Tonoplast-localized transporter ZmNRAMP2 confers root-to-shoot translocation of manganese in maize

Almost all living organisms require manganese (Mn) as an essential trace element for survival. To maintain an irreplaceable role in the oxygen-evolving complex of photosynthesis, plants require efficient Mn uptake in roots and delivery to above-ground tissues. However, the underlying mechanisms of root-to-shoot Mn translocation remain unclear. Here, we identified an Natural Resistance Associated Macrophage Protein (NRAMP) family member in maize (Zea mays), ZmNRAMP2, which localized to the tonoplast in maize protoplasts and mediated transport of Mn in yeast (Saccharomyces cerevisiae). Under Mn deficiency, two maize mutants defective in ZmNRAMP2 exhibited remarkable reduction of root-to-shoot Mn translocation along with lower shoot Mn contents, resulting in substantial decreases in F-v/F-m and plant growth inhibition compared to their corresponding wild-type (WT) plants. ZmNRAMP2 transcripts were highly expressed in xylem parenchyma cells of the root stele. Compared to the WT, the zmnramp2-1 mutant displayed lower Mn concentration in xylem sap accompanied with retention of Mn in root stele. Furthermore, the overexpression of ZmNRAMP2 in transgenic maize showed enhanced root-to-shoot translocation of Mn and improved tolerance to Mn deficiency. Taken together, our study reveals a crucial role of ZmNRAMP2 in root-to-shoot translocation of Mn via accelerating vacuolar Mn release in xylem parenchyma cells for adaption of maize plants to low Mn stress and provides a promising transgenic approach to develop low Mn-tolerant crop cultivars. A tonoplast-localized transporter enables root-to-shoot manganese translocation via mediating vacuolar manganese release of root stellar cells and contributes to low manganese tolerance in maize.

Automated summary

This study identified the protein ZmNRAMP2, which plays a crucial role in root-to-shoot manganese translocation in maize plants. Mutants lacking the ZmNRAMP2 gene showed reduced manganese translocation and inhibited plant growth under manganese deficiency. In contrast, transgenic maize overexpressing ZmNRAMP2 exhibited enhanced manganese translocation and improved tolerance to manganese deficiency. This research provides a promising transgenic approach for developing crop cultivars with increased tolerance to low manganese conditions.