Deciphering plant health status: The link between secondary metabolites, fungal community and disease incidence in olive tree

Front Plant Sci. 2023 Mar 22:14:1048762. doi: 10.3389/fpls.2023.1048762. eCollection 2023.

Abstract

Plant-associated microorganisms are increasingly recognized to play key roles in host health. Among several strategies, associated microorganisms can promote the production of specific metabolites by their hosts. However, there is still a huge gap in the understanding of such mechanisms in plant-microorganism interaction. Here, we want to determine whether different levels of olive leaf spot (OLS) disease incidence were related to differences in the composition of fungal and secondary metabolites (i.e. phenolic and volatile compounds) in leaves from olive tree cultivars with contrasting OLS susceptibilities (ranging from tolerant to highly susceptible). Accordingly, leaves with three levels of OLS incidence from both cultivars were used to assess epiphytic and endophytic fungal communities, by barcoding of cultivable isolates, as well as to evaluate leaf phenolic and volatile composition. Fungal and metabolite compositions variations were detected according to the level of disease incidence. Changes were particularly noticed for OLS-tolerant cultivars, opposing to OLS-susceptible cultivars, suggesting that disease development is linked, not only to leaf fungal and metabolite composition, but also to host genotype. A set of metabolites/fungi that can act as predictive biomarkers of plant tolerance/susceptibility to OLS disease were identified. The metabolites α-farnesene and p-cymene, and the fungi Fusarium sp. and Alternaria sp. were more related to disease incidence, while Pyronema domesticum was related to the absence of disease symptoms. Cultivar susceptibility to OLS disease is then suggested to be driven by fungi, volatile and phenolic host leaves composition, and above all to plant-fungus interaction. A deeper understanding of these complex interactions may unravel plant defensive responses.

Keywords: Venturia oleaginea; endophytes; epiphytes; phenolic compounds; volatile compounds.

Grants and funding

This work is funded by FEDER funds through COMPETE (Programa Operacional Factores de Competitividade), national funds through FCT (Fundação para a Ciência e a Tecnologia) and by Horizon 2020, the European Union’s Framework Programme for Research and Innovation, within the project PRIMA/0002/2018 (INTOMED - Innovative tools to combat crop pests in the Mediterranean), and the Mountain Research Center - CIMO (UIDB/00690/2020 and UIDP/00690/2020) and SusTEC (LA/P/0007/2020) as well as BioISI (UIDB/04046/2020) and CBMA (UIDB/04050/2020). TG thanks FCT, for PhD SFRH/BD/98127/2013 grant. JP thanks Grants for the Recualification of the Spanish University System for 2021-2023, Public University of Navarra. Recualification Modality. Funded by the European Union – NextGenerationEU.