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Ammonium regulates Fe deficiency responses by enhancing nitric oxide signaling in Arabidopsis thaliana

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Abstract

Main conclusion

The accumulation of NH4+ in response to Fe deficiency plays a role not only in the remobilization of Fe from the root cell wall, but also in the transportation of Fe from root to shoot.

Abstract

Ammonium (NH4+) plays an important role in phosphorus-deficiency responses in rice, but its role in responses to Fe deficiency remains unknown. Here, we demonstrate that the accumulation of NH4+ plays a pivotal role when Arabidopsis thaliana plants are subject to Fe deficiency. The Arabidopsis amt1-3 mutant, which is defective in endogenous NH4+ sensing, exhibited increased sensitivity to Fe deficiency compared to WT (wild type; Col-0). In addition, exogenous application of NH4+ significantly alleviated Fe deficiency symptoms in plants. NH4+ triggers the production of nitric oxide (NO), which then induces ferric-chelate reductase (FCR) activity and accelerates the release of Fe from the cell wall, especially hemicellulose, thereby increasing the availability of soluble Fe in roots. NH4+ also increases soluble Fe levels in shoots by upregulating genes involved in Fe translocation, such as FRD3 (FERRIC REDUCTASE DEFECTIVE3) and NAS1 (NICOTIANAMINE SYNTHASE1), hence, alleviating leaf chlorosis. Overall, NH4+ plays an important role in the reutilization of Fe from the cell wall and the redistribution of Fe from root to shoot in Fe-deficient Arabidopsis, a process dependent on NO accumulation.

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Abbreviations

DCCD:

N,N′-Dicyclohexylcarbodiimide

FCR:

Ferric-chelate reductase

NO:

Nitric oxide

SPAD:

Soil plant analysis development

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Acknowledgements

This work was funded by the Youth Innovation Promotion Association of CAS (2015250), the National Key Basic Research Program of China (no. 2014CB441000), and ‘Strategic Priority Research Program’ of the Chinese Academy of Sciences (nos. XDB15030302 and XDB15030202). Thanks are also given to the two anonymous reviewers for their valuable comments to improve the quality of our work.

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Authors and Affiliations

  1. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Xiao Fang Zhu, Xiao Ying Dong, Qi Wu & Ren Fang Shen

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Qi Wu & Ren Fang Shen

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  1. Xiao Fang Zhu
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Correspondence to Ren Fang Shen.

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Zhu, X.F., Dong, X.Y., Wu, Q. et al. Ammonium regulates Fe deficiency responses by enhancing nitric oxide signaling in Arabidopsis thaliana. Planta 250, 1089–1102 (2019). https://doi.org/10.1007/s00425-019-03202-6

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