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; Dugald Reid

doi:10.1038/s41586-024-07607-6

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, Dugald Reid

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

Plants adapt to fluctuating environmental conditions by adjusting their metabolism and gene expression to maintain fitness 1. In legumes, nitrogen homeostasis is maintained by balancing nitrogen acquired from soil resources with nitrogen fixation by symbiotic bacteria in root nodules 2-8. 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.

Original language	English
Journal	Nature
Volume	631
Issue	8019
Pages (from-to)	164-169
Number of pages	6
ISSN	0028-0836
DOIs	https://doi.org/10.1038/s41586-024-07607-6
Publication status	Published - 4 Jul 2024

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Lin, J., Bjørk, P. K., Kolte, M. V., Poulsen, E., Dedic, E., Drace, T., Andersen, S. U., Nadzieja, M., Liu, H., Castillo-Michel, H., Escudero, V., González-Guerrero, M., Boesen, T., Pedersen, J. S., Stougaard, J., Andersen, K. R., & Reid, D. (2024). Zinc mediates control of nitrogen fixation via transcription factor filamentation. Nature, 631(8019), 164-169. https://doi.org/10.1038/s41586-024-07607-6

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title = "Zinc mediates control of nitrogen fixation via transcription factor filamentation",

abstract = "Plants adapt to fluctuating environmental conditions by adjusting their metabolism and gene expression to maintain fitness 1. In legumes, nitrogen homeostasis is maintained by balancing nitrogen acquired from soil resources with nitrogen fixation by symbiotic bacteria in root nodules 2-8. 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. ",

author = "Jieshun Lin and Bj{\o}rk, {Peter K} and Kolte, {Marie V} and Emil Poulsen and Emil Dedic and Taner Drace and Andersen, {Stig U} and Marcin Nadzieja and Huijun Liu and Hiram Castillo-Michel and Viviana Escudero and Manuel Gonz{\'a}lez-Guerrero and Thomas Boesen and Pedersen, {Jan Skov} and Jens Stougaard and Andersen, {Kasper R} and Dugald Reid",

note = "{\textcopyright} 2024. The Author(s).",

year = "2024",

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doi = "10.1038/s41586-024-07607-6",

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Lin, J, Bjørk, PK, Kolte, MV , Poulsen, E , Dedic, E , Drace, T , Andersen, SU , Nadzieja, M , Liu, H, Castillo-Michel, H, Escudero, V, González-Guerrero, M, Boesen, T , Pedersen, JS , Stougaard, J, Andersen, KR & Reid, D 2024, 'Zinc mediates control of nitrogen fixation via transcription factor filamentation', Nature, vol. 631, no. 8019, pp. 164-169. https://doi.org/10.1038/s41586-024-07607-6

TY - JOUR

T1 - Zinc mediates control of nitrogen fixation via transcription factor filamentation

AU - Lin, Jieshun

AU - Bjørk, Peter K

AU - Kolte, Marie V

AU - Poulsen, Emil

AU - Dedic, Emil

AU - Drace, Taner

AU - Andersen, Stig U

AU - Nadzieja, Marcin

AU - Liu, Huijun

AU - Castillo-Michel, Hiram

AU - Escudero, Viviana

AU - González-Guerrero, Manuel

AU - Boesen, Thomas

AU - Pedersen, Jan Skov

AU - Stougaard, Jens

AU - Andersen, Kasper R

AU - Reid, Dugald

PY - 2024/7/4

Y1 - 2024/7/4

N2 - Plants adapt to fluctuating environmental conditions by adjusting their metabolism and gene expression to maintain fitness 1. In legumes, nitrogen homeostasis is maintained by balancing nitrogen acquired from soil resources with nitrogen fixation by symbiotic bacteria in root nodules 2-8. 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.

AB - Plants adapt to fluctuating environmental conditions by adjusting their metabolism and gene expression to maintain fitness 1. In legumes, nitrogen homeostasis is maintained by balancing nitrogen acquired from soil resources with nitrogen fixation by symbiotic bacteria in root nodules 2-8. 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.

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U2 - 10.1038/s41586-024-07607-6

DO - 10.1038/s41586-024-07607-6

M3 - Journal article

C2 - 38926580

SN - 0028-0836

VL - 631

SP - 164

EP - 169

JO - Nature

JF - Nature

IS - 8019

ER -

Zinc mediates control of nitrogen fixation via transcription factor filamentation

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