Identification of a unique ZIP transporter involved in zinc uptake via the arbuscular mycorrhizal fungal pathway

Abstract

Low soil zinc (Zn) availability is a limiting factor for crop yield, and increasing Zn content is a major target for the biofortification of major crops. Arbuscular mycorrhizal (AM) fungi associate with the roots of most terrestrial plant species and improve the host plants growth and nutrition through the mycorrhizal pathway of nutrient uptake. Although the physiology of Zn uptake through the mycorrhizal pathway is well established, the identity of the molecular components responsible for Zn transport in the mycorrhizal pathway are unknown. RNA-seq analysis identified the putative Zn transporter gene MtZIP14 by its marked up-regulation in Medicago truncatula roots when colonised by the AM fungus Rhizophagus irregularis under varying soil Zn supply. Expression of GFP-tagged MtZIP14 in roots revealed that it is exclusively localised to the site of plant-fungal nutrient exchange in cortical cells, the peri-arbuscular membrane. Expression of MtZIP14 in a yeast mutant lacking Zn transport function restored growth under low Zn availability. M. truncatula MtZIP14 loss-of-function mutants had reduced shoot biomass compared to the wild-type when colonised by AM fungi and grown under low Zn. Vesicular and arbuscular colonisation, but not hyphal colonisation, were also lower in mtzip14 mutant plants. Based on these results we propose that MtZIP14 plays a key role in the transport of Zn from AM fungus to plant across the peri-arbuscular membrane, and MtZIP14 function is crucial to plant competitiveness in a low Zn soil. Significance statementMajority of crop plant species associate with arbuscular mycorrhizal fungi, which can increase plant nutrient uptake. Improving our knowledge of how Zn is taken up in mycorrhizal plants will lead to improved plant and human Zn nutrition outcomes. Here, we report a novel plant transporter with a major role in Zn nutrition of mycorrhizal plants. MtZIP14 is involved in Zn transport, is exclusively localised to the specialised plant-fungal interface in roots, and impairment of MtZIP14 gene function results in negative impacts on both plant growth and Zn nutrition.