Among the extensive cortège of plant-associated microorganisms (the so-called plant microbiota), mutualistic fungal and bacterial symbionts are striking examples of soil microorganisms that have successfully coevolved with their hosts since plants adapted to terrestrial ecosystems. They promote plant growth by facilitating the acquisition of scarce nutrients. In these associations, plant root colonization requires complex molecular cross-talk between symbiotic partners to activate a variety of host developmental pathways and specialized symbiotic tissues and organs. Despite the evolutionary distances that separate mycorrhizal and nitrogen-fixing symbioses, recent research has identified certain highly conserved features associated with early stages of root colonization. We focus on recent and emerging areas of investigation concerning these major mutualistic symbioses and discuss some of the molecular pathways and cellular mechanisms involved in their evolution and development.
Phylogenomic analyses and divergence time estimates based on symbiotic plant fossils are shedding light on the evolution of mutualistic symbioses. The earliest land plants [~407 million years ago (Ma)] were associated with fungi producing mycorrhiza-like intracellular structures similar to extant symbioses involving Glomeromycotina and Mucoromycotina. Arbuscular mycorrhizal endosymbioses then diversified by the Late Carboniferous. Pinaceae species from the Late Jurassic and Early Cretaceous (~180 Ma) formed the first ectomycorrhizal associations involving Dikarya. More recently, certain angiosperms evolved a “predisposition” for the evolution of nitrogen-fixing root nodule symbioses (~100 Ma) with bacteria.
A conserved core module of the “common symbiotic signaling pathway” (CSSP) is shared by all host plants that establish endosymbioses, including arbuscular mycorrhizal, rhizobial, and actinorhizal associations. This striking conservation among widely divergent host species underlines the shared evolutionary origin for this ancient symbiotic signaling pathway. Furthermore, chitin-based signaling molecules secreted by both arbuscular mycorrhizal fungi and rhizobia activate the host CSSP after perception by related receptor-like kinases. Downstream signal transduction pathways then lead to the apoplastic intracellular infection modes that characterize the majority of these associations and, finally, to the coordinated development of sophisticated bidirectional symbiotic interfaces found in both arbuscules and nitrogen-fixing nodules. A common feature of all these mutualistic associations is phytohormone-associated modifications of root development, which lead to an increase in potential colonization sites as well as major structural and functional changes to the root during the establishment of symbiotic tissues.
Although we are at last beginning to understand how mutualistic microorganisms communicate with plants, how associated root developmental pathways are modulated, and how plant immune responses are successfully circumvented, many important questions remain. For example, little is currently known about more primitive modes of intercellular apoplastic colonization, whether for ectomycorrhizal fungi or for certain nitrogen-fixing symbioses. Neither do we know whether the CSSP has a key role in ectomycorrhizal associations, nor how host plants distinguish between structurally similar chitin-based “symbiotic” and “pathogenic” microbial signals. Answering these questions should contribute to our understanding of the underlying mechanisms that govern the relationships between plants and their entire microbiota. On a broader level, improved understanding of how environmental and genetic cues, together with plant metabolism, modulate microbial colonization will be crucial for the future exploitation of the microbiota for the benefit of sustainable plant growth.