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A calcium signalling network activates vacuolar K+ remobilization to enable plant adaptation to low-K environments

An Author Correction to this article was published on 22 January 2021

An Author Correction to this article was published on 19 May 2020

This article has been updated

Abstract

Potassium (K) is an essential nutrient, but levels of the free K ions (K+) in soil are often limiting, imposing a constant stress on plants. We have discovered a calcium (Ca2+)-dependent signalling network, consisting of two calcineurin B-like (CBL) Ca2+ sensors and a quartet of CBL-interacting protein kinases (CIPKs), which plays a key role in plant response to K+ starvation. The mutant plants lacking two CBLs (CBL2 and CBL3) were severely stunted under low-K conditions. Interestingly, the cbl2 cbl3 mutant was normal in K+ uptake but impaired in K+ remobilization from vacuoles. Four CIPKs—CIPK3, 9, 23 and 26—were identified as partners of CBL2 and CBL3 that together regulate K+ homeostasis through activating vacuolar K+ efflux to the cytoplasm. The vacuolar two-pore K+ (TPK) channels were directly activated by the vacuolar CBL–CIPK modules in a Ca2+-dependent manner, presenting a mechanism for the activation of vacuolar K+ remobilization that plays an important role in plant adaptation to K+ deficiency.

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Fig. 1: How cbl2 cbl3 mutant plants are hypersensitive to external K+ deficiency.
Fig. 2: K content in the cbl2 cbl3 mutant.
Fig. 3: A quartet of CIPKs functions downstream of CBL2/3 in plant adaptation to low-K conditions.
Fig. 4: Reduced vacuolar K+ inward current in various cbl and cipk mutants.
Fig. 5: Reconstitution of the vacuolar K+ efflux pathway consisting of TPK channels and CBL–CIPK modules.
Fig. 6: A working model depicting dual CBL–CIPK pathways in plant low-K response.

Data availability

All the data supporting the findings of this study are available within the article and its Supplementary Information files or from the corresponding author upon reasonable request.

Change history

  • 19 May 2020

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

  • 22 January 2021

    A Correction to this paper has been published: https://doi.org/10.1038/s41477-021-00857-6

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Acknowledgements

We thank the Arabidopsis Biological Resource Center for providing Arabidopsis thaliana seed stocks. This work was supported by the National Science Foundation (grant nos. MCB-1714795 and ISO-1339239 to S.L.), the Innovative Genomics Institute of the University of California (to S.L.) and the National Natural Science Foundation of China (grant no. 31770266 to F.-G.Z.). C.W. is sponsored by the Tang Distinguished Scholarship of the University of California at Berkeley.

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R.-J.T. and S.L. conceived and designed the experiments. R.-J.T. performed most of the molecular, genetic and physiological experiments. F.-G.Z. conducted the electrophysiological experiments. Y.Y., C.W. and K.L. assisted in some of the molecular experiments and subcellular localization. T.J.K. and P.G.L. provided some tools and reagents. R.-J.T. and S.L. wrote the manuscript. All the authors discussed the results and commented on the manuscripts.

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Correspondence to Sheng Luan.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Ingo Dreyer, Enrico Martinoia and the other, anonymous, reviewer for their contribution to the peer review of this work.

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Tang, RJ., Zhao, FG., Yang, Y. et al. A calcium signalling network activates vacuolar K+ remobilization to enable plant adaptation to low-K environments. Nat. Plants 6, 384–393 (2020). https://doi.org/10.1038/s41477-020-0621-7

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