Molecular communication and nutrient transfer of arbuscular mycorrhizal fungi, symbiotic nitrogen-fixing bacteria, and host plant in tripartite symbiosis

Abstract

Plants colonized by Arbuscular mycorrhizal fungi (AMF) greatly enhance Phosphorus (P) and Nitrogen (N) acquisition, especially by extra radical mycelium. On the other hand, soil bacteria referred to as rhizobia establish a symbiotic relationship with legume plants by making novel root organ known as nodules, which fix atmospheric dinitrogen (N2) and transfer it to the host plant. The symbiotic relationship of both AMF and rhizobia with the same host leguminous plants is termed a "tripartite symbiosis". This tripartite interaction allows legume plants to grow well in nutrient-deficient soils. Sophisticated and complex molecular communication exists between the AMF, rhizobia and host plant during tripartite symbiosis. In this chapter, we focus on some common features of the molecular dialogue shared during tripartite symbiosis. AMF and the nodulation process of rhizobia requires molecular recognition, regulation and specialized complex signaling molecules. For instance, plants secrets strigolactone (SL), which activates and up-regulates the mycorrhizal factor (myc factor) genes of AMF, which make an association with plant root hairs. SL exudates of plant roots also play a crucial role in rhizobial symbiosis, with SL-biosynthesis mutants of Pisum sativum and Lotus japonicus plants showing reduced nodule number. On the other hand, specific flavonoids molecules secreted by legume plants not only trigger the rhizobial nodulation factor (nod factor) genes responsible for nodule formation, but are also vital for hyphal growth of AMF. Moreover, the small polysaccharides, glycoproteins, and proteins (e.g., chitinrelated compounds) responsible for stimulating transcription for enzymes involved in the synthesis of flavonoids are considered to be of fungal origin. Thus, establishment of tripartite symbiosis likely requires coordinated gene regulation synchronized by mutual exchange of diffusible signal molecules to induce the expression of genes involved in activation of a common symbiotic pathway and in colonization by microbial symbionts. Another common feature between AMF and rhizobia is that both benefit from carbohydrates provided by the host plant, which uses these symbionts as a source of energy. Finally, after the exchange of common signaling and the establishment of tripartite symbiotic interactions, the genes responsible for P and N metabolism and translocation are up-regulated, which increases the P and N supply to the host plant, especially in nutrient-scarce conditions, and ultimately increases agricultural productivity. However, to date, our knowledge of the synergistic or antagonism effects of the tripartite symbiosis on different beneficial microbes remains sparse, and requires further investigation in future studies.