Root zone–specific localization of AMTs determines ammonium transport pathways and nitrogen allocation to shoots

Abstract

In plants, nutrient provision of shoots depends on the uptake and transport of nutrients across the root tissue to the vascular system. Nutrient delivery to the vasculature is mediated via the apoplastic transport pathway (ATP), which uses the free space in the cell walls and is controlled by apoplastic barriers and nutrient transporters at the endodermis, or via the symplastic transport pathway (STP). However, the relative importance of these transport routes remains elusive. Here, we show that the STP, mediated by the epidermal ammonium transporter 1;3 (AMT1;3), dominates the radial movement of ammonium across the root tissue when external ammonium is low, whereas apoplastic transport controlled by AMT1;2 at the endodermis prevails at high external ammonium. Then, AMT1;2 favors nitrogen (N) allocation to the shoot, revealing a major importance of the ATP for nutrient partitioning to shoots. When an endodermal bypass was introduced by abolishing Casparian strip (CS) formation, apoplastic ammonium transport decreased. By contrast, symplastic transport was increased, indicating synergism between the STP and the endodermal bypass. We further establish that the formation of apoplastic barriers alters the cell type–specific localization of AMTs and determines STP and ATP contributions. These results show how radial transport pathways vary along the longitudinal gradient of the root axis and contribute to nutrient partitioning between roots and shoots.

Ammonium Transporter (BcAMT1.2) Mediates the Interaction of Ammonium and Nitrate in Brassica campestris

“…When external NH 4 + is high, apoplastic transport mediated by AtAMT1.2 prevails at the root endodermis (Yuan et al, 2007;Duan et al, 2018). AtAMT1.2 exclusively regulates NH 4 + flux into the vasculature (Yuan et al, 2007;Straub et al, 2017) and favors N allocation to the shoot (Duan et al, 2018). BcAMT1.2 pro ::GUS activity, which was expressed mainly in the vascular tissues in Arabidopsis, was enhanced by adding NH 4 + or NO 3 compared with that in Ndeficiency ( Figures 6A-F).…”

“…In Arabidopsis, AtAMT1.1, AtAMT1.3, and AtAMT1.5 are located in rhizodermal cells, and AtAMT1.2 is located in root endodermal and cortical cells (Yuan et al, 2007). Specific localization in the root zone of AMTs determines the pathways of NH 4 + uptake, transport and allocation to shoots (Duan et al, 2018). When external NH 4 + is high, apoplastic transport mediated by AtAMT1.2 prevails at the root endodermis (Yuan et al, 2007;Duan et al, 2018).…”

“…Specific localization in the root zone of AMTs determines the pathways of NH 4 + uptake, transport and allocation to shoots (Duan et al, 2018). When external NH 4 + is high, apoplastic transport mediated by AtAMT1.2 prevails at the root endodermis (Yuan et al, 2007;Duan et al, 2018). AtAMT1.2 exclusively regulates NH 4 + flux into the vasculature (Yuan et al, 2007;Straub et al, 2017) and favors N allocation to the shoot (Duan et al, 2018).…”

Exodermis and Endodermis Respond to Nutrient Deficiency in Nutrient-Specific and Localized Manner

“…Plants are sessile organisms and their fitness is related to their high developmental plasticity and their ability to adjust resource acquisition to local conditions. Root system architecture, branching to nutrient-rich patches, chemical modifications of the rhizosphere, interaction with microorganisms, and engagement of transporters of different parameters, e.g., affinity, are among the most important mechanisms of effective nutrient uptake from a heterogeneous soil environment [27,[32][33][34]. One piece of the nutrient acquisition puzzle is the apoplastic barriers in roots.…”

“…[24][25][26]. The distribution of root membrane transporters fine tunes nutrient acquisition and balances the apoplastic and symplastic transport pathways [25,27]. Nutrient uptake and radial transport are thus precisely optimised across changing nutrient availability by combining fast delivery of nutrients to vascular tissues under non-limiting conditions with the effective nutrient acquisition under limiting conditions [27].…”