Exploring Legume-Rhizobia Symbiotic Models for Waterlogging Tolerance

Abstract

Unexpected and increasingly frequent extreme precipitation events result in soil flooding or waterlogging. Legumes have the capacity to establish a symbiotic relationship with endosymbiotic atmospheric dinitrogen-fixing rhizobia, thus contributing to natural nitrogen soil enrichment and reducing the need for chemical fertilization. The impact of waterlogging on nitrogen fixation and legume productivity needs to be considered for crop improvement. This review focuses on the legumes-rhizobia symbiotic models. We aim to summarize the mechanisms underlying symbiosis establishment, nodule development and functioning under waterlogging. The mechanisms of oxygen sensing of the host plant and symbiotic partner are considered in view of recent scientific advances.

Keywords: hypoxia; legumes; nitric oxide; oxygen sensing; symbiosis; waterlogging.

FIGURE 1

The main O₂-sensing pathways described in plants (identified in Arabidopsis and hypothesized to be present in M. truncatula) and S. meliloti N₂-fixing bacteria. (A) In Arabidopsis, the Cys branch of the N-end rule pathway for protein degradation allows the O₂-dependent regulation of gene expression (Licausi et al., 2013). ERF-VIIs are a class of transcription factors characterized by a conserved N-termini (N-degron) in which Cys₂ determines the protein’s fate in response to O₂ level inside the cell. In aerobic conditions (left), ERF-VIIs are unable to activate the transcription of anaerobic genes. In these conditions, Met Aminopeptidase (MetAP) removes the N-terminal Met, and PCOs oxidize the resulting exposed Cys (C^∗) (Weits et al., 2014; White et al., 2017). After arginylation by Arginyl Transferases (ATE1-2), an Ubiquitin Ligase (PRT6) identifies the proteins as a degradation substrate for the 26S proteasome. Under O₂ deficient conditions (right), the efficiency of ERF-VIIs oxidation is dampened, allowing the stabilization and translocation into the nucleus to finally induce a set of anaerobic genes (Kosmacz et al., 2015), with Arabidopsis RAP2.2 and RAP2.12 playing a major role in comparison to the other ERF-VIIs (Bui et al., 2015). This also happens through fine regulation controlled by the Hypoxia Response Attenuator (HRA1), which antagonizes RAP2.12 through a feedback mechanism that enables a flexible response to different levels of O₂ availability (Giuntoli et al., 2014, 2017). The cis-regulatory element Hypoxia Responsive Promoter Element (HRPE) has been identified as being enriched in some hypoxia-responsive genes (Gasch et al., 2016). (B) FixL-FixJ two-component regulatory system in S. meliloti symbiotic bacteria regulates the expression of nif and fix gene clusters in an O₂-dependent way. In free-living bacteria (left), FixL is inhibited by the binding of O₂ to the heme moiety inside the PAS domain. By establishing symbiosis with the plant, nodule formation gives rise to a microoxic environment surrounding the microbial cells (right). In turn, FixL is activated by auto-phosphorylation and transfers the phosphoryl group to the FixJ transcriptional activator, thus regulating nif and fix genes expression.