Fungal-derived biostimulants boosting Cichorium intybus: effects of Chaetomium globosum and Minimedusa polyspora culture filtrates on growth performance and metabolomic traits

Implementing environmentally friendly and climate-resilient agronomic solutions to increase food production while addressing modern agriculture’s issues is the biggest challenge our society is currently facing. In this context, biostimulants represent a sustainable solution to increase crop resilience and productivity in adverse environmental conditions, while minimizing agrochemicals applications and tackling climate change effects. Among microbial biostimulants, fungi have been reported as particularly effective in promoting plant growth. Moreover, fungi, thanks to a complex extracellular metabolism, exert their influence on plants also through the release in soils of diffusible metabolites in the environment. So, the metabolites released in the culture medium, during growth in controlled conditions, may be applied to simulate these interactions and effectively stimulate plant growth. Indeed, fungal culture filtrates have been consistently reported in several studies to be effective in promoting plant growth by enhancing seed germination, biomass production, and metabolites production. Therefore, this study aimed at investigating the biostimulant effect of fungal culture filtrates of Chaetomium globosum Kunze and Minimedusa polyspora (Hotson) Weresub & P.M. Le Clair on growth performance and metabolomic traits of Cichorium intybus L. (chicory) plants. C. intybus, belonging to the Asteraceae family, is an alimurgic plant whose popularity is steadily increasing due its rich and complex phytochemical profile, including a great number of bioactive substances, and a high nutritional value which make it a plant of agricultural and medicinal importance. This study was conducted as a pot experiment set up in walk-in chambers. Chicory plants, one month after the transfer of the seedlings in pots, were stimulated by soil drenching with 8 ml/pot (30 ml/kg of soil) of the culture filtrates obtained by a 14-days incubation of the fungal strains in Malt Extract Broth (MEB), or the same amount of uninoculated MEB or distilled water in the control groups. Fourteen days after the stimulation, plant biomasses were recovered to estimate several growth parameters and analyze the metabolomic variations occurred in roots and leaves through 1H-NMR 600 MHz. We observed for the first time that M. polyspora culture filtrate promoted an increase of biomass, both in shoots and roots, and of the leaf area, while no increase was observed in plants treated with C. globosum culture filtrate. Based on 1H-NMR metabolomics data, differential metabolites and their related metabolic pathways were highlighted. A common response in C. intybus roots involving the synthesis of 3-OH-butyrate through the decrease of the synthesis of fatty acids and sterols, as a mechanism balancing the NADPH/NADP+ ratio, was observed in both the treatments with C. globosum and M. polyspora culture filtrates. The phenylpropanoid pathway was differently triggered by the fungal culture filtrates. C. globosum culture filtrate increased phenylalanine and chicoric acid in the roots. Chicoric acid, whose biosynthetic pathway in chicory plant is putative and still not well known, is a very promising natural compound playing an important role in plant defense. Instead, M. polyspora culture filtrate interestingly stimulated an increase of 4-OH benzoate, being benzoic acids precursors for a wide variety of essential compounds playing crucial roles in plant fitness and defense response activation. Therefore, both C. globosum and M. polyspora culture filtrates affected C. intybus metabolome and could be considered as fungal bioresources for the development of new biostimulants.