Emerging metabolic signals are increasingly recognized as pivotal regulators of plant immunity and programmed cell death, shaping defense and accommodation strategies during interactions with microbial colonizers. Recent studies in our group have highlighted the role of metabolic signals in modulating plant immune responses during colonization by both beneficial and pathogenic fungi.

Our research in iHEAD focuses on characterizing the interference of fungal root microbiota with TIR-mediated plant immunometabolism. In particular, we study the beneficial fungal endophyte Serendipita indica, which employs a biphasic colonization strategy in Arabidopsis thaliana and barley roots. This involves an initial biotrophic phase followed by a cell death phase, confined to the epidermal and cortical root layers, which is essential for fungal accommodation.

Two fungal enzymes, SiE5NT and SiNucA, act synergistically in the apoplast to produce deoxyadenosine (dAdo), a nucleoside that triggers cell death when taken up by the plant. This process is mediated by the equilibrative nucleoside transporter AtENT3 and a novel Arabidopsis TIR-NLR protein, ISI (Induced by S. indica), which modulates the plant’s immune response. The discovery that dAdo-triggered cell death involves TIR-NLR pathways establishes a novel link between fungal metabolism and plant immunometabolism, where host cell death is finely regulated to support beneficial colonization.

A key question that arises is the absence of caspases in plants and the involvement of an NLR in dAdo-mediated cell death in Arabidopsis, suggesting that this signaling pathway is not conserved between plants and animals and relies on different regulatory and execution mechanisms that are not yet fully understood.

Research Focus

WP1: Novel Nucleotide-Based Molecules in TIR-NLR Immunity 

  We aim to identify novel nucleotide-based molecules involved in TIR-NLR-mediated immunity in A. thaliana roots during fungal colonization. This includes exploring EDS1-independent signaling pathways mediated by TNP proteins, which exhibit catalytic TIR activity leading to cell death. TNP proteins, conserved in vascular land plants, may engage different sets of small active metabolites, as shown by recent findings (Johannsdrees et al., Plant Physiology 2023). These pathways will also be analyzed in macrophages to further extend our understanding.

  WP2: Active Metabolites in Fungal Accommodation 

  This work package focuses on identifying new active metabolites that influence fungal accommodation in plant roots. Through metabolomics, proteomics, and A. thaliana knockout mutants, we aim to create a comprehensive metabolic model of root signaling during plant-microbe interactions.