Transferred resistance – interspecific transfer of plant defence against soilborne pathogens

…plants can transfer defence compounds between them, causing significant metabolome changes and, ultimately, inducing root-knot nematode resistance in otherwise susceptible neighbouring plants. In natural systems, high plant diversity reportedly leads to overyielding–an established ecological principle that has been related to reduced soilborne herbivory (van der Putten et al., 2013). Plant performance in diverse assemblages can be increased through the putative dilution effect of specialist pest and pathogen populations. Interestingly, nematode-resistant plants have been shown to confer resistance to neighbouring plants in what has been coined associational resistance (Liu et al., 2022). Grassland plants suffered significantly lower herbivory and supported smaller populations of plant-parasitic nematodes when grown with a resistant plant. A meta-analysis of cropping systems suggests that this may be a common phenomenon in the field (Chadfield et al., 2022). Such natural bottom-up control processes provide the theoretical basis for crop diversification and intercropping in agroecosystems, but thus far, an explanatory mechanism had not been proposed. The transferred resistance documented by Hama et al. could explain this interaction among plants and soilborne pathogens. Their findings are summarised in Fig. 1, representing how benzoxazinoids (BXs) exuded by rye (Secale cereale) roots into the soil can be taken up, metabolised and translocated by roots of clover (Trifolium repens), an unrelated plant species, and how these plants then reduce nematode infection and reproduction (Fig. 2). The plant composition of a suite of other secondary metabolites, including flavonoids, differed in experimental treatments, as detected through targeted and untargeted metabolomic studies. Here, BXs are evidenced because, contrary to the other metabolites, they were known to be exclusively produced by rye – BXs detected in clover had to be taken up from rye-trained soil. Root exudates not only provide a wealth of nutrients to rhizosphere organisms, structuring communities of microbiota, but also convey information, attracting pests and pathogens, as well as mutualists. Compounds in root exudates can also act as cues for plant–plant communication. For example, exudates emanating from roots of plants infected by root-knot nematodes induce an overcompensation effect of increased performance in other plants, as if anticipating nematode attack (Zhang et al., 2020). This suggests that transferred resistance may well be only partially the cause for reduced nematode infection in receiver plants and calls for further research. Hama et al. showed that rye root exudates were a source for BXs and induced specific changes in the intrinsic metabolite composition of cocropped receiver plants, and nematode resistance was ascertained in clover subsequently grown in rye-free soil. This methodological design of moving clover plants to fresh soil before root-knot nematode inoculation was a sound strategy to control for confounding effects. In doing so, Hama et al. established that the associated metabolome changes occur even in the absence of root-knot nematodes. In fact, transferred resistance to plants that have not been challenged by these nematodes is an ecological paradox, especially because certain metabolome changes were associated with phytotoxic effects: clover plants cocropped with rye had a significant reduction of biomass in shoots and roots compared with the control (Fig. 2). Unless root-knot nematodes are a common soilborne pathogen to clover, there seems to be little ecological advantage to the receiver plants. Indeed, metabolic changes in clover may indicate an ‘unintended’ uptake of the toxic compounds. Hama et al. propose that some BXs may have been metabolised (e.g. through glycosylation) to reduce their toxicity and improve clover tolerance. In practical terms, one could anticipate that this form of transferred resistance would be more advantageous to crops in agroecosystems than to undomesticated plants in diverse natural systems, in which plant-parasitic nematodes may be less impactful and plant–plant competition more pronounced (Costa, 2024). However, the BX-associated phytotoxicity would cause unwanted effects and prevent field application in intercropping strategies. Hama et al. give indications on how rye plants could be managed to provide young clover plants with defence against root-knot nematodes but escape phytotoxicity. Both the density of cocropped plants and the duration of exposure significantly affected the clover–rye interaction, and their results do suggest a long legacy of metabolome changes in clover. The incorporation of rye and clover combinations as part of a cocropping, intercropping or crop rotation in plant protection against root-knot nematode attack will depend on a successful strategy design. Whatever the results of field validation, the contribution of Hama et al. to elucidating the complex interactions among plants and soilborne pathogens will be pivotal in the development of ecological theory with potential application in agroecology. The transferred resistance receiver was a legume, and legumes form nitrogen-fixing symbioses with rhizobia. While the effect of cocropping on nodulation and nitrogen fixation was not examined here, it is likely that exposure to BXs could directly or indirectly alter the activity of rhizobia. Nodulation genes in rhizobia are activated by specific host flavonoids. In addition, flavonoid exposure can alter the competitiveness of specific strains and influence the quorum-sensing-related behaviours of rhizobia (Hassan & Mathesius, 2012). The reductions in total flavonoid concentration observed in clover grown with rye will likely indirectly affect nodulation. However, the effect of BXs was specific for individual flavonoid metabolites with certain functions. For example, an isomer of the nod gene inducer apigenin was reduced in cocropped compared with monocropped clover, while the concentration of the inducer 7,4′-dihydroxyflavone was unchanged. The functions of kaempferol and chrysin, which were also severely reduced under cocropping treatments, remain unknown for the rhizobium–clover symbiosis. Thus, future experiments could explore the effect of cocropping on nitrogen fixation in legumes and the mechanisms involved. Other studies showed the strong positive effects of cocropping maize, another cereal exuding BXs, on nitrogen fixation in legumes, and this was linked to enhanced flavonoid exudation by the legume (e.g. Li et al., 2016). However, it was not investigated if changes in legume flavonoid production were mediated by BXs or other metabolites. Mutants defective in BX production will be necessary to ascertain their effects on the metabolome and the resulting nitrogen fixation capacity of cocropped legumes. Some legume–rhizobia combinations have been shown to reduce root-knot nematode galling (Costa et al., 2021), and the protective role of these rhizobia associations may be hampered by cocropping with BX producers. However, the groundbreaking work by Hama et al. will encourage research to establish whether other forms of resistance, including rhizobia-induced resistance, can also be transferred to neighbouring plants. Further experiments could test how common the transfer of BXs is between different plant species and whether it has broader ecological consequences on the soil microbiome, as well as on specific interactions with other pests, pathogens or mutualists. Elucidating the metabolic transformations, transport processes and functions of associated metabolome changes will be important to understand to what extent the transfer of BXs to receiver plants has resulted in active mechanisms of information flow between different plant species. SRC acknowledges support by the ‘Contrato-Programa’ UID/04050/2025 funded by FCT I.P. doi: 10.54499/UID/04050/2025 and the RHIPL project COMPETE2030-FEDER-007115 2023.17906.ICDT, doi: 10.54499/2023.17906.ICDT. UM acknowledges funding through the Research School of Biology, Australian National University. During the preparation of this work, the authors used Gemini 2.0 to generate part of the images in Figs 1 and 2 (the plant shoots). 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