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The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2

Nature Cell Biology volume 10, pages 1217–1223 (2008)Cite this article

Abstract

Carbon dioxide uptake and water vapour release in plants occur through stomata, which are formed by guard cells. These cells respond to light intensity, CO2 and water availability, and plant hormones1,2. The predicted increase in the atmospheric concentration of CO2 is expected to have a profound effect on our ecosystem. However, many aspects of CO2-dependent stomatal movements are still not understood3. Here we show that the ABC transporter AtABCB14 modulates stomatal closure on transition to elevated CO2. Stomatal closure induced by high CO2 levels was accelerated in plants lacking AtABCB14. Apoplastic malate has been suggested to be one of the factors mediating the stomatal response to CO2 (Refs 4,5) and indeed, exogenously applied malate induced a similar AtABCB14-dependent response as high CO2 levels. In isolated epidermal strips that contained only guard cells, malate-dependent stomatal closure was faster in plants lacking the AtABCB14 and slower in AtABCB14-overexpressing plants, than in wild-type plants, indicating that AtABCB14 catalyses the transport of malate from the apoplast into guard cells. Indeed, when AtABCB14 was heterologously expressed in Escherichia coli and HeLa cells, increases in malate transport activity were observed. We therefore suggest that AtABCB14 modulates stomatal movement by transporting malate from the apoplast into guard cells, thereby increasing their osmotic pressure.

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Figure 1: AtABCB14 is expressed mainly in guard cells and localizes at the plasma membrane.
Figure 2: AtABCB14 affects stomatal closure in response to elevated CO2 levels and malate.
Figure 3: AtABCB14 mediates malate transport.
Figure 4: AtABCB14 mutants show different flowering times.

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Acknowledgements

We thank N. Amrhein, Swiss Federal School of Technology for reading the manuscript, A. Vavasseur for helpful discussion on gas-exchange measurements and M. Schellenberg for making section images of AtABCB14:GUS. This project was supported by the Global Research Laboratory programme of the Ministry of Science and Technology of Korea. The work in the laboratory of E.M. was partially supported by the Swiss National Foundation.

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Author notes

  1. Enrico Martinoia and Youngsook Lee: These authors contributed equally to the work.

Authors and Affiliations

  1. Postech-UZH Global Research Laboratory, Pohang University of Science and Technology, Pohang, 790-784, Korea

    Miyoung Lee, Bo Burla, Yu-Young Kim, Byeongwook Jeon, Enrico Martinoia & Youngsook Lee

  2. Department of Life Science, Pohang University of Science and Technology, Pohang, 790-784, Korea

    Miyoung Lee, Yongwook Choi, Yu-Young Kim, Byeongwook Jeon, Joo-Yeon Yoo, Enrico Martinoia & Youngsook Lee

  3. Institute of Plant Biology, University of Zurich, Zollikerstrasse 107, 8008, Zürich, Switzerland

    Bo Burla & Enrico Martinoia

  4. Laboratory of Cell Dynamics, Graduate School of Bio agricultural Sciences, Nagoya University, Nagoya, 464-8601, Japan

    Masayoshi Maeshima

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Contributions

M.L. performed most of the experiments; Y.C. and J.-Y.Y. assisted with the HeLa cell experiments; B.B. contributed to the gas-exchange experiment; Y.-Y.K. and M.M. contributed to the membrane fractionation experiment; B.J. contributed to the localization study; E.M. and Y.L. designed the experiments and wrote the manuscript.

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Correspondence to Youngsook Lee.

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Supplementary Information

Supplementary Figures S1, S2, S3, S4, S5 and S6 (PDF 978 kb)

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Lee, M., Choi, Y., Burla, B. et al. The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nat Cell Biol 10, 1217–1223 (2008). https://doi.org/10.1038/ncb1782

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