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Dissection of abscisic acid signal transduction pathways in barley aleurone layers

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Abstract

Abscisic acid (ABA) induces genes that are highly expressed during late embryogenesis, but suppresses gibberellin (GA)-responsive genes essential for seed germination and seedling growth. Promoter elements necessary and sufficient for ABA up- and down-regulation of gene expression have been previously defined in barley aleurone layers. We have studied the effect of a protein phosphatase 2C, ABI1, an ABA-inducible protein kinase, PKABA1, and a transcription factor, VP1, on ABA action in a barley aleurone transient expression system. The observations have allowed us to dissect ABA signal transduction pathways leading to either induction or suppression of gene expression. The ABA induction of embryogenesis genes is highly inhibited in the presence of a mutated protein phosphatase 2C, encoded by the abi1-1 dominant mutant gene that is known to block ABA responses in Arabidopsis. However, the abi1-1 gene product has no effect on the ABA suppression of a GA-responsive α-amylase gene. On the other hand, PKABA1 suppresses the expression of α-amylase genes, but has little effect on ABA up-regulated genes. Therefore, it appears that ABA induction and suppression follow two separate signal transduction pathways with the former inhibited by ABI1 and the latter modulated by PKABA1. The presence of VP1 enhances the ABA induction of late embryogenesis genes, but also suppresses germination specific genes. A schematic model based on these observations is presented to explain the effect of these regulatory proteins on ABA-mediated gene expression.

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References

  • Abe, H., Yamaguchi–Shinozaki, K., Urao, T., Iwasaki, T., Hosokawa, D. and Shinozaki, K. 1997. Role of Arabidopsis MYC and MYB homologs in drought–and absicic acid–regulated gene expression. Plant Cell 9: 1859–1868.

    Google Scholar 

  • Anderberg, R.J. and Walker–Simmons, M.K. 1992. Isolation of a wheat cDNA clone for an abscisic acid–inducible transcript with homology to protein kinase. Proc. Natl. Acad. Sci. USA 89: 10183–10187.

    Google Scholar 

  • Armstrong, F., Leung, J., Grabov, A., Brearley, J., Giraudat, J. and Blatt, M.R. 1995. Sensitivity to abscisic acid of guard–cell K+ channels is suppressed by abi1–1,amutantArabidopsis gene encoding a putative protein phosphatase. Proc. Natl. Acad. Sci. USA 92: 9520–9524.

    Google Scholar 

  • Bruce, W.B., Christensen, A.H., Klein, T., Fromm, M. and Quail, P.H. 1989. Photoregulation of a phytochrome gene promoter from oat transferred into rice by particle bombardment. Proc. Natl. Acad. Sci. USA 86: 9692–9696.

    Google Scholar 

  • Busk, P.K. and Pagès, M. 1998. Regulation of abscisic acid–induced transcription. Plant Mol. Biol. 37: 425–435.

    Google Scholar 

  • Chandler, P.M. and Robertson, M. 1994. Gene expression regulated by abscisic acid and its regulation to stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 113–141.

    Google Scholar 

  • Cutler, S., Ghassemian, M., Bonetta, D., Cooney, S. and McCourt, P. 1996. A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273: 1239–1241.

    Google Scholar 

  • Gilroy, S. 1996. Signal tranduction in barley aleurone protoplasts is calcium dependent and independent. Plant Cell 8: 2193–2209.

    Google Scholar 

  • Gilroy, S. and Jones, R.L. 1994. Perception of gibberellin and ab–scisic acid at the external face of the plasma membrane of barley Hordeum vulgare L. aleurone protoplasts. Plant Physiol. 104: 1185–1192.

    Google Scholar 

  • Gomez–Cadenas, A., Verhey, S.D., Holappa, L.D., Shen, Q., Ho, TH.D. and Walker–Simmons, M.K. 1999. An abscisic acid–induced protein kinase, PKABA1, mediates abscisic acid–suppressed gene expression in barley aleurone. Proc. Natl. Acad. Sci. USA 96: 1767–1772.

    Google Scholar 

  • Gosti, F., Beaudoin, N., Serizet, C., Webb, A.A.R., Vartanian, N. and Giraudat, J. 1999. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signalling. Plant Cell 11: 1897–1909.

    Google Scholar 

  • Gubler, F. and Jacobsen, J.V. 1992. Gibberellin–responsive elements in the promoter of a barley high–pI α–amylase gene. Plant Cell 4: 1435–1441.

    Google Scholar 

  • Gubler, F., Kalla, R., Roberts, J.K. and Jacobsen, J.V. 1995. Gibberellin–regulated expression of a myb gene in barley aleu–rone cells: evidence for Myb transactivation of a high–pI α–amylase gene promoter. Plant Cell 7: 1879–1891.

    Google Scholar 

  • Harper, J.F., Huang, J.F. and Lloyd, S.J. 1994. Genetic identification of an autoinhibitor in CDPK, a protein kinase with a calmodulin–like domain. Biochemistry 33: 7267–7277.

    Google Scholar 

  • Hattori, T., Vasil, V., Rosenkrans, L., Hannah, L.C., McCarty, D.R. and Vasil, I.K. 1992. The Viviparous–1 gene and abscisic acid ac–tivate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maize. Genes Dev. 6: 609–618.

    Google Scholar 

  • Heimovaara, D.S., Mundy, J. and Wang, M. 1995. The effect of intracellular pH on the regulation of the Rab 16A and the α–amylase 1/6–4 promoter by abscisic acid and gibberellins. Plant Mol. Biol. 27: 815–820.

    Google Scholar 

  • Hoecker, U., Vasil, I.K. and McCarty, D.R. 1995. Integrated con–trol of seed maturation and germination programs by activator and repressor functions of Viviparous–1 of maize. Genes Dev. 9: 2459–2469.

    Google Scholar 

  • Hong, B., Barg, R. and Ho, T.H.D. 1992. Developmental and organ–specific expression of an ABA–and stress–induced protein in barley. Plant Mol. Biol. 18: 663–674.

    Google Scholar 

  • Jacobsen, J.V., Gubler, F. and Chandler, P.M. 1995. Gibberellin action in germinated cereal grains. In: P.J. Davies (Ed.) Plant Hormones: Physiology, Biochemistry and Molecular Biology, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 246–271.

    Google Scholar 

  • Khursheed, B. and Rogers, J.C. 1988. Barley αamylase genes: quantitative comparison of steady–state mRNA levels from in–dividual members of the two different families expressed in aleurone cells. J Biol. Chem. 263: 18953–18960.

    Google Scholar 

  • Kovtun, Y., Chiu, W.L., Zeng, W. and Sheen, J. 1998. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395: 716–720.

    Google Scholar 

  • Kuo, A., Cappelluti, S., Cervantes, C.M., Rodriguez, M. and Bush, D.S. 1996. Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells. Plant Cell 8: 259–269.

    Google Scholar 

  • Lanahan, M.B., Ho, TH.D., Rogers, S.W. and Rogers, J.C. 1992. A gibberellin response complex in cereal α–amylase gene promot–ers. Plant Cell 4: 203–211.

    Google Scholar 

  • Leung, J., Bouvier–Durand, M., Morris, P.C., Guerrier, D., Chefdor, F. and Giraudat, J. 1994. Arabidopsis ABA response gene ABI1: features of a calcium–modulated protein phosphatase. Science 264: 1448–1452.

    Google Scholar 

  • Leung, J. and Giraudat, J. 1998. Abscisic acid signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 199–222.

    Google Scholar 

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

    Google Scholar 

  • Marcotte, W.R. Jr., Russell, S.H. and Quatrano, R.S. 1989. Abscisic acid–responsive sequences from the Em gene of wheat. Plant Cell 1: 969–976.

    Google Scholar 

  • McCarty, D.R., Carson, C.B., Stinard, P.S. and Robertson, D.S. 1989. Molecular analysis of viviparous–1: an abscisic acid in–sensitive mutant of maize. Plant Cell 1: 523–532.

    Google Scholar 

  • McCarty, D.R., Hattori, T., Carson, C.B., Vasil, V., Lazar, M. and Vasil, I.K. 1991. The Viviparous–1 developmental gene of maize encodes a novel transcriptional activator. Cell 66: 895–905.

    Google Scholar 

  • Meyer, K., Leube, M.P. and Grill, E. 1994. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264: 1452–1455.

    Google Scholar 

  • Michel, D., Salamini, F., Bartels, D., Dale, P., Baga, M. and Sza–lay, A. 1993. Analysis of a desiccation and ABA–responsive promoter isolated from the resurrection plant Craterostigma plantagineum. Plant J. 4: 29–40.

    Google Scholar 

  • Pei, Z.M., Ghassemian, M., Kwak, C.M., McCourt, P. and Schroeder, J. 1998. Role of farnesyltransferase in ABA regula–tion of guard cell anion channels and plant water loss. Science 282: 287–290.

    Google Scholar 

  • Ritchie, S. and Gilroy, S. 1998. Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity. Proc. Natl. Acad. Sci. USA 95: 2697–2702.

    Google Scholar 

  • Robertson, M., Swain, S.M., Chandler, P.M., Olszewski, N.E. 1998. Identification of a negative regulator of gibberellin action, HvSPY, in barley. Plant Cell 10: 995–1007.

    Google Scholar 

  • Robichaud, C.S., Wong, J. and Sussex, I.M. 1980. Control of in vitro growth of viviparous embryo mutants of maize by abscisic acid. Dev. Genet. 1: 325–330.

    Google Scholar 

  • Rogers, J.C. and Rogers, S.W. 1992. Definition and functional im–plications of gibberellin and abscisic acid cis–acting hormone response complexes. Plant Cell 4: 1443–1451.

    Google Scholar 

  • Schultz, T.F., Medina, J., Hill, A. and Quatrano, R.S. 1998. 14–3–3 proteins are part of an abscisic acid–VIVIPAROUS1 (VP1) response complex in the Em promoter and interact with VP1 and EmBP1. Plant Cell 10: 837–847.

    Google Scholar 

  • Schwartz, A., Wu, W.H., Tucker, E.B. and Assmann, S.M. 1994. Inhibition of inward K+channels and stomatal response by ab–scisic acid: an intracellular locus of phytohormone action. Proc. Natl. Acad. Sci. USA 91: 4019–4023.

    Google Scholar 

  • Sheen, J. 1993. Protein phosphatase activity is required for light–inducible gene expression in maize. EMBO J. 12: 3497–3505.

    Google Scholar 

  • Sheen, J. 1996. Ca2+–dependent protein kinases and stress signal transduction in plants. Science 274: 1900–1902.

    Google Scholar 

  • Sheen, J. 1998. Mutational analysis of protein phosphatase 2C in–volved in abscisic acid signal transduction in higher plants. Proc. Natl. Acad. Sci. USA 95: 975–980.

    Google Scholar 

  • Shen, Q. and Ho, T.H.D. 1995. Functional dissection of an ab–scisic acid (ABA)–inducible gene reveals two independent ABA–responsive complexes each containing a G–box and a novel cis–acting element. Plant Cell 7: 295–307.

    Google Scholar 

  • Shen, Q., Uknes, S.J. and Ho, T.H.D. 1993. Hormone response complex of a novel abscisic acid and cycloheximide inducible barley gene. J. Biol. Chem. 268: 23652–23660.

    Google Scholar 

  • Shen, Q., Zhang, P. and Ho, T.H.D. 1996. Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell 8: 1107–1119.

    Google Scholar 

  • Skriver, K. and Mundy, J. 1990. Gene expression in response to abscisic acid and osmotic stress. Plant Cell 2: 503–512.

    Google Scholar 

  • Smith, R. and Walker, J. 1991. Isolation and expression of a maize type 1 protein phosphatase. Plant Physiol. 97: 677–683.

    Google Scholar 

  • van der Veen, R., Heimovaara–Dijkstra, S. and Wang, M. 1992. Cytosolic alkalinization mediated by abscisic acid is necessary, but not sufficient, for abscisic acid–induced gene expression in barley aleurone protoplasts. Plant Physiol. 104: 761–767.

    Google Scholar 

  • Vicient, C.M., Hull, G., Guilleminot, J., Devic, M. and Delseny, M. 2000. Differential expression of the Arabidopsis genes coding for Em–like proteins. J. Exp. Bot. 51: 1211–1220.

    Google Scholar 

  • Wang, M., Van, D.B. and Schram, A.W. 1991. Abscisic acid induces a cytosolic calcium decrease in barley aleurone protoplasts. FEBS Lett. 278: 69–74.

    Google Scholar 

  • Wu, Y., Kuzma, J., Marechal, E., Graeff, R., Lee, H.C., Foster, R., Chua, N.–H. 1997. Abscisic acid signaling through cyclic ADP–ribose in plants. Science 278: 2126–2130.

    Google Scholar 

  • Zeevaart, J.A.D. and Creelmann, R.A. 1988. Metabolism and physi–ology of abscisic acid. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39: 439–473.

    Google Scholar 

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Shen, Q., Gomez-Cadenas, A., Zhang, P. et al. Dissection of abscisic acid signal transduction pathways in barley aleurone layers. Plant Mol Biol 47, 437–448 (2001). https://doi.org/10.1023/A:1011667312754

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