Abstract
Bradyrhizobium diazoefficiens is a nitrogen-fixing endosymbiont, which can grow inside root-nodule cells of the agriculturally important soybean and other host plants. Our previous studies described B. diazoefficiens host-specific global expression changes occurring during legume infection at the transcript and protein level. In order to further characterize nodule metabolism, we here determine by flow injection–time-of-flight mass spectrometry analysis the metabolome of (i) nodules and roots from four different B. diazoefficiens host plants; (ii) soybean nodules harvested at different time points during nodule development; and (iii) soybean nodules infected by two strains mutated in key genes for nitrogen fixation, respectively. Ribose (soybean), tartaric acid (mungbean), hydroxybutanoyloxybutanoate (siratro) and catechol (cowpea) were among the metabolites found to be specifically elevated in one of the respective host plants. While the level of C4-dicarboxylic acids decreased during soybean nodule development, we observed an accumulation of trehalose-phosphate at 21 days post infection (dpi). Moreover, nodules from non-nitrogen-fixing bacteroids (nifA and nifH mutants) showed specific metabolic alterations; these were also supported by independent transcriptomics data. The alterations included signs of nitrogen limitation in both mutants, and an increased level of a phytoalexin in nodules induced by the nifA mutant, suggesting that the tissue of these nodules exhibits defense and stress reactions.
Highlights
IntroductionBradyrhizobium diazoefficiens (previously named Bradyrhizobium japonicum) is an α-proteobacterium able to undergo nitrogen-fixing symbiosis in determinate root nodules of several legumes including Glycine max (soybean), Macroptilium atropurpureum (siratro), Vigna unguiculata (cowpea) and Vigna radiata (mungbean) [1]
Bradyrhizobium diazoefficiens is an α-proteobacterium able to undergo nitrogen-fixing symbiosis in determinate root nodules of several legumes including Glycine max, Macroptilium atropurpureum, Vigna unguiculata and Vigna radiata [1]
Metabolites were extracted from soybean, cowpea and mungbean root nodules infected by B. diazoefficiens at 21 dpi, and from siratro nodules at 31dpi (Table 1)
Summary
Bradyrhizobium diazoefficiens (previously named Bradyrhizobium japonicum) is an α-proteobacterium able to undergo nitrogen-fixing symbiosis in determinate root nodules of several legumes including Glycine max (soybean), Macroptilium atropurpureum (siratro), Vigna unguiculata (cowpea) and Vigna radiata (mungbean) [1]. The establishment of a successful symbiotic interaction is coordinated by both partners and results in the formation of a root nodule structure that contains millions of intracellular, nitrogen-fixing bacteroids [2,3,4,5,6,7]. Nod gene products are responsible for the synthesis of lipochitooligosaccharides (Nod factors) that induce root hair curling, which helps to trap the rhizobia, and a massive subcortical cell division in the plant. Rhizobia usually enter the root hair through infection threads (IT), tubular structures formed by the plant. The continued plant and bacterial cell division leads to a mature root nodule structure that requires a constant integration of plant and bacterial metabolism to efficiently fix atmospheric nitrogen [5,10,11,12]. Atmospheric nitrogen is reduced to ammonium, which is incorporated into ureides in determinate nodules, or into glutamine and asparagine in indeterminate nodules before being exported from nodules to the plant to be further metabolized [10,15,16,17]
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