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

Abstract

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.

Regulatory cascade and biological activity of Beauveria bassiana oosporein that limits bacterial growth after host death

“…The discovery of antibiotics in Penicillium crysogenum is well known, and fungi-particularly those occupying unique ecological niches-continue to be a source for their discovery (31,32). Iron-binding siderophores, synthesized via nonribosomal peptide synthase-mediated pathways, are involved in iron scavenging, uptake, and sequestration, and have been shown to act as virulence factors in various pathogenic fungi (33). Some secondary metabolites act as "toxins," affecting/disrupting host tissues and processes; for example, the Cochliobolus carbonum HC toxin targets host histone deacetylases and is required for infection of maize cultivars that harbor the Hm resistance gene, but not of cultivars that lack Hm (34).…”

Necrotroph Attacks on Plants: Wanton Destruction or Covert Extortion?

“…Iron-chelating siderophores are also utilized by pathogens during infection (Haas et al, 2008). NPS6, encoding a non-ribosomal peptide synthetase involved in siderophore biosynthesis, is a functionally conserved virulence factor of different necrotrophic ascomycetes including A. brassicicola (Oide et al, 2006). Arabidopsis rbohDrbohF double mutants, disrupted in NADPH oxidase function, exhibit increased susceptibility to wildtype A. brassicicola infection but unaltered responses to a strain harboring a loss of function NPS6 allele (Oide et al, 2006).…”

Microbial Siderophores Exert a Subtle Role in Arabidopsis during Infection by Manipulating the Immune Response and the Iron Status

“…Phytopathogenic bacteria and fungi can use siderophores to multiply in the host and to promote infection (Expert, 1999;Haas et al, 2008). Oide et al (2006) demonstrated that in four ascomycete species, Cochliobolus miyabeanus, Cochliobolus heterostrophus, Fusarium graminareum, and Alternaria brassicicola, siderophores are required for resistance to hydrogen peroxide and for full pathogenicity on their respective hosts maize (Zea mays), rice (Oryza sativa), wheat (Triticum aestivum), and Arabidopsis. Likewise, the fire blight-causing agent Erwinia amylovora takes advantage of its siderophore deferrioxamine (DFO) for the infection of apple (Malus domestica) seedlings and flowers and for the resistance to hydrogen peroxide (Dellagi et al, 1998).…”