Intercellular cooperation in a fungal plant pathogen facilitates host colonization

Area of Science:

• Evolutionary Biology
• Mycology
• Plant Pathology

Background:

• Cooperation is a key driver of evolutionary transitions, including multicellularity.
• The role of cellular cooperation in the infection process of multicellular parasites, particularly fungi, is poorly understood.
• Understanding cellular cooperation is crucial for deciphering complex traits like virulence in pathogenic bacteria and fungi.

Purpose of the Study:

• To investigate whether hyphal cells of the fungal pathogen Sclerotinia sclerotiorum cooperate during host plant colonization.
• To determine if a division of labor exists among hyphal cells during infection.
• To elucidate the mechanisms underlying cooperative growth and virulence in Sclerotinia sclerotiorum.

Main Methods:

• Global transcriptome sequencing to analyze gene expression differences between hyphal cells at the center and apex during host colonization versus in vitro growth.
• Reconstruction of a genome-scale metabolic model for Sclerotinia sclerotiorum.
• Flux balance analysis to identify metabolic heterogeneity and support for division of labor.
• A multicell model of fungal hyphae to simulate cooperative functioning and its impact on growth.

Main Results:

• Gene expression patterns diverged significantly between central and apical hyphal cells during Arabidopsis thaliana colonization, indicating a division of labor.
• Metabolic heterogeneity was demonstrated via flux balance analysis, supporting distinct roles for hyphal compartments.
• Continuity between hyphal compartments was essential for optimal growth in planta, highlighting cooperative interdependence.
• Cooperative functioning significantly enhanced fungal growth, particularly during host colonization.

Conclusions:

• Hyphal cells of Sclerotinia sclerotiorum exhibit a division of labor, a cooperative mechanism facilitating host plant colonization.
• This multicellular cooperation enhances fungal growth and virulence, representing an emergent strategy for successful infection.
• The study reveals cooperation as a critical factor in the evolution of virulence in fungal pathogens.