Diversity of Neofusicoccum parvum for the Production of the Phytotoxic Metabolites (-)-Terremutin and (R)-Mellein

Abstract

Two Neofusicoccumparvum isolates and a UV mutant were characterized for their phytotoxin production in vitro, their pathogenicity on grapevine, and their genome sequenced. The isolate Np-Bt67 produced high level of (-)-terremutin, but almost no (R)-mellein, and it was the most aggressive on grapevine, triggering apoplexy. Similar symptoms were not induced by purified (-)-terremutin. The isolate Bourgogne S-116 (Np-B) produced 3-fold less (-)-terremutin and high amounts of (R)-mellein, but it was less aggressive on grapevine than Np-Bt67. The UV9 mutant obtained from Np-B (NpB-UV9) no longer produced (-)-terremutin but overproduced (R)-mellein by 2.5-fold, and it was as pathogenic as its parent. NpB-UV9 differed from its parent by simple mutations in two genes (transcription factor UCR-NP2_6692, regulatory protein UCR-NP2_9007), not located neither near (R)-mellein, nor (-)-terremutin biosynthetic genes, but likely involved in the control of (-)-terremutin biosynthesis. Grapevine immunity was disturbed upon challenge with these pathogens or purified phytotoxins, leading to an upregulation of SA-dependent defenses, while (-)-terremutin interfered with host JA/ET-dependent defenses. Our results suggest that neither (-)-terremutin nor (R)-mellein alone is essential for the pathogenicity of N. parvum on grapevine, since isolate/mutant non-producing these toxins in vitro is pathogenic. However, these phytotoxins could play a quantitative role in the infection process.

Sodium arsenite-induced changes in the wood of esca-diseased grapevine at cytological and metabolomic levels

“…Six other toxins were rather more detected in the wood of apoplectic vines such as OH-tyrosol 1-O-glucoside, cis-4hydroxy-scytalone, dimethylallyl-scopoletin, terremutin, tyrosol-4sulfate, and mellein. Mellein and terremutin are especially produced by Botryosphaeriaceae species such as Neofusicoccum parvum, Diplodia seriata, or Lasiodiplodia (Andolfi et al, 2011;Abou-Mansour et al, 2015;Cimmino et al, 2017;Reveglia et al, 2019;Reveglia et al, 2021;Trotel-Aziz et al, 2022), and their detection in woody tissues was first reported by Abou-Mansour et al (2015) in the brown-striped wood of Botryosphaeria dieback-diseased vines. Our results, therefore, are consistent with those of Bruez et al (2021), who reported that these esca-expressing vines were colonized by Botryosphaeriaceae species.…”

Pathogenicity Factors of Botryosphaeriaceae Associated with Grapevine Trunk Diseases: New Developments on Their Action on Grapevine Defense Responses

“…These mutants remained pathogenic on grapevine, showing that these two metabolites alone are not essential for fungal virulence. However, they could play a quantitative role in the infection process [93]. Apart from secondary metabolites, SSPs may also be involved in the induction of wood necrosis and foliar symptoms of GTD, as discussed in the above paragraph.…”

Phytotoxic Metabolites Produced by Fungi Involved in Grapevine Trunk Diseases: Progress, Challenges, and Opportunities

“…Two N. parvum isolates and a UV mutant were studied for their phytotoxin production in vitro, their pathogenicity on the grapevine, and their genome sequence [ 129 ]. Essentially ( R )-mellein and (-)-terremutin were the main phytotoxins produced by the selected isolates.…”

“…Alternatively, ( R )-mellein and (-)-terremutin could act as a virulence factor (i.e., quantitatively increasing the disease) than as a pathogenicity factor (i.e., required to trigger the disease). To confirm this hypothesis for ( R )-mellein, mutants unable to produce PMs should be created, and their pathogenicity should be compared with their wild-type parent [ 129 ].…”