Grapevine Trunk Diseases: a case of hijacked chemical communication between fungal endophytes and plants and the potential of soil microbiome on promoting plant defence against trunk diseases

With the ongoing climate change, grapevine trunk diseases became a threatening challenge for viticulture worldwide. European wild grapevines from the last viable population in Germany along the Rhine river showed variable degrees of resistance against Neofusicoccum parvum Bt-67, a fungus causing Botryosphaeria dieback. Resistant genotypes showed robust production of Non-glycosylated stilbenes, viniferin trimers. By contrast, the susceptible genotypes accumulated less stilbenes with a significantly higher proportion of glycosylated piceid (Khattab, et al., New Phytologist, 2021).

In addition, the disease outbreak under dry hot summers seems to be controlled by chemical communication between the host and colonizing fungus. We introduce the new concept of a "plant surrender signal" accumulating in host plants under stress and facilitate the fungal transition from latent phase to aggressive necrotrophic behaviour causing apoplectic breakdown in grapevines. Using a cell-based experimental system (Vitis cells) and bioactivity‐guided fractionation, trans‐ferulic acid, a monolignol precursor, was identified as a "surrender signal". This signal specifically activates the secretion of the fungal phytotoxin fusicoccin A aglycone, which targets 14‐3‐3 proteins, manipulating molecular players that regulate programmed cell death, e.g. ROS, actin filaments and metacaspases. Therefore, the channelling of phenylpropanoid pathway from ferulic acid to the trans‐resveratrol phytoalexin could be a target for future therapy (Khattab, et al., Plant Cell and Environment, 2022). Interestingly, in the absence of ferulic acid, the fungus secretes 4‐ hydroxyphenylacetic acid, mimicking auxins on grapevine defence and facilitating fungal spread (Flubacher et al., Plant Cell and Environment, 2023).

As an immediate strategy, we target the soil microbiota that promote viticulture resilience against trunk diseases. Using Shotgun metagenomics as well as molecular and cellular aspects, we identified that enriching the soil with compost and biochar significantly promoted the soil microbiome diversity, and function and it limited the fungal spread in the infected vines.