Analysis of Two in Planta Expressed LysM Effector Homologs from the Fungus Mycosphaerella graminicola Reveals Novel Functional Properties and Varying Contributions to Virulence on Wheat

• Published in: Plant physiology (Bethesda) 2011-06, Vol.156 (2), p.756-769
• Main Authors: Marshall, Rosalind, Kombrink, Anja, Motteram, Juliet, Loza-Reyes, Elisa, Lucas, John, Hammond-Kosack, Kim E., Thomma, Bart P.H.J., Rudd, Jason J.
• Format: Article
• Language: English
• Subjects: Alleles; Amino Acid Sequence; Ascomycota - genetics; Ascomycota - growth & development; Ascomycota - isolation & purification; Ascomycota - pathogenicity; Biological and medical sciences; blotch pathogen; Chitin; Chitin - metabolism; Cladosporium fulvum; Fundamental and applied biological sciences. Psychology; Fungal plant pathogens; Fungal Proteins - chemistry; Fungal Proteins - genetics; Fungal Proteins - metabolism; Fungi; Gene Expression Regulation, Fungal; Gene Expression Regulation, Plant; Genes; Genes, Fungal - genetics; host; Hydrolysis; Hyphae - physiology; Infections; innate immunity; Leaves; Lycopersicon esculentum; maximum-likelihood; Molecular Sequence Data; Mutation - genetics; Mycosphaerella graminicola; Pathogens; Phytopathology. Animal pests. Plant and forest protection; Plant Diseases - genetics; Plant Diseases - microbiology; Plant Immunity - genetics; Plant Leaves - microbiology; Plant physiology and development; Plants; PLANTS INTERACTING WITH OTHER ORGANISMS; protein; Protein Binding; Protein Structure, Tertiary; Proteins; recognition; resistance; Septoria tritici; Sequence Homology, Amino Acid; Solanum; tomato; Transcription, Genetic; Triticum - enzymology; Triticum - genetics; Triticum - microbiology; Triticum aestivum; Up-Regulation - genetics; Virulence; Virulence - genetics; Wheat
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1104/pp.111.176347

Secreted effector proteins enable plant pathogenic fungi to manipulate host defenses for successful infection. Mycosphaerella graminicola causes Septoria tritici blotch disease of wheat (Triticum aestivum) leaves. Leaf infection involves a long (approximately 7 d) period of symptomless intercellular colonization prior to the appearance of necrotic disease lesions. Therefore, M. graminicola is considered as a hemibiotrophic (or necrotrophic) pathogen. Here, we describe the molecular and functional characterization of M. graminicola homologs of (for extracellular protein 6), the Lysin (LysM) domain-containing effector from the biotrophic tomato (Solanum lycopersicum) leaf mold fungus Cladosporiumfulvum, which interferes with chitin-triggered immunity in plants. Three LysM effector homologs are present in the M. graminicola genome, referred to as Mg3LysM, Mg1LysM, and MgxLysM, Mg3LysM and Mg1LysM genes were strongly transcriptionally up-regulated specifically during symptomless leaf infection. Both proteins bind chitin; however, only Mg3LysM blocked the elicitation of chitin-induced plant defenses. In contrast to C. fulvum Ecp6, both Mg1LysM and Mg3LysM also protected fungal hyphae against plant-derived hydrolytic enzymes, and both genes show significantly more nucleotide polymorphism giving rise to nonsynonymous amino acid changes. While Mg1LysM deletion mutant strains of M. graminicola were fully pathogenic toward wheat leaves, Mg3LysM mutant strains were severely impaired in leaf colonization, did not trigger lesion formation, and were unable to undergo asexual sporulation. This virulence defect correlated with more rapid and pronounced expression of wheat defense genes during the symptomless phase of leaf colonization. These data highlight different functions for MgLysM effector homologs during plant infection, including novel activities that distinguish these proteins from C. fulvum Ecp6.