FcStuA from Fusarium culmorum Controls Wheat Foot and Root Rot in a Toxin Dispensable Manner

Abstract

Fusarium culmorum is one of the most harmful pathogens of durum wheat and is the causal agent of foot and root rot (FRR) disease. F. culmorum produces the mycotoxin deoxynivalenol (DON) that is involved in the pathogenic process. The role of the gene FcStuA, a StuA ortholog protein with an APSES domain sharing 98.5% homology to the FgStuA protein (FGSG10129), was determined by functional characterisation of deletion mutants obtained from two F. culmorum wild-type strains, FcUk99 (a highly pathogenic DON producer) and Fc233B (unable to produce toxin and with a mild pathogenic behavior). The ΔFcStuA mutants originating from both strains showed common phenotypic characters including stunted vegetative growth, loss of hydrophobicity of the mycelium, altered pigmentation, decreased activity of polygalacturonic enzymes and catalases, altered and reduced conidiation, delayed conidial germination patterns and complete loss of pathogenicity towards wheat stem base/root tissue. Glycolytic process efficiency [measured as growth on glucose as sole carbon (C) source] was strongly impaired and growth was partially restored on glutamic acid. Growth on pectin-like sources ranked in between glucose and glutamic acid with the following order (the lowest to the highest growth): beechwood xylan, sugarbeet arabinan, polygalacturonic acid, citrus pectin, apple pectin, potato azogalactan. DON production in the mutants originating from FcUK99 strain was significantly decreased (−95%) in vitro. Moreover, both sets of mutants were unable to colonise non-cereal plant tissues, i.e. apple and tomato fruits and potato tubers. No differences between mutants, ectopic and wild-type strains were observed concerning the level of resistance towards four fungicides belonging to three classes, the demethylase inhibitors epoxiconazole and tebuconzole, the succinate dehydrogenase inhibitor isopyrazam and the cytochrome bc1 inhibitor trifloxystrobin. StuA, given its multiple functions in cell regulation and pathogenicity control, is proposed as a potential target for novel disease management strategies.

The APSES transcription factor LmStuA is required for sporulation, pathogenic development and effector gene expression in Leptosphaeria maculans

“…Accordingly, the silencing of LmStuA triggered multiple defects in L. maculans. Silenced LmStuA mycelia showed morphological defects consistent with the defects usually associated with StuA mutations or deletions, as in F. oxysporum, A. nidulans, F. graminearum and F. culmorum, with less aerial mycelium and stunted colonies (Lysøe et al, 2011;Ohara and Tsuge, 2004;Pasquali et al, 2013).…”

“…Its involvement in pathogenicity has also been investigated. In Fusarium oxysporum , deletion of FoStuA has a major effect on sporulation processes, but does not result in decreased virulence (Ohara and Tsuge, ), whereas, in Fusarium graminearum , deletion of FgStuA greatly reduces pathogenicity on wheat heads and the expression of secondary metabolites (Lysøe et al ., ), and, in Fusarium culmorum , deletion of FcStuA leads to a complete loss of pathogenicity towards wheat stem base and root tissues (Pasquali et al ., ). In Glomerella cingulata , StuA is required for the generation of appressorial turgor pressure and full pathogenicity on intact apple fruit (Tong et al ., ).…”

“…Accordingly, the silencing of LmStuA triggered multiple defects in L. maculans . Silenced LmStuA mycelia showed morphological defects consistent with the defects usually associated with StuA mutations or deletions, as in F. oxysporum , A. nidulans , F. graminearum and F. culmorum , with less aerial mycelium and stunted colonies (Lysøe et al ., ; Ohara and Tsuge, ; Pasquali et al ., ). Since the observation of Clutterbuck (), showing that StuA mutants of A. nidulans are altered in conidiophore development, conidia production has also systematically been shown to be reduced in all fungi in which this gene has been mutated.…”

“…The symptoms did not evolve with time to cause disease on the leaves. This phenotype is consistent with that which has been described in other phytopathogens, such as G. cingulata , U. maydis , M. oryzae , S. nodorum , F. graminearum and F. culmorum (García‐Pedrajas et al ., ; IpCho et al ., ; Lysøe et al ., ; Nishimura et al ., ; Pasquali et al ., ; Tong et al ., ), whereas StuA is considered to be dispensable for pathogenicity in F. oxysporum (Ohara and Tsuge, ). Thus, except for StuA of F. oxysporum , the importance of StuA in pathogenicity seems to be conserved among phytopathogenic fungi, whatever their pathogenic behaviour, including dimorphic transition ( U. maydis ) or the requirement for appressoria to penetrate host leaves (i.e.…”

Fusarium species and chemotypes associated with fusarium head blight and fusarium root rot on wheat in Sardinia

“…The two disease types, despite sharing large weapon sets for infection (Mudge et al, 2006), do adopt at least partly different mechanisms for their establishment (Desmond et al, 2008;Pasquali et al, 2013).…”