Compatibility between Legumes and Rhizobia for the Establishment of a Successful Nitrogen-Fixing Symbiosis

Abstract

The root nodule symbiosis established between legumes and rhizobia is an exquisite biological interaction responsible for fixing a significant amount of nitrogen in terrestrial ecosystems. The success of this interaction depends on the recognition of the right partner by the plant within the richest microbial ecosystems on Earth, the soil. Recent metagenomic studies of the soil biome have revealed its complexity, which includes microorganisms that affect plant fitness and growth in a beneficial, harmful, or neutral manner. In this complex scenario, understanding the molecular mechanisms by which legumes recognize and discriminate rhizobia from pathogens, but also between distinct rhizobia species and strains that differ in their symbiotic performance, is a considerable challenge. In this work, we will review how plants are able to recognize and select symbiotic partners from a vast diversity of surrounding bacteria. We will also analyze recent advances that contribute to understand changes in plant gene expression associated with the outcome of the symbiotic interaction. These aspects of nitrogen-fixing symbiosis should contribute to translate the knowledge generated in basic laboratory research into biotechnological advances to improve the efficiency of the nitrogen-fixing symbiosis in agronomic systems.

Keywords: legume; nodulation; rhizobia; soil bacteria.

Figure 1

Signal exchange in the legume-rhizobia interaction. Flavonoids and isoflavonoids secreted by legume roots activate the Nodulation protein D (NodD) transcription factor on compatible rhizobia inducing the transcription of nod genes, which are required for the synthesis of Nod factors. Nod factors are perceived by receptors present in the plasma membrane of root cells, triggering the signaling pathway required for the development and infection of the nodule, where bacteria are allocated, and nitrogen fixation occurs.

Figure 2

The complexity of bacterial root microbiota. The bacterial community decreases in complexity from the rich soil microbiota to the rhizosphere, the rhizoplane, the endosphere, and the nodule. The rhizosphere is colonized by a subset of the bulk soil community, and the rhizoplane hosts epiphytes that are firmly attached to the root surface. The endosphere (root interior) is inhabited by endophytes. The root nodule is the habitat of symbiotic nitrogen-fixing bacteria, known as rhizobia, and also harbors a diversity of non-fixing bacteria called nodule endophytes. Infection threads can be coinhabited by endophytes and rhizobia.

Figure 3

The interplay between nodulation and defense signaling pathways. Plants perceive bacterial molecules (pathogen-associated molecular patterns, PAMPs) using pattern recognition receptors (PPRs) that activate mitogen activated kinase (MAPK) cascades that trigger host defense responses. Adapted pathogens use the type III secretion system (T3SS) to deliver effector proteins into the cytosol of host cells. Bacterial effectors can inhibit the MAPK cascade, leading to suppression of host defenses. In some plants varieties, these effectors are recognized by nucleotide binding site- leucine rich repeat domains (NBS-LRR) receptors, which trigger a second tier of host defense responses. Recognition of Nod factors produced by compatible rhizobia by specific receptors (NFR) triggers a signaling cascade leading to nodulation (NF-Pathway). Rhizobial effectors can also promote nodulation by directly activating the NF-Pathway. The symbiosis receptor-like kinase (SYMRK) is also necessary for nodule formation, but the nature of its putative ligand is unknown. In a second stage of rhizobia recognition, exopolysaccharides (EPS) produced by rhizobia are perceived by exopolysaccharide protein receptor 3 (EPR3), inactivating the defense signaling pathway through unknown mechanisms.