Abstract
In symbiotic root nodules of legumes, terminally differentiated rhizobia fix atmospheric N2 producing an NH4+ influx that is assimilated by the plant. The plant, in return, provides photosynthates that fuel the symbiotic nitrogen acquisition. Mechanisms responsible for the adjustment of the symbiotic capacity to the plant N demand remain poorly understood. We have investigated the role of systemic signaling of whole-plant N demand on the mature N2-fixing nodules of the model symbiotic association Medicago truncatula/Sinorhizobium using split-root systems. The whole-plant N-satiety signaling rapidly triggers reductions of both N2 fixation and allocation of sugars to the nodule. These responses are associated with the induction of nodule senescence and the activation of plant defenses against microbes, as well as variations in sugars transport and nodule metabolism. The whole-plant N-deficit responses mirror these changes: a rapid increase of sucrose allocation in response to N-deficit is associated with a stimulation of nodule functioning and development resulting in nodule expansion in the long term. Physiological, transcriptomic, and metabolomic data together provide evidence for strong integration of symbiotic nodules into whole-plant nitrogen demand by systemic signaling and suggest roles for sugar allocation and hormones in the signaling mechanisms.
Highlights
A hallmark trait of legumes is to form nodules with soil bacteria called rhizobia.The symbiotic root organs allow the plant to acquire nitrogen (N) from the air
This study shows that the whole-plant N status triggers systemic signaling impacting mature nodule functioning and development associated with massive metabolic changes and transcriptome reprogramming(s)
The whole-plant N-satiety treatment results in the systemic repression of symbiotic N2 fixation (SNF). This down-regulation occurs within hours after providing a high level of mineral N to the treated side of the split-root system (Fig. 2) and is correlated with the systemic activation of the senescence of the N2-fixing bacteroids (Fig. 3). These responses correlate with the down-regulation of the leghemoglobin gene family, several transcripts involved in ammonium assimilation, as well as in the rapid up-regulation of the transcripts encoding nodule cysteine proteases and many other plant proteins involved in nodule senescence, including the MtNAC969 transcription factor
Summary
A hallmark trait of legumes is to form nodules with soil bacteria called rhizobia.The symbiotic root organs allow the plant to acquire nitrogen (N) from the air. The anaplerotic ‘γ-aminobutyric acid (GABA) shunt’ involving pyruvate and GABA (most probably provided by the plant) has been proposed to bypass two steps of the TCA cycle by producing succinate semialdehyde, alanine, and succinate (Prell et al, 2009). This pathway might enhance energy generation under hypoxic conditions and, might improve the efficiency of SNF (Prell et al, 2009; Sulieman and Schulze, 2010; Sulieman, 2011)
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