The nitrate‐reduction gene cluster components exert lineage‐dependent contributions to optimization of Sinorhizobium symbiosis with soybeans

Abstract

Receiving nodulation and nitrogen fixation genes does not guarantee rhizobia an effective symbiosis with legumes. Here, variations in gene content were determined for three Sinorhizobium species showing contrasting symbiotic efficiency on soybeans. A nitrate-reduction gene cluster absent in S. sojae was found to be essential for symbiotic adaptations of S. fredii and S. sp. III. In S. fredii, the deletion mutation of the nap (nitrate reductase), instead of nir (nitrite reductase) and nor (nitric oxide reductase), led to defects in nitrogen-fixation (Fix ). By contrast, none of these core nitrate-reduction genes were required for the symbiosis of S. sp. III. However, within the same gene cluster, the deletion of hemN1 (encoding oxygen-independent coproporphyrinogen III oxidase) in both S. fredii and S. sp. III led to the formation of nitrogen-fixing (Fix ) but ineffective (Eff ) nodules. These Fix /Eff nodules were characterized by significantly lower enzyme activity of glutamine synthetase indicating rhizobial modulation of nitrogen-assimilation by plants. A distant homologue of HemN1 from S. sojae can complement this defect in S. fredii and S. sp. III, but exhibited a more pleotropic role in symbiosis establishment. These findings highlighted the lineage-dependent optimization of symbiotic functions in different rhizobial species associated with the same host.

Coordinated Regulation of the Size and Number of Polyhydroxybutyrate Granules by Core and Accessory Phasins in the Facultative Microsymbiont Sinorhizobium fredii NGR234

“…This Fix ϩ Eff Ϫ phenotype has also been reported for a glnD mutant of Rm1021 (47) and hemN1 mutants of S. fredii CCBAU45436 and Sinorhizobium sp. CCBAU05631 nodulating wild soybean (48). In this study, V. unguiculata plants inoculated with the ΔphaP1P2 or ΔphaP2P3 mutant of NGR234 exhibited slight but nonsignificant reduction in shoot dry weight compared to that of plants inoculated with the wild-type strain.…”

Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery

“…The regulation mechanisms of nodulation and T3SS genes by zinc homeostasis during the establishment of symbiosis remain elusive, considering that around one-third of the genome can be differentially expressed under zinc starvation conditions. In contrast to the elite strain S. fredii CCBAU45436, more severe defects in nodulation were observed for the znuA mutant of Sinorhizobium strains that harbor an incomplete set of c06450, zip1, and zip2 in their genomes and are characterized by their limited symbiotic host range and geographical distribution patterns (24)(25)(26)(54)(55)(56). These findings imply that accessory components in zinc starvation machinery may contribute to the modulation of nutrient immunity and ecological success of rhizobia.…”

“…The rhizobium-legume symbiosis is a model system of mutualistic interactions between bacteria and eukaryotes and has global impacts on the nitrogen cycle due to its ability to reduce atmospheric nitrogen into ammonium. Rhizobia need key symbiosis genes (nod, nif, and fix) to form nitrogen-fixing nodules on legumes, though diverse core and accessory functions are also required for optimizing the compatibility and efficiency of rhizobial interactions with legumes (22)(23)(24)(25)(26). It was recently reported that znuABC genes of a broad-host-range strain Sinorhizobium fredii CCBAU45436 were upregulated in nodules of cultivated soybean (Glycine max) and wild soybean (Glycine soja) compared to those in free-living rhizobial cells in rich medium (26,27), implying that the nodule is a zinc-limiting condition for rhizobia.…”

Multidisciplinary approaches for studying rhizobium–legume symbioses

“…Others have shown that relatively small differences between rhizobial genomes can result in significant variations in symbiotic ability (Jozefkowicz et al 2017). Additionally, studies have highlighted rhizobial lineage-specific adaptations to symbiosis (Tian et al 2012;L.X. Liu et al 2017) and have identified rhizobial genes blocking symbiosis in a plant-cultivarspecific manner (Crook et al 2012;Price et al 2015;Nguyen et al 2017).…”