open access publication

Article, 2024

Zinc mediates control of nitrogen fixation via transcription factor filamentation

Nature, ISSN 0028-0836, 1476-4687, Volume 631, 8019, Pages 164-169, 10.1038/s41586-024-07607-6

Contributors

Lin, Jie-Shun 0000-0002-3726-0303 (Corresponding author) [1] Bjørk, Peter Klemmed 0000-0002-5641-7791 [1] Kolte, Marie V 0000-0001-6997-3888 [1] Poulsen, Emil [1] Dedic, Emil 0000-0003-1372-4932 [1] Drace, Taner [1] Andersen, Stig Uggerhøj 0000-0002-1096-1468 [1] Nadzieja, Marcin 0000-0002-6643-8019 [1] Liu, Huijun 0000-0002-8605-619X [1] Castillo-Michel, Hiram A [2] Escudero, Viviana 0000-0002-3506-9054 [3] González-Guerrero, Manuel 0000-0001-7334-5286 [3] [4] Boesen, Thomas 0000-0002-5633-6844 [1] Pedersen, Jan Skov [1] Stougaard, Jens 0000-0002-9312-2685 [1] Andersen, Kasper Røjkjaer 0000-0002-4415-8067 (Corresponding author) [1] Reid, Dugald E 0000-0001-9291-9775 (Corresponding author) [5]

Affiliations

  1. [1] Aarhus University
    2. [NORA names: AU Aarhus University; University; Denmark; Europe, EU; Nordic; OECD];
  2. [2] European Synchrotron Radiation Facility
    3. [NORA names: France; Europe, EU; OECD];
  3. [3] Centre for Plant Biotechnology and Genomics
    4. [NORA names: Spain; Europe, EU; OECD];
  4. [4] Technical University of Madrid
    5. [NORA names: Spain; Europe, EU; OECD];
  5. [5] La Trobe University
    6. [NORA names: Australia; Oceania; OECD]

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.

Keywords

activity, bacteria, balance nitrogen, breakdown, concentration, concentration readout, conditions, control, control of nitrogen fixation, crop, development, environmental conditions, environmental signals, expression, factor control, filament mechanism, filaments, fitness1, fixation, fixed nitrogen, function, gene expression, genes, higher levels, homeostasis, initial breakdown, integration, integration of environmental signals, intracellular second messengers, ions, legume crops, legumes, levels, low zinc concentrations, mechanism, megastructures, messenger, metabolic activity, metabolism, metal, metal ions, micronutrients, multiple pathways, nitrate, nitrogen, nitrogen conditions, nitrogen fixation, nitrogen homeostasis, nodule function, nodules, optimal delivery, pathway, perspective, plant development, plant micronutrient, plants, readout, regulation, resources, response, response to high levels, results, root, root nodules, second messengers, sensor, signal, soil, soil nitrate, soil resources, symbiotic bacteria, target multiple pathways, transcription, transcription factor control, transcriptional regulation, transition, zinc, zinc concentrations

Funders

  • European Research Council
  • Carlsberg Foundation
  • Bill & Melinda Gates Foundation
  • European Synchrotron Radiation Facility
  • European Commission

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