LaALMT1 mediates malate release from phosphorus‐deficient white lupin root tips and metal root to shoot translocation

• Published in: Plant, cell and environment cell and environment, 2020-07, Vol.43 (7), p.1691-1706
• Main Authors: Zhou, Yaping, Neuhäuser, Benjamin, Neumann, Günter, Ludewig, Uwe
• Format: Article
• Language: English
• Subjects: Alkaline soils; aluminium; aluminium‐activated malate transporter; Aluminum; Anions; citrate; Citric acid; Clusters; CRISPR; Efflux; electrophysiology; exudation; Gametocytes; Homology; Hydroponics; Lupins; Lupinus - genetics; Lupinus - metabolism; Malate; Malates - metabolism; Membrane Transport Proteins - genetics; Membrane Transport Proteins - metabolism; Meristem - metabolism; Molecular modelling; Oocytes; organic acid; Organic acids; Organic phosphorus; phosphate; Phosphates; Phosphorus; Phosphorus - deficiency; Phylogeny; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Shoots - metabolism; Real-Time Polymerase Chain Reaction; Roots; Sequence Alignment; Soils; Translocation; Xylem; Xylem - metabolism
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.13762

Under phosphorus (P) deficiency, Lupinus albus (white lupin) releases large amounts of organic acid anions from specialized root structures, so‐called cluster or proteoid roots, to mobilize and acquire sparingly soluble phosphates from a restricted soil volume. The molecular mechanisms underlying this release and its regulation are, however, poorly understood. Here, we identified a gene belonging to the aluminium (Al)‐activated malate transporter (ALMT) family that specifically contributes to malate, but not citrate release. This gene, LaALMT1, was most prominently expressed in the root apices under P deficiency, including those of cluster roots and was also detected in the root stele. Contrary to several ALMT homologs in other species, the expression was not stimulated, but moderately repressed by Al. Aluminium‐independent malate currents were recorded from the plasma membrane localized LaALMT1 expressed in Xenopus oocytes. In composite lupins with transgenic roots, LaALMT1 was efficiently mutated by CRISPR‐Cas9, leading to diminished malate efflux and lower xylem sap malate concentrations. When grown in an alkaline P‐deficient soil, mutant shoot phosphate concentrations were similar, but iron and potassium concentrations were diminished in old leaves, suggesting a role for ALMT1 in metal root to shoot translocation, a function that was also supported by growth in hydroponics. White lupin (Lupinus albus) is recognized for its outstanding phosphate mobilization from phosphorus‐deficient soils with cluster roots via organic acid anion release. A root tip‐localized ALMT protein (from the family of aluminium activated malate transporters) specifically releases malate under P‐deficiency from clusters to mobilize phosphate, independent of aluminium. In addition, LaALMT1 also participates in root to shoot translocation of metals, such as iron.