Symbiotic competence in Lotus japonicus is affected by plant nitrogen status: transcriptomic identification of genes affected by a new signalling pathway

Abstract

Summary In leguminous plants, symbiotic nitrogen (N) fixation performances and N environmental conditions are linked because nodule initiation, development and functioning are greatly influenced by the amount of available N sources. We demonstrate here that N supply also controls, beforehand, the competence of leguminous plants to perform the nodulation program. Lotus japonicus plants preincubated for 10 d in high‐N conditions, and then transferred to low N before the Mesorhizobium loti inoculation, had reduced nodulation. This phenotype was maintained for at least 6 d and a complete reacquisition of the symbiotic competence was observed only after 9 d. The time‐course analysis of the change of the symbiotic phenotype was analysed by transcriptomics. The differentially expressed genes identified are mostly involved in metabolic pathways. However, the transcriptional response also includes genes belonging to other functional categories such as signalling, stress response and transcriptional regulation. Some of these genes show a molecular identity and a regulation profile, that suggest a role as possible molecular links between the N‐dependent plant response and the nodule organogenesis program.

Asparagine: an amide of particular distinction in the regulation of symbiotic nitrogen fixation of legumes

“…Research using functional genomics approaches has focused on nodule functionality and metabolism under adverse environmental stresses. Comprehensive transcriptomic profilings of nodulated plants grown under stressful conditions have shown a remarkable consistency with previously reported physiological results and given new findings for differential gene expression and functions (Ruffel et al, 2008;Omrane et al, 2009;Ferguson et al, 2010). Thus, genomic approaches represent the current main stream of biotechnological approaches which aim for designing higher efficient tolerant cultivars for stressful environments (Tran & Mochida, 2010;Jogaiah et al, 2012).…”

“…Although several experiments were conducted at both physiological and biochemical levels, the mechanism of sensing N-status in plant cells is not yet fully understood (Ruffel et al, 2008;Omrane et al, 2009;Ferguson et al, 2010). It is generally accepted that these phloem-translocated signals are AAs, which may act as internal sensors for the plant N-status (Parsons et al, 1993;Touraine, 2004;Schubert, 2007).…”

Unexpectedly low nitrogen acquisition and absence of root architecture adaptation to nitrate supply in a Medicago truncatula highly branched root mutant

“…S5 available at JXB online). The higher expression in TR185 of genes involved in flavonoid synthesis support the hypothesis that the mutant was under permanent N starvation, in agreement with previous observations in L. japonicus roots (Omrane et al , 2009). Flavonoid accumulation is known to decrease polar auxin transport, inducing a deregulation of LR elongation and thus short root architecture (Peer et al , 2004; Peer and Murphy, 2007; Laffont et al , 2010).…”

“…Most of the genes involved in cell-wall degradation were upregulated in TR185 compared with WT, whereas those involved in cell-wall synthesis were downregulated. Such modifications have been previously observed for Lotus japonicus in N-starvation conditions (Omrane et al , 2009). Most of the transcripts encoding cell-wall arabinogalactan proteins were downregulated in TR185, in agreement with the reduced root elongation observed in Arabidopsis AGP-defective mutants (van Hengel and Roberts, 2002; Shi et al , 2003; Seifert and Roberts, 2007).…”

“…Transcriptomic analyses have confirmed that many genes involved in N assimilation or C primary metabolism are responsive to variation of nitrate supply (Wang et al , 2003; Scheible et al , 2004; Bi et al , 2007). Transcriptomic studies of legumes subjected to variation in nitrate supply are consistent with those obtained in Arabidopsis (Ruffel et al , 2008; Omrane et al , 2009). …”