Abstract
Legumes fix atmospheric nitrogen through a symbiotic relationship with bacteroids in root nodules. Following fixation in pea (Pisum sativum L.) nodules, nitrogen is reduced to amino acids that are exported via the nodule xylem to the shoot, and in the phloem to roots in support of growth. However, the mechanisms involved in amino acid movement towards the nodule vasculature, and their importance for nodule function and plant nutrition, were unknown. We found that in pea nodules the apoplasmic pathway is an essential route for amino acid partitioning from infected cells to the vascular bundles, and that amino acid permease PsAAP6 is a key player in nitrogen retrieval from the apoplasm into inner cortex cells for nodule export. Using an miRNA interference (miR) approach, it was demonstrated that PsAAP6 function in nodules, and probably in roots, and affects both shoot and root nitrogen supply, which were strongly decreased in PsAAP6-miR plants. Further, reduced transporter function resulted in increased nodule levels of ammonium, asparagine, and other amino acids. Surprisingly, nitrogen fixation and nodule metabolism were up-regulated in PsAAP6-miR plants, indicating that under shoot nitrogen deficiency, or when plant nitrogen demand is high, systemic signaling leads to an increase in nodule activity, independent of the nodule nitrogen status.
Highlights
Leguminous plant species are able to access atmospheric dinitrogen (N2) through a symbiotic relationship with Rhizobium bacteria that are housed in unique root structures called nodules
We found that in pea nodules the apoplasmic pathway is an essential route for amino acid partitioning from infected cells to the vascular bundles, and that amino acid permease PsAAP6 is a key player in nitrogen retrieval from the apoplasm into inner cortex cells for nodule export
Results revealed that PsAAP6 is expressed in the uninfected zone of the indeterminate nodule, which is in line with recent tissuespecific transcriptome studies, including AAP6 expression analyses, in Medicago truncatula nodules (Limpens et al, 2013)
Summary
Leguminous plant species are able to access atmospheric dinitrogen (N2) through a symbiotic relationship with Rhizobium bacteria that are housed in unique root structures called nodules. The resulting ammonia is transported across the symbiosome membrane into the infected nodule cells and assimilated to glutamine, asparagine, and other amino acids (Atkins et al, 1982;White et al, 2007). Asparagine, other amino acids, or ureides are exported from the nodule via the xylem to the shoot, or in the phloem to the root for metabolism and growth (Pate et al, 1969, 1979;Atkins et al, 1982;Tegeder, 2014). Temperate legumes, including pea, develop indeterminate nodules in which the uninfected meristem continues to differentiate, forming a cylindrical or coralloid structure
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