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With a little help from the neighbours: Intercellular cooperation in a fungal plant pathogen facilitates host colonization

Intercellular cooperation in a fungal plant pathogen facilitates host colonization
Some bacterial pathogens are known to rely on cooperation between individuals and species for efficient colonization of their host and the onset of disease. LIPM researchers (UMR INRA / CNRS) examined in this PNAS article the regulation of genes in cells from different parts of a fungal plant pathogen and found evidence for cooperation between these fungal cells. They further show that cooperation between fungal cells is particularly important for the efficient colonization of resistant plants. These findings establish cooperation as a mechanism supporting disease caused by fungal pathogens that should be taken into account in the design of disease management strategies.

Cooperation is associated with major transitions in evolution such as the emergence of multicellularity. It is central to the evolution of many complex traits in nature, including growth and virulence in pathogenic bacteria. Whether cells of multicellular parasites function cooperatively during infection remains, however, largely unknown.

The LIPM researchers demonstrate in this article that hyphal cells making the filaments of the fungal pathogen Sclerotinia sclerotiorum reprogram towards division of labor to facilitate the colonization of host plants. Using global transcriptome sequencing, they reveal that gene expression patterns diverge markedly in cells at the center and apex of hyphae during Arabidopsis thaliana colonization compared with in vitro growth.

The authors then reconstructed a genome-scale metabolic model for S. sclerotiorum and used metabolic flux balance analysis to demonstrate metabolic heterogeneity supporting division of labor between hyphal cells. Accordingly, continuity between the central and apical compartments of invasive hyphae was required for optimal growth in planta. Using a multicell model of fungal hyphae, we show that this cooperative functioning enhances fungal growth predominantly during host colonization. This work identifies cooperation in fungal hyphae as a mechanism emerging at the multicellular level to support host colonization and virulence.

These results establish cooperation as a mechanism supporting diseases caused by fungal pathogens that should be considered in the design of disease management strategies.

See also

Rémi Peyrauda, Malick Mbengue, Adelin Barbacci & Sylvain Raffaele. Intercellular cooperation in a fungal plant pathogen facilitates host colonization.PNAS February 19, 2019 116 (8) 3193-3201; https://doi.org/10.1073/pnas.1811267116