Production and regulation of potato-scab-inducing phytotoxins by Streptomyces scabies

Babcock, Martin J.; Eckwall, Eric C.; Schottel, Janet L.

doi:10.1099/00221287-139-7-1579

Cited by 66 publications

(49 citation statements)

References 20 publications

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“…If we assume the monooxygenase catalyzed a single initial post-cyclization hydroxylation, then the most likely monooxygenase target would be the L-phenylalanyl ␣-carbon atom based on the logic of natural thaxtomin congener profiles found in extracts (1). This is because the only monohydroxylated thaxtomins that have been isolated from extracts and characterized are hydroxylated on the phenylalanyl ␣-carbon (thaxtomin B and thaxtomin 6) (19); thaxtomins carrying single hydroxyl groups on the phenylalanyl ring have not been identified in extracts.…”

Section: Discussionmentioning

confidence: 99%

Involvement of a Cytochrome P450 Monooxygenase in Thaxtomin A Biosynthesis by Streptomyces acidiscabies

et al. 2002

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The biosynthesis of the thaxtomin cyclic dipeptide phytotoxins proceeds nonribosomally via the thiotemplate mechanism. Acyladenylation, thioesterification, N-methylation, and cyclization of two amino acid substrates are catalyzed by the txtAB-encoded thaxtomin synthetase. Nucleotide sequence analysis of the region 3 of txtAB in Streptomyces acidiscabies 84.104 identified an open reading frame (ORF) encoding a homolog of the P450 monooxygenase gene family. It was proposed that thaxtomin A phenylalanyl hydroxylation was catalyzed by the monooxygenase homolog. The ORF was mutated in S. acidiscabies 84.104 by using an integrative gene disruption construct, and culture filtrate extracts of the mutant were assayed for the presence of dehydroxy derivatives of thaxtomin A. Reversed-phase high-performance liquid chromatography (HPLC) and HPLC-mass spectrometry indicated that the major component in culture filtrate extracts of the mutant was less polar and smaller than thaxtomin A. Comparisons of electrospray mass spectra as well as 1 H-and 13 C-nuclear magnetic resonance spectra of the purified compound with those previously reported for thaxtomins confirmed the structure of the compound as 12,15-N-dimethylcyclo-(L-4-nitrotryptophyl-L-phenylalanyl), the didehydroxy analog of thaxtomin A. The ORF, designated txtC, was cloned and the recombinant six-His-tagged fusion protein produced in Escherichia coli and purified from cell extracts. TxtC produced in E. coli exhibited spectral properties similar to those of cytochrome P450-type hemoproteins that have undergone conversion to the catalytically inactive P420 form. Based on these properties and the high similarity of TxtC to other wellcharacterized P450 enzymes, we conclude that txtC encodes a cytochrome P450-type monooxygenase required for postcyclization hydroxylation of the cyclic dipeptide.

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Section: Discussionmentioning

confidence: 99%

Involvement of a Cytochrome P450 Monooxygenase in Thaxtomin A Biosynthesis by Streptomyces acidiscabies

et al. 2002

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“…Thaxtomins are unique 4-nitroindol-3-yl-containing 2,5-dioxopiperazines produced by at least three plant-pathogenic Streptomyces species (16,17,25). These toxins constitute a family of phytotoxic secondary metabolites that were originally purified from S. scabies-infected plant tissue (15,25) but are also produced in oatmeal-based media (1,26). Thaxtomin production is positively correlated with plant pathogenicity (17) and may be quantitatively related to virulence within S. scabies (26).…”

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confidence: 99%

Cloning and expression of a gene from Streptomyces scabies encoding a putative pathogenicity factor

Bukhalid

Loria

1997

J Bacteriol

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We cloned a 9.4-kb DNA fragment from Streptomyces scabies ATCC 41973 that allows the nonpathogen Streptomyces lividans 66 TK24 to necrotize and colonize potato tuber slices and produce scab-like symptoms on potato minitubers. Deletion analysis demonstrated that activity was conferred by a 1.6-kb DNA region. Sequence analysis of a 2.4-kb DNA fragment spanning the DNA region necessary for activity revealed three open reading frames (ORFs). The deduced amino acid sequence of ORF1, designated ORFtnp, showed high levels of identity with the first 233 amino acids of the putative transposases of the IS1164 elements from Rhodococcus rhodochrous (71%) and Mycobacterium bovis (68%), members of the Staphylococcus aureus IS256 family of transposases. No significant homologies to ORF2 and ORF3 were found in the nucleic acid and protein databases. ORFtnp is located 5 of ORF3. ORF2 is incomplete and is located 3 of ORF3. Subcloning of the individual ORFs demonstrated that ORF3, designated nec1, is sufficient for necrotizing activity in S. lividans 66 TK24. S. lividans 66 TK24 expressing nec1 does not produce thaxtomin A but produces an unidentified extracellular water-soluble compound that causes necrosis on potato tuber discs. The G؉C content of nec1 suggests that it has moved horizontally from another genus. Southern analysis of ORFtnp and nec1 demonstrate that these genes are physically linked in Streptomyces strains, including S. scabies and Streptomyces acidiscabies strains, that are pathogenic on potato and that produce the phytotoxin thaxtomin A. These data suggest that nec1 may have been mobilized into S. scabies through a transposition event mediated by ORFtnp.Streptomyces spp. are gram-positive filamentous bacteria. Almost all described species are soil saprophytes, and many produce biologically active secondary metabolites, including antibiotics. However, a few species are plant pathogenic. These species infect underground structures of many plant species. Streptomyces scabies (Thaxt.) Lambert and Loria (22) is the predominant and best-studied of the plant-pathogenic species and causes an economically important disease of potato tubers called potato scab (28,29). Streptomyces acidiscabies Lambert and Loria, although apparently limited in distribution, also causes disease on potato tubers (21). The symptoms caused by S. acidiscabies are indistinguishable from those caused by S. scabies, and both species infect tap roots of radish, turnip, and other crops (23). Streptomyces ipomoeae (Person and Martin) Waksman and Henrici (43) infects storage and fibrous roots of sweet potato (6). There is evidence that several other Streptomyces species may be able to cause disease on plants (reviewed in reference 27).Plant-pathogenic Streptomyces species are diverse, based on physiological, morphological, DNA-DNA hybridization, and ribosomal analyses (13,20,39). However, similarities in host range and disease symptomology for some of these species suggest a common mechanism of pathogenicity. Thaxtomins are unique 4-nitroindol-3-yl-c...

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“…Comparison of phytotoxin production in agar and liquid cultures with oatmeal, oat bran and potato peel media (Babcock et al 1993;Beauséjour et al 1999;Goyer et al 1998) showed that shake culture in potato peel broth provided high phytotoxin productivity and facilitated mass culture (Fig. S3), and this culture method was selected for further experiments.…”

Section: Isolation Of Phytotoxin Produced By S Turgidiscabies Strain 65mentioning

confidence: 99%

“…Phytotoxin production of S. turgidiscabies strains 65 and NBRC 16080 T The phytotoxicity of crude chloroform extracts of strain 65 and the type strain of S. turgidiscabies, NBRC 16080, cultured on oatmeal agar (Babcock et al 1993) was examined on rape seedlings. Extracts of both strains showed strong growth inhibitory activity at the dose corresponding to the amount of extract obtained from 10 mL of bacterial culture (Fig.…”

Section: Microarray Analysis Of Thaxtomin Biosynthetic Genes Of S Tumentioning

confidence: 99%

Phytotoxin produced by the netted scab pathogen, Streptomyces turgidiscabies strain 65, isolated in Sweden

et al. 2018

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Streptomyces spp. are a highly diverse group of bacteria most of which are soil-inhabiting saprophytes. A few are plant pathogens that produce a family of phytotoxins called thaxtomins and cause significant economic losses, e.g., by reducing the marketability of potato tubers (Solanum tuberosum). In northern Europe, S. scabies, S. turgidiscabies and S. europaeiscabiei are the most common plant pathogenic species. In this study, a Streptomyces strain isolated from a netted scab lesion on a tuber of potato cv. Bintje in northern Sweden was identified as S. turgidiscabies but was found to differ in the genomic region carrying genes required for thaxtomin biosynthesis. Our results showed that the strain did not produce thaxtomin but rather phytotoxin fridamycin E, which is an anthraquinone novel to plant pathogenic Streptomyces spp. Fridamycin E was shown to reduce or inhibit sprouting of potato microtubers in vitro. While fridamycin E is known to have antibiotic activity against Gram-positive bacteria, the inhibitory activity of fridamycin E on plant growth is a novel finding.

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Production and regulation of potato-scab-inducing phytotoxins by Streptomyces scabies

Cited by 66 publications

References 20 publications

Involvement of a Cytochrome P450 Monooxygenase in Thaxtomin A Biosynthesis by Streptomyces acidiscabies

Involvement of a Cytochrome P450 Monooxygenase in Thaxtomin A Biosynthesis by Streptomyces acidiscabies

Cloning and expression of a gene from Streptomyces scabies encoding a putative pathogenicity factor

Phytotoxin produced by the netted scab pathogen, Streptomyces turgidiscabies strain 65, isolated in Sweden

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