Zinc mediates control of nitrogen fixation via transcription factor filamentation

Jieshun Lin (), Peter K. Bjørk, Marie V. Kolte, Emil Poulsen, Emil Dedic, Taner Drace, Stig U. Andersen, Marcin Nadzieja, Huijun Liu, Hiram Castillo-Michel, Viviana Escudero, Manuel González-Guerrero, Thomas Boesen, Jan Skov Pedersen, Jens Stougaard, Kasper R. Andersen () and Dugald Reid ()
Additional contact information
Jieshun Lin: Aarhus University
Peter K. Bjørk: Aarhus University
Marie V. Kolte: Aarhus University
Emil Poulsen: Aarhus University
Emil Dedic: Aarhus University
Taner Drace: Aarhus University
Stig U. Andersen: Aarhus University
Marcin Nadzieja: Aarhus University
Huijun Liu: Aarhus University
Hiram Castillo-Michel: European Synchrotron Radiation Facility
Viviana Escudero: Universidad Politécnica de Madrid
Manuel González-Guerrero: Universidad Politécnica de Madrid
Thomas Boesen: Aarhus University
Jan Skov Pedersen: Aarhus University
Jens Stougaard: Aarhus University
Kasper R. Andersen: Aarhus University
Dugald Reid: La Trobe University

Nature, 2024, vol. 631, issue 8019, 164-169

Abstract: Abstract Plants adapt to fluctuating environmental conditions by adjusting their metabolism and gene expression to maintain fitness1. In legumes, nitrogen homeostasis is maintained by balancing nitrogen acquired from soil resources with nitrogen fixation by symbiotic bacteria in root nodules2–8. Here we show that zinc, an essential plant micronutrient, acts as an intracellular second messenger that connects environmental changes to transcription factor control of metabolic activity in root nodules. We identify a transcriptional regulator, FIXATION UNDER NITRATE (FUN), which acts as a sensor, with zinc controlling the transition between an inactive filamentous megastructure and an active transcriptional regulator. Lower zinc concentrations in the nodule, which we show occur in response to higher levels of soil nitrate, dissociates the filament and activates FUN. FUN then directly targets multiple pathways to initiate breakdown of the nodule. The zinc-dependent filamentation mechanism thus establishes a concentration readout to adapt nodule function to the environmental nitrogen conditions. In a wider perspective, these results have implications for understanding the roles of metal ions in integration of environmental signals with plant development and optimizing delivery of fixed nitrogen in legume crops.

Date: 2024
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DOI: 10.1038/s41586-024-07607-6

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