Phosphopantetheinyl transferase (Ppt)-mediated biosynthesis of lysine, but not siderophores or DHN melanin, is required for virulence of Zymoseptoria tritici on wheat

Abstract

Zymoseptoria tritici is the causal agent of Septoria tritici blotch (STB) disease of wheat. Z. tritici is an apoplastic fungal pathogen, which does not penetrate plant cells at any stage of infection, and has a long initial period of symptomless leaf colonisation. During this phase it is unclear to what extent the fungus can access host plant nutrients or communicate with plant cells. Several important primary and secondary metabolite pathways in fungi are regulated by the post-translational activator phosphopantetheinyl transferase (Ppt) which provides an essential co-factor for lysine biosynthesis and the activities of non-ribosomal peptide synthases (NRPS) and polyketide synthases (PKS). To investigate the relative importance of lysine biosynthesis, NRPS-based siderophore production and PKS-based DHN melanin biosynthesis, we generated deletion mutants of ZtPpt. The ∆ZtPpt strains were auxotrophic for lysine and iron, non-melanised and non-pathogenic on wheat. Deletion of the three target genes likely affected by ZtPpt loss of function (Aar- lysine; Nrps1-siderophore and Pks1- melanin), highlighted that lysine auxotrophy was the main contributing factor for loss of virulence, with no reduction caused by loss of siderophore production or melanisation. This reveals Ppt, and the lysine biosynthesis pathway, as potential targets for fungicides effective against Z. tritici.

Precision Phenotyping Reveals Novel Loci for Quantitative Resistance to Septoria Tritici Blotch

“…Segment 24, which explained 8% of the variance in pycnidia melanization and lies within the QTL9 region identified in earlier mapping studies, contained a single gene encoding a protein involved in lysine biosynthesis. Recent work on the wheat pathogen Cochliobolus sativus showed that lysine was essential for melanin biosynthesis [ 45 ] and lysine was recently shown to be essential for virulence in Z. tritici [ 46 ]. We conclude from this analysis that many of the genes found in the intervals identified in the GWAS are plausible candidates to explain the observed phenotypes associated with STB resistance, but functional validation studies will be needed to confirm whether any of these genes actually play a role in resistance.…”

Population-level transposable element expression dynamics influence trait evolution in a fungal crop pathogen

“…The specific biological roles of the different metabolites are poorly understood with few exceptions (Hassani et al, 2022; Singh et al, 2022b). However, individual metabolites can play major roles in species interactions with competitors or hosts (Derbyshire et al, 2018; Krishnan et al, 2018). Similarly, TE insertions in crop plants are associated with a wide range of agronomic traits and secondary metabolites such as in tomatoes (Domínguez et al, 2020).…”

Differential Regulation and Production of Secondary Metabolites among Isolates of the Fungal Wheat Pathogen Zymoseptoria tritici

“…Melanin is encoded by broadly diverse fungal species and has been shown to have a critical role in fungal survival under stress conditions (see, e.g., a review in reference 55 ) and play, broadly, a role in fungal pathogenicity ( 34 ). However, melanin-deficient strains of Z. tritici were not altered in their virulence or host colonization under test conditions ( 56 ), suggesting that melanin in Z. tritici plays other critical roles that require further testing.…”