Signal molecules and cell-surface components involved in early stages of the legume–rhizobium interactions

• Signaling during early stages of legume–rhizobium symbiosis is of great interest from many years because legumes provide high environmental and agricultural benefits for humans, among them are important sources of food, feed, and biofuel crops.
• Over the last decade, our understanding of this “molecular dialog” between both symbiotic partners: host plants and their microsymbionts, has grown immensely, leading to broadening our knowledge of early stages of these plant–microbe interactions.
• The availability of reduced nitrogenous compounds in soil is a major limiting factor for plant growth and effectiveness of agricultural crops.
• Because of this reason, the process of biological nitrogen fixation conducted by symbiotic soil bacteria collectively called rhizobia is crucial for providing high amounts of nitrogen forms available for plants.
• The establishment of symbiosis is a complex process, in which multiple signals and cell-surface compounds derived from both the host plant and bacteria are involved, among them flavonoids and rhizobial lipochitin oligosaccharides play crucial roles.

Legumes are a highly important source of food, feed, and biofuel crops. With a few exceptions, these plants can enter into a complex symbiotic relationship with specific soil bacteria collectively called rhizobia. This interaction leads to formation of a new, highly specialized root organ – the nodule, inside which bacteria, differentiated into bacteroids, reduce atmospheric dinitrogen into forms of nitrogen that are useable by the plant. The legume–rhizobium association is highly specific and tightly controlled mainly by the host plant, in such a way that a particular legume interacts with only a limited set of rhizobial species. The establishment of symbiosis is a complex process, which involves a coordinated exchange of multiple signals between the host plant and its microsymbiont; among them, flavonoids secreted by legume roots and rhizobial lipochitin oligosaccharides (Nod factors) play a crucial role. Also, other plant-derived and bacterial cell-surface components and low-molecular-weight metabolites are engaged in the signaling. Among these, there are several proteins derived from the host plants (Nod factor receptors, signal transduction cascade proteins, lectins, trifolins, remorins), non-flavonoid inducers of rhizobial nod genes, H2O2, NO, and phytohormones. Additionally, rhizobia are actively involved in extracellular signaling to their host legumes to initiate infection and nodule morphogenesis. These bacteria produce and secrete many different compounds including hopanoids, indole-3-acetic acid, quorum sensors, bradyoxetin, lumichrome, H2O2 and NO, several types of surface polysaccharides (extracellular polysaccharide, lipopolysaccharide, capsular polysaccharide, cyclic β-glucan, glucomannan, gel-forming-polysaccharide, cellulose), and proteins secreted via types I and III secretion systems (glycanases, rhicadhesins, NodO, and Nops – nodulation outer proteins). They all contribute to various stages of symbiotic interactions, e.g., attachment to roots, host recognition, infection thread formation, and invasion of nodules. This review summarizes many aspects of the roles of extracellular signals, proteins, and polysaccharides in the early stages of legume–rhizobium symbiosis, showing high complexity in this “molecular dialog” and its interconnection with other cellular processes.