SYMRK, an enigmatic receptor guarding and guiding microbial endosymbioses with plant roots.

T he research field of plant–microbe interactions experiences a surge of fundamental insights thanks to the adoption of a restricted number of model systems. However, to see the broader picture and understand the complexity of evolutionary relationships, it is equally important to study relevant non-model interactions. This task is (still) difficult because of the lack of genomics and genetics tools, but rewarding when the outcome proves some long-standing assumptions and suggests new ways to address old questions. A nice example is the work of Gherbi et al. (1) presented in this issue of PNAS. Their article deals with a nonmodel plant, Casuarina glauca, whose roots interact with both symbiotic fungi and nitrogen-fixing bacteria, and evidences the central and ancestral role of the plant receptor SYMRK in the establishment of the three major types of root endosymbioses. Microbial associations with plant roots form underground networks of diverse and intimate interactions. Three major groups of endophytic root symbioses are of crucial importance for the geobiochemical cycle and the ecological equilibrium of our planet. Fungi of the order of the Glomeromycota form arbuscular myccorhiza (AM) in a ubiquitous ancestral symbiosis with roots of the majority of land plants leading to nutrient exchange at an extended fungus–plant membrane interface (arbuscules) inside cortical root cells (2). More recently in evolution, two types of root symbioses with nitrogen-fixing bacteria arose in the Eurosid I clade of dicots (3). Molecular dinitrogen can only be enzymatically reduced by prokaryotes. In symbiotic interactions, the bacteria directly deliver the fixed nitrogen to the host and provide nitrogen input in the ecosystem using the sun energy captured by the host via photosynthesis. Legume roots interact with Gram-negative rhizobia, whereas non-legume actinorhizal plants interrelate with Frankia bacteria that are Gram-positive filamentous actinomycetes (4, 5). Although based on different schemes, in both cases, the roots develop special structures, nodules, that house nitrogen-fixing bacteria installed inside cortical cells. The legume endosymbioses are the most amenable to molecular dissection. Rhizobial functions for nodulation have been studied by forward and reverse genetics and numerous legume genes with a key role in the interaction have been identified with forward genetics and map-based cloning in the model legumes Medicago truncatula and Lotus japonicus (4). Bacterial lipochitooligosaccharide nodulation factors (NFs) trigger the programs for organ formation and entry. Entry is (mostly) intracellular in the epidermis via deviation of root hair tip growth to form a closed compartment for bacterial colonization (root hair curling) followed by inverted tip growth and intracellular infection thread formation. Several legume complementation groups are known that are essential for nodule initiation. At the top of the signal perception transduction hierarchy are the NF receptors, LysM-type receptor kinases, whose inactivation eliminates all responses to bacteria or purified NFs (4). Purified NFs trigger many events in root hair cells, including an early calcium influx, rhythmic calcium oscillations (spiking) around the nucleus, root hair deformations (for curling), gene expression, and cell division. Also essential for nodulation and for most (but not all) of the early responses are genes encoding cation channels located in the nuclear membrane, a calcium–calmodulin-dependent kinase (CCamK) that presumably decodes the calcium spiking and a plasma membrane-located receptor-like kinase with extracellular leucine-rich repeat domains, SYMRK (synonym for MsNork MtDmi3 LjSymRK PsSym19 SrSymRK CgSymRK), which is needed for nodule initiation as well as for bacterial internalization in cortex cells during symbiosome formation (6–10) (Fig. 1). These functions are also required for AM establishment in the legume hosts and must have been recruited from this ancestral interaction to function in the nodulation program (11). Now, Gherbi et al. (1) demonstrate for the first time that one of these genes, SYMRK, is required in a nonlegume interaction. C. glauca is a pioneer plant that grows in marginal soils and establishes AM with fungi and actinorhizal nodules with Frankia strains.