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

Abstract

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.

The arbuscular mycorrhizal fungus Rhizophagus irregularis uses a reductive iron assimilation pathway for high‐affinity iron uptake

“…RiFTR s' gene expression patterns suggest that maintenance of Fe homeostasis in the IRM might be essential for root colonization and for the development of a successful symbiosis. In this respect, high‐affinity Fe uptake systems have been shown to be required for the colonization and virulence of several phytopathogenic fungi (Eichhorn et al ., ; Oide et al ., ; Albarouki et al ., ) and for the maintenance of mutualism in the Epichloë festucae /perennial ryegrass interaction (Johnson et al ., ). The finding that NP6, a virulent gene conserved in many filamentous fungi, is involved both in the biosynthesis of siderophores and in tolerance to H 2 O 2 has led to propose that the pathogen requirement to sequestrate Fe via siderophore production is not only to take up Fe but also to protect from reactive oxygen species (Oide et al ., ; Hwang et al ., ).…”

Intracellular siderophore but not extracellular siderophore is required for full virulence in Metarhizium robertsii

“…Infection of mouse macrophages with A. fumigatus wild type, but not with a ΔsidA strain which produces neither extracellular nor intracellular siderophores, induced the expression of TNFα, a cytokine essential for host defense (Roilides et al, 1998;Seifert et al, 2008). Siderophore-mediated pathogen recognition also occurs in plants as Colletotrichum graminicola, the causal agent of anthracnose stalk rot and leaf blight of maize, shuts down SIA during biotrophic growth to avoid detection and redeploys SIA during necrotrophic growth (Albarouki and Deising, 2013;Albarouki et al, 2014). Metachelin A is unique among fungi because it is O-mannosylated, a modification closely resembling the C-glycosylation of salmochelin which is deployed by some animal-pathogenic bacteria to evade siderocalin sequestration (Abergel et al, 2006;Muller et al, 2009).…”

“…In the plant pathogens Cochliobolus heterostrophus, Gibberella zeae and Alternaria alternata, SIA and not RIA is essential for full virulence (Chen et al, 2013;Condon et al, 2014;Oide et al, 2006;Park et al, 2006;Schrettl et al, 2004). In Colletotrichum graminicola, SIA and RIA have complementary roles: RIA is deployed during the biotrophic phase, when extracellular siderophore production is downregulated to avoid host detection; SIA is then used to support necrotrophic growth (Albarouki and Deising, 2013;Albarouki et al, 2014). In Ustilago maydis, SIA is dispensable for virulence whereas RIA impairment strongly affects growth and sporulation in planta.…”

Down‐regulation of cladofulvin biosynthesis is required for biotrophic growth of Cladosporium fulvum on tomato

“…Similarly, many C. fulvum genes encoding predicted functional cell wall‐degrading enzymes and carbohydrate‐active enzymes are weakly expressed or silent during biotrophic growth (de Wit et al ., ). Consistent with our hypothesis, siderophore biosynthesis in the hemibiotrophic maize pathogen Colletotrichum graminicola is specifically down‐regulated during biotrophic growth, which prevents the activation of host immune responses (Albarouki et al ., ).…”