Legume plants have the capacity to enter different endosymbiotic interactions with soil microbes. Whereas the symbiotic interaction with rhizobial prokaryotes leads to the formation of root nodules, the interaction with soil fungi of the genus Glomus results in the establishment of an arbuscular mycorrhiza. Both interactions are characterised by bidirectional nutrient transfer, since the microbial symbionts obtain carbon compounds in return for supplying nutrients to the plant. In particular the early stages of the two symbioses are characterized by the activation of a common signaling network.
A remarkable feature of legume plants is their capacity to enter a nitrogen-fixing root nodule endosymbiosis with prokaryotes from the genera Rhizobium, Sinorhizobium, Mesorhizobium, Bradyrhizobium and Azorhizobium that are collectively termed rhizobia. This extremely host-specific interaction is initiated in the root cortex after a perception of species-specific rhizobial lipochitooligosaccharide nodulation factor (Nod-factor) morphogens through membrane-bound LysM-type receptor kinases. Signal transduction triggers the expression of additional genes located further downstream in the Nod-factor perception pathway and finally results in the organogenesis of a unique plant organ, the root nodule.
Nodules are colonized by the rhizobial prokaryotes through specific structures called infection threads. Subsequent to the endocytotic uptake of rhizobia at the infection thread tips, cells from the inner region of root nodules house the nitrogen-fixing endosymbiotic microsymbionts in transient organelles referred to as symbiosomes. Here, rhizobia differentiate into bacteroids capable of carrying out biological nitrogen fixation, the conversion of atmospheric dinitrogen to ammonia. To drive bacteroid energy metabolism required for the cleavage of the stable triple bond of dinitrogen, the plant supplies dicarboxylic acids to the endosymbiotic prokaryotes. In exchange for this, ammonia is released by the symbiosomes through channel proteins located in a highly specialized perisymbiotic membrane.
Indeterminate root nodules formed by legumes of the genera Vicia, Pisum, and Medicago are characterized by a persistent apical meristem that leads to the continuous formation of different zones in the central nodule tissue: the meristematic zone, the prefixing zone, the interzone, the fixation zone, and the senescence zone. Apart from studying nitrogen fixation, the formation of indeterminate-type root nodules is an excellent model to address processes of general relevance for plant biology, e.g. the de-differentiation of root cortical cells prior to nodule primordium establishment, the formation of a persistent apical meristem, the differentiation of specific tissues and the sharing of metabolic tasks between infected and non-infected cells.
Whereas the root nodule symbiosis is unique to legumes, more than 80% of higher plants enter an arbuscular mycorrhiza (AM) endosymbiosis with fungi of the phylum Glomeromycota, with prominent representatives being Glomus intraradices and Glomus mosseae. In AM, fungal hyphae from an extraradical mycelium penetrate the root epidermis through an appressorium structure and subsequently proliferate in the inner cortex. These intraradical, intercellular hyphae terminate in highly branched, intracellular structures designated arbuscules.
Comparable to root nodules, nutrient exchange occurs at the intracellular interface between the symbionts, the peri-arbuscular membrane that surrounds the arbuscules. In addition, it is assumed that the intraradical hyphae are a major site for the transfer of nutrients, most importantly for the allocation of carbohydrates to the fungus. In return for the supply with carbohydrates, the fungal microsymbiont transfers minerals, and in particular phosphorus, from the soil to the plant. In this case, the arbuscules are assumed to be the major site of nutrient exchange with mycorrhiza-specific phosphate transporters being exclusively localized at the arbuscular interface.
From a functional point of view, AM essentially enlarges the size and surface area of a plant root system that way facilitating an optimized uptake of phosphorus and minerals from the soil. Due to the emergence of arbuscular mycorrhiza appr. 400 million years ago, it has been speculated that the ability to enter this symbiosis was a prerequisite for the evolution of land plants.