Can mycorrhizal fungi improve the quality of fruits and vegetables?

By: Manuela Giovannetti, University of Pisa, Italy
email: manuela.giovannetti@unipi.it

Beneficial soil microorganisms play a key role in sustainable agriculture, by promoting the completion of biogeochemical cycles, maintaining long-term soil fertility, reducing the input of chemical fertilizers and pesticides, boosting plant nutrition and health. Among them, arbuscular mycorrhizal (AM) fungi (AMF), members of the Glomeromycotina, are a well represented group of microbes, establishing mutualistic symbioses with more than 80% of land plants, including the major food crops, from cereals to legumes, fruit trees, vegetables, medicinal plants and economically relevant species, such as sunflower, cotton, sugarcane, tobacco, coffee, tea and cocoa.

AMF are obligately biotrophic symbionts which obtain carbon from the plant, and, in return, transfer soil mineral nutrients to their hosts. AMF improve plant performance and health also by increasing plant tolerance to biotic and abiotic stresses, carbon sequestration and soil aggregation.

Recent findings showed that AMF may modulate plant secondary metabolism, increasing the activity of antioxidant enzymes and promoting the production of health-promoting compounds, a topic which gained increasing interest and attention not only in the scientific literature, but also in the community of consumers and producers. Indeed, phytochemicals, such as polyphenols, glucosinolates, flavonoids and carotenoids, may reduce oxidative damages, prevent chronic and heart diseases, and decrease the risk of mortality from cancer.

Many works reported a number of data on the metabolic changes induced by AMF, with particular focus on phytochemicals with therapeutic importance, such as biochanin A, formononetin, genistein, daidzein, which may be active in the prevention of osteoporosis and degenerative diseases, sesquiterpene lactones, active in the inhibition of cell proliferation and tumor growth, furanocoumarins and pterocarpans, inducing apoptosis in human colon carcinoma cell lines.

Diverse medicinal and aromatic plants has been studied for their response to mycorrhizal symbioses, in terms of health-promoting phytochemicals. For example, sweet basil which showed higher levels of antioxidant compounds, such as rosmarinic acid and caffeic acid and of essential oils in shoots and leaves, when inoculated with different Glomus species, fennel seeds contained higher concentrations of essential oils when plants were inoculated with R. fasciculatum, compared with non-mycorrhizal controls (+62.5%), and mycorrhizal Echinacea purpurea produced higher levels of therapeutic phytochemicals (up to 30 times).

So far, only a few food crops - lettuce, onion, tomato, maize, artichoke, strawberry, pepper and sweet potato - have been studied for the metabolic changes induced by mycorrhizal symbioses. Among these, different plant varieties showed variable responses to different AMF inocula, stressing the importance of plant and fungal genotype in the production of phytochemicals.

In particular, results obtained from greenhouse and field experiments reported the following data:

- TOMATO: in four out of six cultivars the content of antioxidant compound lycopene in the fruit was increased by single inoculation with F. mosseae or mixed inocula containing both F. mosseae and R. irregulare in microcosms experiments, while in the field the same AM symbionts enhanced the production of ascorbic acid. Interestingly, the content of ß-carotene and total phenols showed higher values under organic management in the field.

- ARTICHOKE: the cultivar Terom increased its antioxidant activity and the concentration of total phenolics when inoculated with F. mosseae and R. irregulare both in microcosms experiments and in the field, while Romanesco cultivar showed increased values of total phenolics only with a commercial inoculum based on R. irregulare. 

- ONION: in the variety Nasik red N-53 the two mycorrhizal inoculants F. mosseae and R. irregulare enhanced the levels of phenolics in microcosms, while no effects were found with the variety Hyskin in the field.

- PEPPER: in greenhouse, the variety San Luis showed higher content of carotenes and xanthofills when inoculated with a specific AMF mixture, while the variety Cacho de cabra increased the concentration of ascorbic acid only when treated with a native inoculum, compared with a commercial one.

- STRAWBERRY: different commercial AMF inoculated in microcosms on six different varieties showed contrasting results, the most remarkable being represented by the absence of effects on the content of a number of phytochemicals.

- LETTUCE: some green and red leaf lettuce varieties contained larger amounts of anthocyanins, carotenoids, chlorophylls, tocopherol, and total phenolics, and showed a higher antioxidant activity, compared with control plants, when inoculated with different AMF in microcosms. Interestingly, carotenoids, total phenols and anthocyanins showed differential concentrations, depending on leaf position and harvest season.

- SWEET POTATO: two AMF isolates, F. mosseae and R. irregulare, increased the concentration of ß-carotene in microcosm, while in the field different AMF mixtures did not show any effect.

The results reported so far underline some flaws, the most important entailing the utilization of a low number of AMF species as inocula (about 24 out of 323), generally the same ones all over the world: further works should be carried out using a high number of different species and isolates of AMF, in order to fully exploiting their large physiological and genetic diversity. Moreover, as in agricultural soils many different AMF may simultaneously colonize the same host plant, it is important to investigate plant responses to inoculation with multiple AMF species and the compatibility of native AMF isolates with the inoculated ones. In conclusion, AMF ability to modulate the biosynthesis of phytochemicals with health-promoting activity should be further exploited, by pursuing a targeted selection of the best performing AMF species and isolates, to be utilized as valuable biotechnological tools for the production of safe and healthy plant foods.