Wheat roots efflux a diverse array of organic N compounds and are highly proficient at their recapture

Abstract

Background & aims Small organic N compounds could contribute to N nutrition, but an alternative view is that root uptake may serve to recapture compounds that efflux out of roots. However, it is unclear if plants can recapture leaked organic N compounds because no studies have examined quantitative relationships between efflux and uptake at sub-micromolar concentrations. Methods This study examines efflux and uptake of a broad suite of small organic N compounds by wheat (Triticum aestivum L.).15 N-labeling and capillary electrophoresis-mass spectrometry were used to estimate efflux and uptake. Results One hundred and ten organic N compounds were detected in exudates. Amino acids were abundant but accounted for less than half of organic N. Other abundant compound classes were amines and polyamines, quaternary ammonium compounds, nucleobases and nucleosides. Uptake occurred simultaneously with efflux for all 45 compounds for which rates of efflux could be reliably determined, even though concentrations were 0.01 to 0.5 μM.Conclusions These findings indicate that wheat is highly proficient at recapturing much of the diverse array of organic N compounds in root exudates. The ability to salvage effluxed compounds present at very low concentrations means that wheat might also be able to take up organic N compounds from the soil solution.

Simultaneous efflux and uptake of metabolites by roots of wheat

“…Many metabolites (defined here as organic compounds less than 1000 Da) have been reported from root exudates including sugars, amino acids, organic acids, lipids, phenolics and other secondary metabolites (Flores et al 1999;Dakora and Phillips 2002;Jones et al 2003;Read et al 2003;Walker et al 2003;Badri and Vivanco 2009;Chaparro et al 2013;Strehmel et al 2014), and high molecular weight metabolites such as polysaccharides and proteins (Walker et al 2003). In recent years the application of untargeted mass spectrometry-based methods has built on previous work and uncovered an even larger number and diversity of metabolites in root exudates (Strehmel et al 2014;Warren 2015). For example, capillary electrophoresismass spectrometry of exudates of wheat detected 110 organic N metabolites and found that while amino acids were abundant, they accounted for less than half of the organic N in root exudates (Warren 2015).…”

“…In recent years the application of untargeted mass spectrometry-based methods has built on previous work and uncovered an even larger number and diversity of metabolites in root exudates (Strehmel et al 2014;Warren 2015). For example, capillary electrophoresismass spectrometry of exudates of wheat detected 110 organic N metabolites and found that while amino acids were abundant, they accounted for less than half of the organic N in root exudates (Warren 2015). These recent studies have identified an impressive number of metabolites, but have not been especially comprehensive.…”

“…These recent studies have identified an impressive number of metabolites, but have not been especially comprehensive. For example, the capillary electrophoresis-mass spectrometry used to examine exudates in wheat could detect only organic N metabolites that were cationic at low pH (Warren 2015), while the liquid chromatography-mass spectrometry method used to examine exudates of Arabidopsis could not examine highly hydrophilic metabolites (Strehmel et al 2014).…”

“…Plants would appear to have a well-developed ability to re-capture small N-containing metabolites such as amino acids (Phillips et al 2004(Phillips et al , 2006. The ability to salvage effluxed N-containing metabolites at micromolar or smaller concentrations (Warren 2015) means that plants may also have a more general capacity to take up Ncontaining metabolites from the soil solution. Several studies have shown passive efflux and active uptake of sugars by roots (Jones and Darrah 1996;Sacchi et al 2000;Stubbs et al 2004); however, it was suggested the role of exogenous sugar uptake would be of little ecological significance in photosynthetic plants owing to the low soil solution concentrations of mono-and disaccharides (Jones et al 2004).…”

“…For example, it remains unclear if the ability to take up organic metabolites extends to the re-capture of the highly dilute metabolites effluxed from roots (Warren 2015). An additional challenge is that past studies targeted one metabolite class (e.g., amino acids, or sugars, or organic acids) rather than the breadth of metabolite classes present in exudates.…”