Letter | Published:

OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis

Nature volume 514, pages 367371 (16 October 2014) | Download Citation

  • A Corrigendum to this article was published on 25 February 2015

Abstract

Water is crucial to plant growth and development. Environmental water deficiency triggers an osmotic stress signalling cascade, which induces short-term cellular responses to reduce water loss and long-term responses to remodel the transcriptional network and physiological and developmental processes1,2,3,4. Several signalling components that have been identified by extensive genetic screens for altered sensitivities to osmotic stress seem to function downstream of the perception of osmotic stress. It is known that hyperosmolality and various other stimuli trigger increases in cytosolic free calcium concentration ([Ca2+]i)5,6. Considering that in bacteria and animals osmosensing Ca2+ channels serve as osmosensors7,8, hyperosmolality-induced [Ca2+]i increases have been widely speculated to be involved in osmosensing in plants1,9. However, the molecular nature of corresponding Ca2+ channels remain unclear6,10,11. Here we describe a hyperosmolality-gated calcium-permeable channel and its function in osmosensing in plants. Using calcium-imaging-based unbiased forward genetic screens we isolated Arabidopsis mutants that exhibit low hyperosmolality-induced [Ca2+]i increases. These mutants were rescreened for their cellular, physiological and developmental responses to osmotic stress, and those with clear combined phenotypes were selected for further physical mapping. One of the mutants, reduced hyperosmolality-induced [Ca2+]i increase 1 (osca1), displays impaired osmotic Ca2+ signalling in guard cells and root cells, and attenuated water transpiration regulation and root growth in response to osmotic stress. OSCA1 is identified as a previously unknown plasma membrane protein and forms hyperosmolality-gated calcium-permeable channels, revealing that OSCA1 may be an osmosensor. OSCA1 represents a channel responsible for [Ca2+]i increases induced by a stimulus in plants, opening up new avenues for studying Ca2+ machineries for other stimuli and providing potential molecular genetic targets for engineering drought-resistant crops.

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Acknowledgements

We thank M. R. Knight for providing an aequorin vector and aequorin expressing Arabidopsis seeds, S. Gilroy for a YC3.6 vector and YC3.6 expressing Arabidopsis seeds, M. R. Knight and S. Gilroy for sharing unpublished data on genetic screening and physical mapping, X. Dong and M. Chen for advice on physical mapping, J. Grandl, G. Chen and Q. Liu for advice concerning electrophysiology, W. G. Zhang and M. H. Zhu for providing HEK293 cells and advice on transfection, Y. Gao and S. Johnson for confocal imaging, and D. R. McClay, T.-p. Sun, J. Grandl and P. N. Benfey for discussions and critical reading of the manuscript. F.Y. and J.Z. were supported in part by grants from Hangzhou Normal University (PanDeng11001008001) and Zhejiang NSF (Z3110433). This work was supported by grants from USDA (CSREES-2005-35304-16196, CSREES-2006-35100-17304) and NSF (MCB-0451072, IOS-0848263) to Z.-M.P.

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Author notes

    • Huimin Yang
    •  & Yan Xue

    These authors contributed equally to this work.

Affiliations

  1. Department of Biology, Duke University, Durham, North Carolina 27708, USA

    • Fang Yuan
    • , Huimin Yang
    • , Yan Xue
    • , Dongdong Kong
    • , Rui Ye
    • , Chijun Li
    • , Jingyuan Zhang
    • , Lynn Theprungsirikul
    • , Tayler Shrift
    • , Bryan Krichilsky
    • , Yikun He
    • , James N. Siedow
    •  & Zhen-Ming Pei
  2. Center on Plant Environmental Sensing, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, Zhejiang 310036, China

    • Fang Yuan
    •  & Jingyuan Zhang
  3. Department of Physics, Duke University, Durham, North Carolina 27708, USA

    • Douglas M. Johnson
    •  & Gary B. Swift

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Contributions

F.Y., H.Y., Y.X., D.K., R.Y., C.L., J.Z., T.S., B.K., D.M.J. and G.B.S. conducted aequorin imaging and genetic screen. F.Y., H.Y., Y.X., J.Z., L.T., conducted map-based cloning. F.Y., Y.X., D.K., R.Y. and Z.-M.P. conducted Ca2+ imaging and electrophysiological analyses in HEK293 cells and plant cells. F.Y., H.Y., Y.X., J.Z., L.T., T.S., B.K. and Y.H. carried out physiological analyses. Z.-M.P. designed the overall research with input from J.N.S. Z.-M.P., F.Y. and J.N.S. wrote the manuscript. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Fang Yuan or Zhen-Ming Pei.

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https://doi.org/10.1038/nature13593

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