Roots have to balance multitrophic interactions with pathogenic, parasitic and beneficial rhizosphere microorganisms. Most members of the legume family also form specific symbiotic nitrogen-fixing symbioses with rhizobia, although this evolved later than their interactions with pathogens and parasites. These interactions start in the rhizosphere, the area around the root that shows selective abundance of bacterial, fungal and nematode species. Their attraction and colonisation of the root is to a large extent driven by plant metabolites exuded into the rhizosphere, which can affect chemotaxis and motility of parasites, growth of fungal hyphae, as well as microbial metabolism and gene expression.
One diverse class of phenolic metabolites with signalling roles in both mutualism and pathogenesis are plant flavonoids. Some likely ancient functions of flavonoids in many plant species include their activity as phytoalexins against fungal pathogens and oomycetes, and in controlling chemotaxis and motility of parasitic nematodes. However, in legumes, they act specifically in regulation of nodulation gene activity, and this likely evolved more recently. Even though the flavonoid pathway is very diverse, metabolomic analysis of root exudates identified specific isoflavonoids as one class of signals activated by both pathogenic and symbiotic microbes, prompting the question whether some microorganisms are using flavonoids are cues even though they are directed at other microorganisms as signals. We linked isoflavonoid function to altered nodulation gene expression, changes in bacterial quorum sensing perception, as well as chemotaxis and motility of parasitic root knot nematodes. Genetic modification of isoflavonoid synthesis and exudation in the model legume Medicago truncatula altered microbial interactions with legume roots, shifting the balance towards improved symbiosis and reduced infection of parasites.