Siderophore accumulation and phytopathogenicity in Microbotryum violaceum

Birch, L.; Ruddat, Manfred

doi:10.1016/j.fgb.2004.11.001

Cited by 20 publications

(11 citation statements)

References 43 publications

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“…In this study, a mutant defective in L-ornithine N5-monooxygenase, the enzyme responsible for the first committed step of fungal siderophore biosynthesis, was as virulent to maize as the wild type, demonstrating that the siderophores by themselves do not play an essential role in the virulence of U. maydis. A recent report on another plant pathogenic basidiomycete, Microbotryum violaceum, also noted that rhodotorulic acid, the hydroxamate-type siderophore produced by this species, does not contribute to virulence on Silene latifolia (Birch and Ruddat, 2005). By contrast, this study demonstrates that the siderophores produced by the NRPS encoded by NPS6 play a role in virulence in at least four different species of plant pathogenic ascomycetes.…”

Section: Role Of Extracellular Siderophores In Fungal Virulence To Plcontrasting

confidence: 43%

NPS6, Encoding a Nonribosomal Peptide Synthetase Involved in Siderophore-Mediated Iron Metabolism, Is a Conserved Virulence Determinant of Plant Pathogenic Ascomycetes

et al. 2006

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NPS6, encoding a nonribosomal peptide synthetase, is a virulence determinant in the maize (Zea mays) pathogen Cochliobolus heterostrophus and is involved in tolerance to H2O2. Deletion of NPS6 orthologs in the rice (Oryza sativa) pathogen, Cochliobolus miyabeanus, the wheat (Triticum aestivum) pathogen, Fusarium graminearum, and the Arabidopsis thaliana pathogen, Alternaria brassicicola, resulted in reduced virulence and hypersensitivity to H2O2. Introduction of the NPS6 ortholog from the saprobe Neurospora crassa to the Δnps6 strain of C. heterostrophus restored wild-type virulence to maize and tolerance to H2O2, demonstrating functional conservation in filamentous ascomycete phytopathogens and saprobes. Increased sensitivity to iron depletion was identified as a conserved phenotype of Δnps6 strains. Exogenous application of iron enhanced the virulence of Δnps6 strains of C. heterostrophus, C. miyabeanus, F. graminearum, and A. brassicicola to each host. NPS6 is responsible for the biosynthesis of extracellular siderophores by C. heterostrophus, F. graminearum, and A. brassicicola. Application of the extracellular siderophore of A. brassicicola restored wild-type virulence of the ΔAbnps6 strain to Arabidopsis. It is proposed that the role of extracellular siderophores in fungal virulence to plants is to supply an essential nutrient, iron, to their producers in planta and not to act as phytotoxins, depriving their hosts of iron.

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Section: Role Of Extracellular Siderophores In Fungal Virulence To Plcontrasting

confidence: 43%

NPS6, Encoding a Nonribosomal Peptide Synthetase Involved in Siderophore-Mediated Iron Metabolism, Is a Conserved Virulence Determinant of Plant Pathogenic Ascomycetes

et al. 2006

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“…Moreover, the intracellular siderophore has also been implicated in the virulence of Mangaporthe grisae in rice [36]. Nevertheless, the role of individual iron homeostasis-maintaining mechanisms in virulence largely depends on the pathogen–host system because the siderophores produced by the phytopathogenic basidiomycetes Ustilago maydis and Microbotryum violaceum do not contribute to their virulence [37,38], and because there are siderophore-lacking animal pathogenic ascomycetes, for example, C. albicans, and basidiomycetes, for example, C. neoformans. In C.…”

Section: Discussionmentioning

confidence: 99%

Distinct Roles for Intra- and Extracellular Siderophores during Aspergillus fumigatus Infection

et al. 2007

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Siderophore biosynthesis by the highly lethal mould Aspergillus fumigatus is essential for virulence, but non-existent in humans, presenting a rare opportunity to strategize therapeutically against this pathogen. We have previously demonstrated that A. fumigatus excretes fusarinine C and triacetylfusarinine C to capture extracellular iron, and uses ferricrocin for hyphal iron storage. Here, we delineate pathways of intra- and extracellular siderophore biosynthesis and show that A. fumigatus synthesizes a developmentally regulated fourth siderophore, termed hydroxyferricrocin, employed for conidial iron storage. By inactivation of the nonribosomal peptide synthetase SidC, we demonstrate that the intracellular siderophores are required for germ tube formation, asexual sporulation, resistance to oxidative stress, catalase A activity, and virulence. Restoration of the conidial hydroxyferricrocin content partially rescues the virulence of the apathogenic siderophore null mutant ΔsidA, demonstrating an important role for the conidial siderophore during initiation of infection. Abrogation of extracellular siderophore biosynthesis following inactivation of the acyl transferase SidF or the nonribosomal peptide synthetase SidD leads to complete dependence upon reductive iron assimilation for growth under iron-limiting conditions, partial sensitivity to oxidative stress, and significantly reduced virulence, despite normal germ tube formation. Our findings reveal distinct cellular and disease-related roles for intra- and extracellular siderophores during mammalian Aspergillus infection.

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“…By contrast, in the biotrophic plant pathogenic smut fungi Microbotryum violaceum , infecting white campion ( Silene latifolia ), and Ustilago maydis , infecting maize ( Zea mays ), reductive iron assimilation, but not siderophore-mediated iron uptake, is required for full virulence (Mei et al ., 1993 ; Birch and Ruddat, 2005 ). Supporting the idea that reductive iron assimilation is required for virulence of biotrophs, Albarouki and Deising ( 2013 ) have shown that the ferroxidase gene FET3-1 of the hemibiotroph Colletotrichum graminicola is specifically expressed in and required for development of biotrophic hyphae, and that this gene is a determinant of virulence.…”

Section: Introductionmentioning

confidence: 99%

Biotrophy‐specific downregulation of siderophore biosynthesis in Colletotrichum graminicola is required for modulation of immune responses of maize

Albarouki

Schafferer

et al. 2014

Molecular Microbiology

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The hemibiotrophic maize pathogen C olletotrichum graminicola synthesizes one intracellular and three secreted siderophores. eGFP fusions with the key siderophore biosynthesis gene, SID1, encoding l-ornithine-N 5-monooxygenase, suggested that siderophore biosynthesis is rigorously downregulated specifically during biotrophic development. In order to investigate the role of siderophores during vegetative development and pathogenesis, SID1, which is required for synthesis of all siderophores, and the non-ribosomal peptide synthetase gene NPS6, synthesizing secreted siderophores, were deleted. Mutant analyses revealed that siderophores are required for vegetative growth under iron-limiting conditions, conidiation, ROS tolerance, and cell wall integrity. Δsid1 and Δnps6 mutants were hampered in formation of melanized appressoria and impaired in virulence. In agreement with biotrophy-specific downregulation of siderophore biosynthesis, Δsid1 and Δnps6 strains were not affected in biotrophic development, but spread of necrotrophic hyphae was reduced. To address the question why siderophore biosynthesis is specifically downregulated in biotrophic hyphae, maize leaves were infiltrated with siderophores. Siderophore infiltration alone did not induce defence responses, but formation of biotrophic hyphae in siderophore-infiltrated leaves caused dramatically increased ROS formation and transcriptional activation of genes encoding defence-related peroxidases and PR proteins. These data suggest that fungal siderophores modulate the plant immune system.

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Siderophore accumulation and phytopathogenicity in Microbotryum violaceum

Cited by 20 publications

References 43 publications

NPS6, Encoding a Nonribosomal Peptide Synthetase Involved in Siderophore-Mediated Iron Metabolism, Is a Conserved Virulence Determinant of Plant Pathogenic Ascomycetes

NPS6, Encoding a Nonribosomal Peptide Synthetase Involved in Siderophore-Mediated Iron Metabolism, Is a Conserved Virulence Determinant of Plant Pathogenic Ascomycetes

Distinct Roles for Intra- and Extracellular Siderophores during Aspergillus fumigatus Infection

Biotrophy‐specific downregulation of siderophore biosynthesis in Colletotrichum graminicola is required for modulation of immune responses of maize

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