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Which genes determine fungal life-style in the interaction with plants?

Fungi establish different interactions with plants. Close related fungal strains or species may cause diseases or not depending on their repertoire of pathogenicity mechanisms and on the ability of the plant to defend against colonization. Pathogenic fungi attract much of our attention because they cause important losses in crops and ecosystems. However, non-pathogenic fungi also persist in nature, and they may be able to survive on host surfaces, growing epiphytically and establishing specific types of interactions with plants. Comparing the genomes (repertoire of genes) and transcriptomes (genes expressed) of pathogenic and non-pathogenic fungal strains in their interaction with plants provides cues about the genetic determinants that lead, or not, to disease.

The fungus Plectosphaerella cucumerina is a pathogen of some crops, but also a model organism for the study of Arabidopsis thaliana basal and nonhost resistance to necrotrophic fungi. In this work, the “Plant Innate Immunity and Resistance to necrotrophic fungi” group of the CBGP has sequenced, annotated, and compared for the first time the genomes and transcriptomes of three strains of the genus Plectosphaerella with different lifestyles on A. thaliana: PcBMM, a natural pathogen of wild-type plants (Col-0), Pc2127, a nonpathogenic strain on Col-0 but pathogenic on the immunocompromised cyp79B2 cyp79B3 mutant, and P0831, a non-pathogenic strain isolated from a natural population of A. thaliana that grows epiphytically on Col-0 and cyp79B2 cyp79B3 plants. The genomes of these Plectosphaerella strains are very similar and do not differ in the number of genes with pathogenesis-related functions, with the exception of secreted carbohydrate-active enzymes (CAZymes), which are up to five times more abundant in the pathogenic strain PcBMM. Analysis of the fungal transcriptomes in inoculated plants at initial colonization stages confirm the key role of secreted CAZymes in the necrotrophic interaction. The authors also found that P0831 epiphytic growth on A. thaliana involves the transcription of specific repertoires of fungal genes, which might be necessary for its growth adaptation. The sequences of Plectosphaerella spp. genomes and transcriptomes described in this article are the first published of this fungal species and also the first genomic project of plant fungal pathogens led by CBGP researchers, who had the collaborative support of Toni Gabaldón Group (CRG). This comparative genomic study could contribute to design crop protection strategies specifically targeting pathogenic fungi.

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Figure 1. Differential interactions of Plectosphaerella strains PcBMM (pathogenic), Pc2127 (non
pathogenic), and P0831 (epiphytic) with Arabidopsis wild-type plants (Col-0) and immune-deficient
mutants ein2 pad4 sid2 dde2 and cyp79B2 cyp79B3. A, Macroscopic disease symptoms at 7 days
postinoculation (dpi). (B) Heatmaps of gene expression showing the fungal genes significantly up
regulated (log2FC≥2, FDR<0.05) in plants at 10 and 16 hours post inoculation (hpi) in relation to in vitro
growth. (C). Number of in planta expressed fungal genes in the tested conditions and time points. (D)
Validation by qRT-PCR of the expression of some fungal selected genes in plants at different time
points.

Original Paper:

Muñoz-Barrios, A., Sopeña-Torres, S., Ramos, B., López, G., Del Hierro García, I., Díaz-González, S., González-Melendi, P., Mélida, H., Fernández-Calleja, V., Mixão, V., Martín Dacal, M., Marcet-Houben, M., Gabaldón, T., Sacristan, S., Molina, A. 2020. Differential expression of fungal genes determines the lifestyle of Plectosphaerella strains during Arabidopsis thaliana colonization. Molecular Plant-Microbe Interactions®. DOI: 10.1094/MPMI-03-20-0057-R

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