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To the roots of induced systemic resistance in the Arabidopsis-Trichoderma-Fusarium tripartite interaction

Final Report Summary - TO THE ROOTS OF ISR (To the roots of induced systemic resistance in the Arabidopsis-Trichoderma-Fusarium tripartite interaction)

The world’s population is expected to exceed 9 billion people by 2050 and recent FAO estimates indicate that global agricultural production will have to increase by 60 % to meet the projected demand. Significantly adding to the challenge, this increase will have to be obtained in a sustainable way. In order to keep in pace with global demands as well as health and environmental concerns, agriculture must continuously find innovative ways of producing sufficient and quality food and feed. Losses caused by bacterial, viral and fungal microbes is a significant hurdle towards reaching this aim. The exploitation of biological control organisms (BCOs) can make a significant contribution to this goal by reducing losses by plant pathogens. Several BCOs are already exploited in a commercial context, and the so-called biopesticide market is expected to grow further in the years ahead. Beneficial soil fungi belonging to the species Trichoderma are ideal candidates as BCO. These fungi can be antimicrobial, directly inhibiting the growth of pathogenic organisms but can also induce a systemic defense response (ISR) in the plant, leading to a more rapid and robust systemic activation of defense when the plant is subsequently challenged by a pathogen. Several strains also appear compatible with pesticide use, thus facilitating integrated control strategies. However despite such promising characteristics, their utilization and adoption for plant protection purposes has so far remained limited, at least partly due to their more variable performance in practice. A better understanding of their working mechanisms can significantly improve this performance. Genome-wide investigations of the tripartite plant-Trichoderma-pathogen interaction are still scarce, although this knowledge can provide substantial novel information to improve our understanding of ISR, which can form the basis for the development of rational disease management options. In addition, plant root responses have long been neglected, despite the fact that they are the first point of contact for soil microbes and drive aboveground plant responses. In this project the focus will be on the root-infecting fungal pathogen Fusarium oxysporum, which is listed in the top 10 of fungal plant pathogens due to its worldwide impact.
The central research objective of this project is to identify the plant responses originating in the roots that drive the ISR process in the Arabidopsis-Fusarium-Trichoderma interaction. This is achieved by a comparative genomics study of the tripartite interaction in Arabidopsis roots, with Fusarium oxysporum as soil-borne plant pathogen (expertise of outgoing host CSIRO Agriculture Brisbane, Australia) and Trichoderma spp. as BCO (expertise of return host CPMG, KU Leuven, Belgium). The unique characteristic of this project is to bridge research domains on Trichoderma and Fusarium plant responses, thereby focusing on the largely unknown processes that take place in plant roots.
In the project, the fellow has screened several Trichoderma strains belonging to different species for their biocontrol capacity through ISR. Highly promising biocontrol traits were discovered for a strain that had been isolated locally from a disease-suppressive soil. The strain, further termed Tg5, belongs to a species that is not yet well-known for its biocontrol capacities, but the fellow found that Tg5 is highly antimicrobial against a wide spectrum of pathogens and a good ISR-inducer as well. Interestingly, the fellow could also demonstrate that the metabolites secreted by the Tg5 strain are equally able to induce ISR in Arabidopsis against the soil-borne pathogen Fusarium oxysporum. Using a specially developed split-root assay, the fellow investigated the local and systemic ISR responses of Trichoderma-colonized Arabidopsis roots to the soil-borne pathogen Fusarium oxysporum at the transcriptome level. Moreover, the genome of the Tg5 strain was sequenced and a metabolic analysis identified the bioactive fraction in the Tg5 secretions. The analysis of the transcriptomic data showed the involvement of a large number of differentially expressed genes in Arabidopsis roots, that can be grouped in several significantly altered biological pathways. These included amongst others the modulation of hormonal biosynthesis and signaling as well as the induction of phenylpropanoid compounds. An interesting overlap was visible in the plant root responses to the Trichoderma strain, or to its metabolites alone. In addition, the beneficial Tg5 strain and the pathogenic F. oxysporum appeared to induce several similar patterns in the plant roots as well. In addition, the ISR-effect of the Tg5 strain as well as its metabolites was confirmed against the grey mould pathogen Botrytis cinerea in tomato.
The results of the project give a detailed insight into the root transcriptome response during the three-party interaction, and indicate that the Trichoderma strain, together with its bioactive metabolites, has very promising characteristics for use in practice. Moreover, the increased insight resulting from this project into how plant roots respond to such a beneficial fungus can help us to find more microbial candidates for biological control applications. In these ways this research project can contribute to the formation of integrated solutions for more sustainable pest management in our modern-day agriculture.