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Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase

Abstract

Protein kinases are involved in stress signalling in both plant and animal systems. The hormone abscisic acid mediates the responses of plants to stresses such as drought, salinity and cold. Abscisic-acid-activated protein kinase (AAPK)—found in guard cells, which control stomatal pores—has been shown to regulate plasma membrane ion channels1. Here we show that AAPK-interacting protein 1 (AKIP1), with sequence homology to heterogeneous nuclear RNA-binding protein A/B, is a substrate of AAPK. AAPK-dependent phosphorylation is required for the interaction of AKIP1 with messenger RNA that encodes dehydrin, a protein implicated in cell protection under stress conditions. AAPK and AKIP1 are present in the guard-cell nucleus, and in vivo treatment of such cells with abscisic acid enhances the partitioning of AKIP1 into subnuclear foci which are reminiscent of nuclear speckles. These results show that phosphorylation-regulated RNA target discrimination by heterogeneous nuclear RNA-binding proteins2 may be a general phenomenon in eukaryotes, and implicate a plant hormone in the regulation of protein dynamics during rapid subnuclear reorganization.

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Figure 1: AKIP1 encodes a protein that binds single-stranded RNA.
Figure 2: AKIP1 specifically interacts with AAPK in the yeast two-hybrid system.
Figure 3: AKIP1 and AAPK localization in guard cells.
Figure 4: Phosphorylation of AKIP1 by ABA-activated AAPK regulates AKIP1 binding to dehydrin mRNA.
Figure 5: Interaction of AAPK-phosphorylated AKIP1 with dehydrin transcript.

References

  1. Li, J., Wang, X. Q., Watson, M. B. & Assmann, S. M. Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287, 300–303 (2000)

    CAS  Article  Google Scholar 

  2. Ostrowski, J. et al. Insulin alters heterogeneous nuclear ribonucleoprotein K protein binding to DNA and RNA. Proc. Natl Acad. Sci. USA 98, 9044–9049 (2001)

    CAS  Article  Google Scholar 

  3. Schroeder, J. I., Kwak, J. M. & Allen, G. J. Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410, 327–330 (2001)

    CAS  Article  Google Scholar 

  4. Assmann, S. M. & Wang, X.-Q. From milliseconds to millions of years: guard cells and environmental responses. Curr. Opin. Plant Biol. 4, 421–428 (2001)

    CAS  Article  Google Scholar 

  5. Burd, C. G. & Dreyfuss, G. Conserved structures and diversity of functions of RNA-binding proteins. Science 265, 615–621 (1994)

    CAS  Article  Google Scholar 

  6. Krecic, A. M. & Swanson, M. S. hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11, 363–371 (1999)

    CAS  Article  Google Scholar 

  7. Khan, F. A., Jaiswal, A. K. & Szer, W. Cloning and sequence analysis of a human type A/B hnRNP protein. FEBS Lett. 290, 159–161 (1991)

    CAS  Article  Google Scholar 

  8. Misteli, T. Protein dynamics: implications for nuclear architecture and gene expression. Science 291, 843–847 (2001)

    CAS  Article  Google Scholar 

  9. Li, J. & Assmann, S. M. An ABA-activated and calcium-independent protein kinase from guard cells of fava bean. Plant Cell 8, 2359–2368 (1996)

    CAS  Article  Google Scholar 

  10. Mori, I. C. & Muto, S. Abscisic acid activates a 48-kilodalton protein kinase in guard cell protoplasts. Plant Physiol. 113, 833–839 (1997)

    CAS  Article  Google Scholar 

  11. Busk, P. K. & Pages, M. Regulation of abscisic acid-induced transcription. Plant Mol. Biol. 37, 425–435 (1998)

    CAS  Article  Google Scholar 

  12. Shen, L., Outlaw, W. H. Jr & Epstein, L. M. Expression of an mRNA with sequence similarity to pea dehydrin (Psdhn 1) in guard cells of Vicia faba in response to exogenous abscisic acid. Physiol. Planta 95, 99–105 (1995)

    CAS  Article  Google Scholar 

  13. Dixon, A. K., Richardson, P. J., Lee, K., Carter, N. P. & Freeman, T. C. Expression profiling of single cells using 3 prime end amplification (TPEA) PCR. Nucleic Acids Res. 26, 4426–4431 (1998)

    CAS  Article  Google Scholar 

  14. Li, J., Lee, Y. R. & Assmann, S. M. Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel. Plant Physiol. 116, 785–795 (1998)

    CAS  Article  Google Scholar 

  15. Freire, M. A. & Pagès, M. Functional characteristics of the maize RNA-binding protein MA16. Plant Mol. Biol. 29, 797–807 (1995)

    CAS  Article  Google Scholar 

  16. Lorkovic, Z. J. & Barta, A. Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res. 30, 623–635 (2002)

    CAS  Article  Google Scholar 

  17. Lorkovic, Z. J., Wieczorek Kirk, D. A., Lambermon, M. H. L. & Filipowicz, W. Pre-mRNA splicing in higher plants. Trends Plant Sci. 5, 160–167 (2000)

    CAS  Article  Google Scholar 

  18. Lambermon, M. H. L. et al. UBP1, a novel hnRNP-like protein that functions at multiple steps of higher plant nuclear pre-mRNA maturation. EMBO J. 19, 1638–1649 (2000)

    CAS  Article  Google Scholar 

  19. Macknight, R. et al. FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89, 737–745 (1997)

    CAS  Article  Google Scholar 

  20. Schomburg, F. M., Patton, D. A., Meinke, D. W. & Amasino, R. M. FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13, 1427–1436 (2001)

    CAS  Article  Google Scholar 

  21. Lu, C. & Fedoroff, N. A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12, 2351–2366 (2000)

    CAS  Article  Google Scholar 

  22. Xiong, L. et al. Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev. Cell 1, 771–781 (2001)

    CAS  Article  Google Scholar 

  23. Hugouvieux, V., Kwak, J. M. & Schroeder, J. I. An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106, 477–487 (2001)

    CAS  Article  Google Scholar 

  24. Gómez, J. et al. A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature 344, 262–264 (1988)

    Article  Google Scholar 

  25. Dunn, M. A., Brown, K., Lightowlers, R. & Hughes, M. A. A low-temperature-responsive gene from barley encodes a protein with single-stranded nucleic acid-binding activity which is phosphorylated in vitro. Plant Mol. Biol. 30, 947–959 (1996)

    CAS  Article  Google Scholar 

  26. Melcak, I., Melcakova, S., Kopsky, V., Vecerova, J. & Raska, I. Prespliceosomal assembly on microinjected precursor mRNA takes place in nuclear speckles. Mol. Biol. Cell 12, 393–406 (2001)

    CAS  Article  Google Scholar 

  27. Stone, J. M., Collinge, M. A., Smith, R. D., Horn, M. A. & Walker, J. C. Interaction of a protein phosphatase with an Arabidopsis serine-threonine receptor kinase. Science 266, 793–795 (1994)

    CAS  Article  Google Scholar 

  28. Gygi, S. P., Rochon, Y., Franza, B. R. & Aebersold, R. Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720–1730 (1999)

    CAS  Article  Google Scholar 

  29. Kinoshita, T. & Shimazaki, K. Blue light activates the plasma membrane H+-ATPase by phosphorylation of C-terminus in stomatal guard cells. EMBO J. 18, 5548–5558 (1999)

    CAS  Article  Google Scholar 

  30. Moz, Y., Silver, J. & Naveh-Many, T. Protein-RNA interactions determine the stability of the renal NaPi-2 cotransporter mRNA and its translation in hypophosphatemic rats. J. Biol. Chem. 274, 25266–25272 (1999)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank S. Gilroy and E. Kunze for the use of their confocal and fluorescence microscopes; M. Guiltinan for use of the gene gun; H. Ma for providing the SNF1 and SNF4 constructs; P. James for providing the PJ69-4A strain; L. Ding for assistance with AKIP1 constructs; and P. Minnich for technical support. This research was supported by NSF (S.M.A.) and partly supported by a Grant-in-Aid for Scientific Research on Priority Areas from Ministry of Education, Sports and Culture of Japan (K.S. and T.K.).

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Correspondence to Jiaxu Li or Sarah M. Assmann.

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Li, J., Kinoshita, T., Pandey, S. et al. Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase. Nature 418, 793–797 (2002). https://doi.org/10.1038/nature00936

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