The mycorrhiza-specific ammonium transporter ZmAMT3;1 mediates mycorrhiza-dependent nitrogen uptake in maize roots

Most plant species can form symbioses with arbuscular mycorrhizal fungi (AMFs), which may enhance the host plant's acquisition of soil nutrients. In contrast to phosphorus nutrition, the molecular mechanism of mycorrhizal nitrogen (N) uptake remains largely unknown, and its physiological relevance is unclear. Here, we identified a gene encoding an AMF-inducible ammonium transporter, ZmAMT3;1, in maize (Zea mays) roots. ZmAMT3;1 was specifically expressed in arbuscule-containing cortical cells and the encoded protein was localized at the peri-arbuscular membrane. Functional analysis in yeast and Xenopus oocytes indicated that ZmAMT3;1 mediated high-affinity ammonium transport, with the substrate NH4+ being accessed, but likely translocating uncharged NH3. Phosphorylation of ZmAMT3;1 at the C-terminus suppressed transport activity. Using ZmAMT3;1-RNAi transgenic maize lines grown in compartmented pot experiments, we demonstrated that substantial quantities of N were transferred from AMF to plants, and 68%-74% of this capacity was conferred by ZmAMT3;1. Under field conditions, the ZmAMT3;1-dependent mycorrhizal N pathway contributed >30% of postsilking N uptake. Furthermore, AMFs downregulated ZmAMT1;1a and ZmAMT1;3 protein abundance and transport activities expressed in the root epidermis, suggesting a trade-off between mycorrhizal and direct root N-uptake pathways. Taken together, our results provide a comprehensive understanding of mycorrhiza-dependent N uptake in maize and present a promising approach to improve N-acquisition efficiency via plant-microbe interactions.

Automated summary

This study identified a gene, ZmAMT3;1, in maize roots that plays a crucial role in the uptake of ammonium, enhancing the plant's ability to acquire nitrogen from the soil through symbiotic interactions with arbuscular mycorrhizal fungi (AMFs). The research also revealed that AMFs can regulate the expression and activity of other nitrogen transport proteins in the root epidermis, indicating a trade-off between mycorrhizal and direct root nitrogen uptake pathways.