Metabolic changes induced by Cuscutacampestris Yunck in the host species Artemisia campestris subsp. variabilis (Ten.) Greuter as a strategy for successful parasitisation

Main conclusions C. campestris parasitisation increases internal host defences at the expense of environmentally directed ones in the host species A. campestris, thus limiting plant defence against progressive parasitisation. Cuscuta campestris Yunck is a holoparasitic species that parasitises wild species and crops. Among their hosts, Artemisia campestris subsp. variabilis (Ten.) Greuter is significantly affected in natural ecosystems. Limited information is available on the host recognition mechanism and there are no data on the interactions between these species and the effects on the primary and specialised metabolism in response to parasitisation. The research aims at evaluating the effect of host-parasite interactions, through a GC-MS untargeted metabolomic analysis, chlorophyll a fluorescence, ionomic and delta C-13 measurements, as well as volatile organic compound (VOC) fingerprint in A. campestris leaves collected in natural environment. C. campestris parasitisation altered plant water status, forcing stomatal opening, stimulating plant transpiration, and inducing physical damages to the host antenna complex, thus reducing the efficiency of its photosynthetic machinery. Untargeted-metabolomics analysis highlighted that the parasitisation significantly perturbed the amino acids and sugar metabolism, inducing an increase in the production of osmoprotectants, which generally accumulate in plants as a protective strategy against oxidative stress. Notably, VOCs analysis highlighted a reduction in sesquiterpenoids and an increase in monoterpenoids levels; involved in plant defence and host recognition, respectively. Moreover, C. campestris induced in the host a reduction in 3-hexenyl-acetate, a metabolite with known repellent activity against Cuscuta spp. We offer evidences that C. campestris parasitisation increases internal host defences via primary metabolites at the expense of more effective defensive compounds (secondary metabolites), thus limiting A. campestris defence against progressive parasitisation.

Automated summary

Parasitisation by C. campestris enhances internal host defences but reduces environmentally directed defences, limiting the plant's ability to defend against parasitisation. The parasitisation alters plant water status, amino acid and sugar metabolism, and VOC levels, ultimately affecting the efficiency of photosynthesis and plant defence mechanisms. Overall, C. campestris parasitisation leads to an increase in osmoprotectants and changes in plant volatile compounds, impacting the host's ability to defend against parasitic invasion.