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The Plant Immune System: a multidisciplinary approach to uncover how plants simultaneously deal with beneficial and parasitic organisms to maximize profits and protection

Final Report Summary - PLANTIMMUSYS (The Plant Immune System: a multidisciplinary approach to uncover how plants simultaneously deal with beneficial and parasitic organisms to maximize profits and protection)

As a result of the rapidly growing human population, mankind faces the enormous challenge to increase agricultural productivity while decreasing our ecological footprint in a changing climate. Plants are continuously threatened by a multitude of pathogens and pests, resulting in global crop losses that are estimated at over 25%. To sustain increase of crop production, novel more sustainable strategies for crop protection need to be developed, which imposes a major challenge on the plant science research community.

In nature, plants nurture a large community of beneficial microbes that provide them with essential services, such as enhanced mineral uptake, nitrogen fixation, growth promotion, and protection from pathogens. These plant microbiota are predominantly hosted by the root system, and can be selected for by the plant via root exudates. Selected rhizosphere microbes promote plant health by priming the plant’s immune system, a phenomenon called induced systemic resistance (ISR) and which does not suffer from typical growth-defense tradeoffs. This ERC research programme was focused on unraveling how the plant immune system orchestrates simultaneous interactions with multiple beneficial and harmful organisms. The research output provides a firm knowledge basis for sustainable crop-improving strategies that enhance crop productivity with less input of agrochemicals and fertilizers.

Research highlights:

1) Plants excrete up to 20% of their photosynthetically fixed carbon sources into the root environment, thereby influencing the composition of root-associated microbiota. We showed that upon infection by the downy mildew pathogen, plant roots recruit a specific consortium of beneficial microbes, that in turn stimulate plant immunity against the attacking pathogen and promote growth of the plant. Detailed knowledge on such sophisticated plant-beneficial microbe interactions can aid in the design of dedicated biological control strategies that allow plants to produce more from less.

2) The root-specific transcription factor MYB72 emerged as a central regulator of systemic immunity that is triggered by specific beneficial microbes in the rhizosphere. We unraveled in detail the gene regulatory network of rhizobacteria-activated MYB72 in plant roots. We demonstrated that airborne microbial signals are involved in the activation of MYB72 and that this transcription factor is involved in the biosynthesis and excretion of iron mobilizing phenolic compounds with selective antimicrobial activity. We present a model in which MYB72-regulated metabolites play a central role in systemic activation of broad-spectrum disease resistance, enhanced iron uptake by the plant, and modulation of the composition of the root microbiome with mutual benefits for both plant and inducing microbe.

3) Plant hormones play a delicate role in the regulation and fine tuning of plant growth and defense. Using a novel high-density time series RNA-Seq approach, we unraveled the response of plants to the defense-related hormones jasmonic acid and salicylic acid in unprecedented detail. We obtained detailed insight into the chronology of the molecular processes that unfold in response to hormonal defense stimulation. Computational analysis of the underlying gene regulatory networks predicted so-far unknown roles of a number transcription factors, several of which proved to have important biological functions in defense against necrotrophic pathogens or insect herbivores.

In this ERC research programme, new discoveries have advanced our understanding of how plants are able to simultaneously deal with pests, pathogens, and beneficial root-associated mutualists and maximize profitable as well as protective functions from the root microbiome. Besides exciting fundamental new insights into plant immune system functioning, we also provided a firm knowledge basis for the design of more sustainable crop improvement strategies that would allow enhanced crop production with less input of agrochemicals.