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ABA-unresponsive SnRK2 protein kinases regulate mRNA decay under osmotic stress in plants

Nature Plants volume 3, Article number: 16204 (2017) Cite this article

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Abstract

Rapid changes in messenger RNA population are vital for plants to properly exert multiple adaptive responses under continuously changing stress conditions. Transcriptional activation mediated by the ‘abscisic acid (ABA)-activated SnRK2 protein kinases–ABA-responsive element (ABRE)-binding proteins/ABRE-binding factors (AREB/ABFs)’ signalling module is a crucial step in the expression of stress-inducible genes under osmotic stress conditions in Arabidopsis1–4. In addition to transcriptional control, proper transcript levels of individual genes can be achieved by post-transcriptional regulation, but how this regulation functions under stress conditions and the underlying molecular mechanisms remain elusive. Here, we show that ABA-unresponsive osmotic stress-activated subclass I SnRK2s and their downstream substrate, VARICOSE (VCS), an mRNA decapping activator, regulate mRNA decay under osmotic stress conditions. The expression of many stress-responsive genes was similarly misregulated in a mutant lacking all functional subclass I SnRK2s and in VCS-knockdown plants. Additionally, the mRNA decay of the transcripts of these genes was impaired in these plants under osmotic stress conditions. Furthermore, these plants showed growth retardation under osmotic stresses. Notably, subclass I-type SnRK2s have been identified in seed plants but not in lycophytes or mosses. Therefore, the post-transcriptional regulation mediated by the ‘subclass I SnRK2s–VARICOSE’ signalling module represents an additional mechanism of gene expression control that facilitates drastic changes in mRNA populations under osmotic stresses and might enhance the adaptability of seed plants to stress conditions.

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Figure 1: SRK2G/SnRK2.1 localizes and physically interacts with VCS in P-bodies under osmotic stress conditions.
Figure 2: Subclass I SnRK2s are major protein kinases that phosphorylate VCS in response to osmotic stresses.
Figure 3: The srk2abgh mutant and VCS-knockdown lines displayed enhanced growth retardation under osmotic stress conditions.
Figure 4: Aberrant mRNA decay in srk2abgh and VCS-knockdown plants under osmotic stress conditions.

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Acknowledgements

The authors thank Y. Tanaka, A. Watanabe and S. Mizukado for excellent technical assistance, E. Toma for skilful editorial assistance, T. Umezawa and M. Mizoguchi for providing the srk2abgh mutant line and Y. Fujita for providing the pGreenII0229-NosT vector. This work was financially supported by grants from a Grant-in-Aid for Scientific Research on Innovative Areas (no. JP15H05960 to K. Y.-S.) and for Scientific Research (A) (no. JP25251031 to K. Y.-S.) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and the Program for the Promotion of Basic Research Activities for Innovative Biosciences (BRAIN) of Japan (to K. S. and K. Y.-S.).

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Author notes

  1. Fumiyuki Soma and Junro Mogami: These authors contributed equally to this work.

Authors and Affiliations

  1. Laboratory of Plant Molecular Physiology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, 113-8657, Tokyo, Japan

    Fumiyuki Soma, Junro Mogami, Takuya Yoshida, Midori Abekura, Satoshi Kidokoro, Junya Mizoi & Kazuko Yamaguchi-Shinozaki

  2. Gene Discovery Research Group, RIKEN Center for Sustainable Resource Science, Yokohama, 230-0045, Kanagawa, Japan

    Fuminori Takahashi & Kazuo Shinozaki

Authors
  1. Fumiyuki Soma
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Contributions

F.S., J.Mo. and K.Y.-S. designed the research. F.S. and J.Mo. contributed equally. F.S., J.Mo., T.Y., M.A., F.T. and S.K. performed the experiments. F.S., J.Mo., T.Y., M.A., F.T. and J.Mi. analysed the data. F.S., J.Mo., K.S. and K.Y.-S. wrote the paper. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Kazuko Yamaguchi-Shinozaki.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Figures 1–12. (PDF 56735 kb)

Supplementary Table 1

Candidate SRK2G-interacting proteins were identified in samples from untreated plants using LC-MS/MS analyses. (XLSX 204 kb)

Supplementary Table 2

Many candidate SRK2G-interacting proteins were detected in extracts from SRK2G-GFP plants treated with 0.8 M mannitol. (XLSX 12 kb)

Supplementary Table 3

List of genes showing increased expression levels in the srk2abgh mutant in comparison to the expression levels in wild-type plants after treatment with dehydration for 5 h. (XLSX 49 kb)

Supplementary Table 4

Comparison of mRNA stability of subclass I SnRK2-regulated genes within each genotype under control and high-salinity conditions. (XLSX 53 kb)

Supplementary Table 5

Primer pairs used in this study. (XLSX 40 kb)

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Soma, F., Mogami, J., Yoshida, T. et al. ABA-unresponsive SnRK2 protein kinases regulate mRNA decay under osmotic stress in plants. Nature Plants 3, 16204 (2017). https://doi.org/10.1038/nplants.2016.204

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