains were not affected in pathogenicity, symptomatology, or in planta growth (15). Thus, the xanthomonadins apparently are not important to the pathogen after infection of the host plant.Xanthomonas campestris pv. campestris, the causal agent of black rot of crucifers and one of the most serious disease problems in crucifer production, naturally infects its host via hydathodes or wounds in the leaves (28). A cluster of seven transcriptional units required for xanthomonadin production (pigA to pigG) was previously identified in X. campestris pv. campestris (13,15). In addition to a loss of xanthomonadin production, pigB mutant strains were also greatly impaired in the production of extracellular polysaccharide (EPS) and a pheromone (DF). Mutations in the other pig transcriptional units did not appear to have pleiotropic affects. When tested on the host plant, pigB mutants were significantly reduced in epiphytic survival and natural host infection via hydathodes (16). DF extracellularly restored all of these traits to a pigB mutant strain (4, 15, 16), indicating that DF is needed for xanthomonadin and EPS production, as well as for epiphytic survival and host infection. These results suggest that DF acts as a signal for the initiation of xanthomonadin and EPS production and that xanthomonadins and EPS may play a role in host infection and/or epiphytic survival.The results of other studies suggest an association of xanthomonadins with protec...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Biological Role of Xanthomonadin Pigments in Xanthomonas campestris pv. Campestris

Poplawsky

Urban

Chun

2000

Appl Environ Microbiol

100

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“…However, it is being established progressively that xanthomonadin protects bacteria against photooxidative damage. Pigment-deficient mutants of Xanthomonas juglandis (20), Xanthomonas oryzae pv. oryzae (37), and Xanthomonas campestris pv.…”

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Genetic Locus Encoding Functions Involved in Biosynthesis and Outer Membrane Localization of Xanthomonadin in Xanthomonas oryzae pv. oryzae

et al. 2002

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Xanthomonadins are membrane-bound, brominated, aryl-polyene pigments specific to the genus Xanthomonas. We have characterized a genetic locus (pig) from Xanthomonas oryzae pv. oryzae which contains four open reading frames (ORFs) that are essential for xanthomonadin production. Three of these ORFs are homologous to acyl carrier proteins, dehydratases, and acyl transferases, suggesting a type II polyketide synthase pathway for xanthomonadin biosynthesis. The fourth ORF has no homologue in the database. For the first time, we report that a putative cytoplasmic membrane protein encoded in the pig locus is required for outer membrane localization of xanthomonadin in X. oryzae pv. oryzae. We also report the identification of a novel 145-bp palindromic Xanthomonas repetitive intergenic consensus element that is present in two places in the pig locus. We estimate that more than 100 copies of this element might be present in the genome of X. oryzae pv. oryzae and other xanthomonads.Members of the genus Xanthomonas cause diseases in a wide range of host plants (25). Many of them can also survive and multiply on plant leaf surfaces as epiphytes without affecting the host (15,44). A characteristic feature of most xanthomonads is the production of yellow, membrane-bound (46), halogenated, aryl-polyene pigments (2, 3) called xanthomonadins, which serve as useful chemotaxonomic (45) and diagnostic markers (41). Xanthomonadin is not essential for in planta growth of bacterial cells (13,35,48). However, it is being established progressively that xanthomonadin protects bacteria against photooxidative damage. Pigment-deficient mutants of Xanthomonas juglandis (20), Xanthomonas oryzae pv. oryzae (37), and Xanthomonas campestris pv. campestris (33) are more susceptible to photooxidative damage than are wild-type strains. In vitro, xanthomonadin protects membrane lipids in egg-phosphatidylcholine liposomes against peroxidation (37). A transposon-induced xanthomonadin-deficient mutant of X. campestris pv. campestris has been recently shown to be 1,000-fold reduced for epiphytic survival in conditions of high light intensity (33). These observations suggest that xanthomonadin might aid the survival of xanthomonads on plant leaf surfaces by providing protection against photooxidative damage. In spite of their apparent importance, very little is known about the biosynthesis and mechanism of action of xanthomonadins.An 18.6-kb genomic region from X. campestris pv. campestris that contains seven transcriptional units (pig genes) required for xanthomonadin production has been isolated (34, 35). One of the transcriptional units, pigB, is involved in biosynthesis of a diffusible factor that affects the production of xanthomonadin as well as extracellular polysaccharide (34). The unavailability of nucleotide sequences for these transcriptional units, however, limits further insight into the mechanism of xanthomonadin biosynthesis. X. oryzae pv. oryzae mutants that are defective in shikimate dehydrogenase activity have been shown to be deficie...

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“…Thus, these pigments are commonly used as chemotaxonomic (2,36) and diagnostic (32) markers. Although the biological role of xanthomonadins is not well understood, a correlation between these pigments and protection against photobiological damage has been observed (14). A correlation between EPS production and virulence has been widely reported for Xanthomonas campestris (7,9,33,38,39).…”

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confidence: 99%

pigB determines a diffusible factor needed for extracellular polysaccharide slime and xanthomonadin production in Xanthomonas campestris pv. campestris

Poplawsky

Chun

1997

J Bacteriol

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Seven xanthomonadin transcriptional units (pigA through pigG) were identified by transposon saturation mutagenesis within an 18.6-kbp portion of the previously identified 25.4-kbp pig region from Xanthomonas campestris pv. campestris (strain B-24). Since marker exchange mutant strains with insertions in one 3.7-kbp portion of pig could not be obtained, mutations in this region may be lethal to the bacterium. Complementation analyses with different insertion mutations further defined and confirmed the seven transcriptional units. Insertional inactivation of one of the transcriptional units, pigB, resulted in greatly reduced levels of both xanthomonadins and extracellular polysaccharide slime, and a pigB-encoding plasmid restored both traits to these strains. pigB mutant strains could also be restored extracellularly by growth adjacent to strains with insertion mutations in any of the other six xanthomonadin transcriptional units, the parent strain (B-24), or strains of five different species of Xanthomonas. Strain B-24 produced a nontransforming diffusible factor (DF), which could be restored to pigB mutants by the pigB-encoding plasmid. Several lines of evidence indicate that DF is a novel bacterial pheromone, different from the known signal molecules of Vibrio, Agrobacterium, Erwinia, Pseudomonas, and Burkholderia spp.Members of the genus Xanthomonas are distributed worldwide and are the causal agents for disease for at least 124 monocot and 268 dicot plant hosts (20). Many of the phytopathogenic xanthomonads are disseminated on seed (22), and at least some of these pathogens survive and multiply as epiphytes prior to plant infection (13,35). Two common traits of Xanthomonas spp. are the production of yellow pigments (xanthomonadins) and extracellular polysaccharide slime (EPS) (32). The xanthomonadins are yellow, membrane-bound, brominated aryl-polyene pigments unique to the genus Xanthomonas (35). Thus, these pigments are commonly used as chemotaxonomic (2, 36) and diagnostic (32) markers. Although the biological role of xanthomonadins is not well understood, a correlation between these pigments and protection against photobiological damage has been observed (14). A correlation between EPS production and virulence has been widely reported for Xanthomonas campestris (7,9,33,38,39).In a previous study with X. campestris pv. campestris (causal agent of black rot of crucifers), six functional domains for xanthomonadin production were identified within a 25-kbp genomic clone (pIG102) (25). Sequences from this region (pig) restored pigment production to all 19 induced and naturally occurring xanthomonadin mutants tested (25). Clone pIG102 also conferred xanthomonadin production on a strain of Pseudomonas. Thus, it was concluded that at least some of these functional domains must be structural genes. The original purpose of this work was to perform a transcriptional analysis of pig by using transcriptional lacZ fusions created with the transposon Tn3HoHo1. In the course of this study, we made two unexpected observat...

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The brominated aryl-polyene (xanthomonadin) pigments ofXanthomonas juglandis protect against photobiological damage

Cited by 41 publications

References 12 publications

Biological Role of Xanthomonadin Pigments in Xanthomonas campestris pv. Campestris

Biological Role of Xanthomonadin Pigments in Xanthomonas campestris pv. Campestris

Genetic Locus Encoding Functions Involved in Biosynthesis and Outer Membrane Localization of Xanthomonadin in Xanthomonas oryzae pv. oryzae

pigB determines a diffusible factor needed for extracellular polysaccharide slime and xanthomonadin production in Xanthomonas campestris pv. campestris

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