Between 2018 and 2022 the global amount of fresh underground crop harvest that was transported internationally increased from around 26.9 to 32.0 Mio t per year (FAO, 2023). Potatoes and onions accounted for around 50% and 30% of this amount, respectively. Based on the findings of the present study, it is likely that a significant portion of these agricultural goods were accompanied on their international journey by live propagules of AM fungi. Phytosanitary procedures and certificates required for import of fresh vegetables and tuber crops vary between countries but often do not involve antimicrobial treatments capable of eliminating fungal propagules (WTO, 2010). The UAE’s current import regulations for underground crops require that these test negative for the presence of plant pests and diseases, but no general disinfection treatment (MOCCAE, 2024). Australia has recently seen an increase in the export of agricultural goods that underwent phytosanitary irradiation (Akter et al., 2023), and it is possible that such treatment was responsible for the inability of sweet potatoes from Australia to establish AM fungal root colonization. Low doses of ionizing radiation have previously been shown to eliminate AM fungi in soil (Jakobsen, 1984).
To this day, AM fungi are neither considered pathogens nor invasive species, and the presence of their propagules in agricultural harvest products is rarely assessed as part of standard phytosanitary evaluations. The present study may thus be one of the first to demonstrate that international trade of underground crops potentially facilitates long-distance dispersal of AM fungi from agricultural soils.
The location and nature of AM fungal propagules within and around underground crop harvest deserves further investigation. It has been shown that excised fragments of mycorrhizal root systems are a source of AM inoculum (Klironomos & Hart, 2002), and that extraradical AM mycelium can remain infective for several months, even after removal of the host plant shoot (Pepe et al., 2018). In the present study, harvest products consisting primarily of root tissues of mycotrophic plants, such as carrots, sweet potatoes, and taro corms, might thus have provided AM inoculum in form of intraradical and extraradical mycelium. Short mycorrhizal roots and root primordials attached to the basal plate of onion bulbs or garlic cloves might have been responsible for the comparatively high inoculum potential of these harvest products.
Like several other species of the Amaranthaceae/Chenopodiaceae, Beta vulgaris has been described as facultatively mycotrophic (Brundrett, 1991). Some reports found that representatives of that species were non-hosts to AM fungi (Hajiboland et al., 2020), while others have reported a low to moderate extent of AM fungal colonization under experimental conditions (Yadav et al., 2023). The observation of AM in roots of S. bicolor plants inoculated with fresh beetroot peel suggests that the latter contained live propagules of AM fungi, and/or that these had been attached to the peel surface. The attachment of traces of soil to the surface of the harvest products, e.g. in small epidermal cracks or cavities, cannot be excluded for any of the crop samples tested in the present study. For this reason, the observation of inoculum potential in the tested underground harvest does not allow for a conclusion on the mycorrhizal status of the original crops or plant organs. Soil contamination might also be the reason for the transmission of AM fungal propagules with pumpkin peel. Though pumpkin fruits are not considered underground harvest, they often lie on the ground surface as they develop. It has also been observed that AM fungi form spores and hyphae in plant tissues that do not support functional AM symbioses, such as dead roots, seeds, and possibly other porous organic materials (Müller et al., 2017; Rydlová & Vosátka, 2000). The presence of AM spores and hyphae in epidermal tissues of pumpkin fruits, onion bulbs, and other underground shoot parts can thus not be excluded.
Though most of the AM fungal propagules within or attached to crop harvest might ultimately be eliminated in the waste and sewage stream, it cannot be ruled out that a certain portion would find its way back into soil, e.g. when fresh kitchen scraps are disposed into gardens or backyards. Underground crops used as planting material, such as mini bulbs or potato tubers, would very likely transfer AM fungal inoculum from nurseries to farms, unless they undergo a fungicidal treatment. It is also possible that AM fungal propagules would move into washing water as vegetables are cleaned for food preparation. In such cases, they might return to a field or garden when kitchen greywater is used for plant irrigation, or when the washing water is disposed without treatment. When fresh belowground harvest or kitchen scraps are fed to farm animals, live AM fungal propagules are likely to survive their digestive tract and end up in the manure (Mangan & Adler, 2002).
In the present study, plants growing in an alkaline dune soil from the UAE established AM symbioses upon inoculation with underground harvest that originated from various ecological zones. It has been shown that the climate, soil pH, soil fertilization level, and other environmental conditions have an impact on the AM fungal community composition (Duenas et al., 2020; Fang et al., 2023; Kivlin et al., 2011), but individual AM fungal strains differ in their degree of environmental niche specialization (d'Entremont & Kivlin, 2023). Agricultural soils are likely to favour euryoecious ‘generalists’ that can establish symbioses under a wide range of environmental conditions and with a broad spectrum of host plant species. Such AM fungal strains might also have a particularly high potential to become invasive.
In conclusion, the results of the present study suggest that a significant portion of internationally traded underground harvest contains live propagules of AM fungi that can be a source of inoculum for plants growing in sandy soils of the UAE and most likely also other agricultural or natural soil environments. The relative contribution of international trade of underground harvest products to global dispersal of AM fungi deserves further investigation. Similarly, risks associated with the introduction of AM fungi from underground harvest products into natural and agricultural systems should be further assessed. Should future studies reveal a correlation between the AM fungal abundance and diversity in underground crop harvest and the original field soil, sampling, and analysis of internationally traded underground harvest might be used as a relatively simple tool for monitoring and comparison of AM fungal communities in agricultural soils worldwide.