Essential oil vapor triggers resistance pathways in Vitis vinifera and blocks plasmopora viticola infection

Abstract

The amount of synthetic pesticides applied in viticulture is relatively high compared to other agricultural crops, due to the high sensitivity of grapevine to diseases such as downy mildew (Plasmopora viticola). Alternatives to reduce fungicides are utterly needed to promote a sustainable vineyard-ecosystems and meet consumer acceptance.
Essential oils (EOs) are amongst the most promising natural plant protection agents and have shown their antifungal properties previously. However, the efficiency of EOs depends highly on timing and application technique. Additionally, the molecular interactions of host, pathogen and EO, which underlie the efficiency of EOs, are not understood. The presented study aimed to a) evaluate whether a continuous fumigation of EO can control downy mildew and b) decipher molecular mechanisms triggered in host and pathogen by EO. A custom made climatic chamber was constructed, which enabled a continuous fumigation of vines with different EOs during long term experiments.
Several experiments were carried out with vine cuttings infected with Plasmopora viticola and subsequently exposed to continuous fumigation of different EOs with different concentrations and application times (24 h to 10 d). Experiments were stopped when infection symptoms were clearly present on the control. Physiological parameters (photosynthesis, growth rate) were recorded and leaves were sampled at different time points for subsequent RNA extraction.
The post-infection oregano oil vapor treatment during 24h was sufficient to reduce downy mildew development to 95%. Leaf RNA sampled after 24 hours and 10 days of EO treatment was used for RNA-seq analysis. Sequenced reads were mapped onto the Vitis vinifera and Plasmopora viticola genomes. Less than 1% of reads could be mapped onto the Plasmopora genome from treated samples, whereas up to 30 % reads mapped from the controls, thereby confirming visual observation of P. viticola absence under treatment. An average of 80 % reads could be mapped onto the V. vinifera genome for differential expression analysis, which yielded 4800 modulated transcripts. Grapevine genes triggered by EO treatment were mainly linked to plant biotic stress response and plant-pathogen interactions. Key genes controlling ethylene synthesis, phenylpropanoids and flavonoid synthesis were also highly activated by EO. We report here for the first time the effects of EO treatments on the control of a grapevine pathogen, concomitantly with the molecular description of EO-host-pathogen interactions. These results strongly support the hypothesis that the antifungal efficiency of EO is indirect and mainly due to switching on resistance pathways of the host plants. These results are of major importance for the production and research on biopesticides, plant stimulation products as well as for resistance breeding strategies.