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

PLoS Biol. 2018 Oct 24;16(10):e2006024. doi: 10.1371/journal.pbio.2006024. eCollection 2018 Oct.

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.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Ammonium Compounds / metabolism*
  • Arabidopsis / physiology
  • Arabidopsis Proteins / physiology
  • Biological Transport / physiology
  • Cation Transport Proteins / metabolism
  • Cation Transport Proteins / physiology*
  • Cell Wall
  • Gene Expression Regulation, Plant / genetics
  • Ion Transport / physiology
  • Membrane Transport Proteins / physiology
  • Nitrogen / metabolism
  • Plant Proteins / metabolism
  • Plant Proteins / physiology*
  • Plant Roots / metabolism*
  • Plant Roots / physiology

Substances

  • Ammonium Compounds
  • Arabidopsis Proteins
  • Cation Transport Proteins
  • Membrane Transport Proteins
  • Plant Proteins
  • ammonium transporters, plant
  • Nitrogen

Grants and funding

Deutsche Forschungsgemeinschaft www.dfg.de (grant number WI1728/18-1). ERA-CAPS Programme. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.