Snow mold is a severe plant disease caused by psychrophilic or psychrotolerant fungi, of which Microdochium species are the most harmful. A clear understanding of Microdochium biology has many gaps; the pathocomplex and its dynamic are poorly characterized, virulence factors are unknown, genome sequences are not available, and the criteria of plant snow mold resistance are not elucidated. Our study aimed to identify comprehensive characteristics of a local community of snow mold-causing Microdochium species colonizing a particular crop culture. By using the next-generation sequencing (NGS) technique, we characterized fungal and bacterial communities of pink snow mold-affected winter rye (Secale cereale) plants within a given geographical location shortly after snowmelt. Twenty-one strains of M. nivale were isolated, classified on the basis of internal transcribed spacer 2 (ITS2) region, and characterized by morphology, synthesis of extracellular enzymes, and virulence. Several types of extracellular enzymatic activities, the level of which had no correlations with the degree of virulence, were revealed for Microdochium species for the first time. Our study shows that genetically and phenotypically diverse M. nivale strains simultaneously colonize winter rye plants within a common area, and each strain is likely to utilize its own, unique strategy to cause the disease using “a personal” pattern of extracellular enzymes.

Microdochium nivale is a progressive and devastating phytopathogen that causes different types of cereal crop and grass diseases that are poorly characterized at the molecular level. Although rye (Secale cereale L.) is one of the most resistant crops to most of the phytopathogens, it is severely damaged by M. nivale. The recent high-quality chromosome-scale assembly of rye genome has improved whole-genome studies of this crop. In the present work, the first transcriptome study of the M. nivale-infected crop plant (rye) with the detailed functional gene classification was carried out, along with the physiological verification of the RNA-Seq data. The results revealed plant reactions that contributed to their resistance or susceptibility to M. nivale. Phytohormone abscisic acid was shown to promote plant tolerance to M. nivale. Flavonoids were proposed to contribute to plant resistance to this pathogen. The upregulation of plant lipase encoding genes and the induction of lipase activity in M. nivale-infected plants revealed in our study were presumed to play an important role in plant susceptibility to the studied phytopathogen. Our work disclosed important aspects of plant-M. nivale interactions, outlined the directions for future studies on poorly characterized plant diseases caused by this phytopathogen, and provided new opportunities to improve cereals breeding and food security strategies.

To cause plant diseases, phytopathogenic fungi use numerous extracellular enzymes, among which, the phenoloxidases (POs) seem underestimated for the pathogens of non-woody plants. Our study aimed to (1) compare extracellular PO activities (lignin peroxidase, Mn peroxidase, laccase, and tyrosinase) in differentially virulent strains (inhabiting winter rye in a single field) of the phytopathogenic species, Microdochium nivale; (2) check whether these activities are responsive to host plant metabolites; and (3) search for correlations between the activities, lignin-decomposing capacity, and virulence. All strains displayed all four enzymatic activities, but their levels and dynamics depended on the particular strain. The activities displayed the hallmarks of co-regulation and responsiveness to the host plant extract. No relationships between the virulence of strains and levels of their extracellular PO activities or lignin-degrading capacity were revealed. We consider that different strains may rely on different POs for plant colonization, and that different POs contribute to the “uniqueness” of the enzymatic cocktails that are delivered into host plant tissues by different virulent strains of M. nivale. Our study supports the hypothesis of the differential behavior of closely related M. nivale strains, and discusses an important role of POs in the interactions of phytopathogens with herbaceous plants.