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Fusarium oxysporum mediated underpinning of cell type-specific modulation in multiple host interaction

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Parasitic fungus causing wilt and plant death targets different crops to wreak havoc

Fusarium oxysporum is a formidable parasite; attracted by chemicals released from plant roots, it systemically invades its host, causing massive collapse and death. By studying its molecular dialogue with plants, EU researchers with the FOUNDATION project are looking for new control strategies.

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More than 120 forms of Fusarium oxysporum (Fo), each adapted to a specific crop, cause gigantic economic losses worldwide. “A recently emerged strain, Tropical Race 4, currently threatens to eradicate global banana production,” says Antonio Di Pietro, project coordinator and Professor of Genetics at the University of Cordoba.

Parasite molecules ‘talk’ to the host plant

The research group studied the interaction of Fo in four different plant species: tomato, banana, the model plant Arabidopsis, and the ancestral land plant Marchantia polymorpha. “This enables us to identify the conserved mechanisms underlying biotrophic, or live cell, infection stages of Fo wilt disease during interaction with a broad host range,” outlines Di Pietro. This research was undertaken with the support of the Marie Skłodowska-Curie Actions programme. Some time ago, the research team discovered a chemotropic sensing mechanism by which this fungus locates plants in the soil and grows towards chemoattractants released by the roots. The invader then grows silently in the root and colonises the vascular tissue, often leading to plant death. A second type of crosstalk occurs when the fungus grows between the cells of the root cortex, the apoplast. Di Pietro explains: “By using discovery proteomics, we are looking for key signalling molecules from both parties that likely shape the biotrophic molecular dialogue.”

Evasion of the plant immune system is key to successful infection

FOUNDATION has provided unprecedented glimpses of the early infection stages and the molecular dialogue with the multiple plant hosts. For example, the research group has identified the pathogenicity molecules (effectors) that mediate compatibility between fungus and plant. Releasing these effectors helps the pathogen to become more virulent, so the scientists turned to look at M. polymorpha, a newly developed model infection system. Amey Redkar, the Marie Skłodowska-Curie fellow, says: “We aim to determine the function of the identified virulence proteins in this ancient, early, non-vascular land plant to understand how pathogen effector proteins have evolved.”

Applications for pathogen resistance in other crops

Evidence under the FOUNDATION belt suggests that monogenic resistance against Fo is based on molecular recognition of fungal molecules by specific host plant receptors. This then kick-starts the plant immune response. However, pathogens can change their molecules or target the plant’s defence system with specific effector proteins to suppress the immune response. Detailed knowledge of the ‘arms race’ between Fo and its hosts should reveal new resistance strategies. FOUNDATION research has generated new, large-scale data sets, a valuable resource for the scientific community. “Moreover,” Di Pietro continues, “we can now mine the apoplastic root proteome during Fo infection.” An activity-based protein profiling (ABPP) approach has rarely been achieved so far in fungal root interactions and can be used to find missing parts of the molecular cascades for development of sustainable resistance.

A methodological constraint prompted a multi-model approach

Obtaining sufficient fungal biomass for digging out these biotrophic fungal signals has been a challenge. Hence, the FOUNDATION multi-model host system has been crucial. Tomato-Fusarium, for example, is a well characterised system that provides abundant root biomass for biochemical analysis. “We also performed ABPP in the Banana-Fusarium pathosystem, another rare achievement,” Redkar points out. Simultaneously, this provided opportunities to cross validate results from different crop plants. Application of fungicides to the soil is now banned in most agricultural settings so improving plant resistance is the most efficient way to manage these devastating, difficult-to-control diseases. Di Pietro sums up: “FOUNDATION has provided key insights into the molecular biology of vascular wilt disease and opened up new avenues for crop resistance breeding.”

Keywords

FOUNDATION, plant, fungus, resistance, wilt, biotrophic, Fusarium oxysporum, immune response, immune system, resistance breeding

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