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

Nature Plants volume 6, pages 384–393 (2020)Cite this article

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

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

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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.

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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.

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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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  1. These authors contributed equally: Ren-Jie Tang, Fu-Geng Zhao.

Authors and Affiliations

  1. Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA

    Ren-Jie Tang, Chao Wang, Kunlun Li, Thomas J. Kleist, Peggy G. Lemaux & Sheng Luan

  2. Nanjing University–Nanjing Forestry University Joint Institute for Plant Molecular Biology, State Key Laboratory for Pharmaceutical Biotechnology, College of Life Sciences, Nanjing University, Nanjing, China

    Fu-Geng Zhao & Yang Yang

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Contributions

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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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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