Skip to main content
SpringerLink
Log in

Crosstalk Between Gibberellin and Abscisic Acid in Cereal Aleurone

  • Thematic Articles
  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The antagonism between gibberellins (GA) and abscisic acid (ABA) is an important factor regulating the developmental transition from embryogenesis to seed germination. In cereal aleurone layers, the expression of genes encoding hydrolytic enzymes needed for seedling growth, such as α-amylases and proteases, is induced by GA but suppressed by ABA. In addition, ABA induces the expression of genes that may play a role in the establishment of stress tolerance. Because of these well-defined biochemical and molecular markers, the cereal aleurone layers have been used as a convenient system for studying GA/ABA actions. Both gain- and loss-of-function approaches have been followed by the constitutive or the RNAi-mediated knockdown expression of specific regulatory molecules. The GA signaling pathway is anchored by the transcription factor GAMyb, which interacts with a specific region in the promoter of GA up-regulated genes, and an upstream regulatory molecule SLN1 (SLR1) that appears to be a functional homolog of the Arabidopsis GAI/RGA regulatory proteins. It is established that the ABA induction and suppression of gene expression follow two distinct signaling pathways, with the former requiring a transcription factor ABI5, but inhibited by a protein phosphatase 2C, and the latter mediated by a protein kinase PKABA1 and an unknown factor. The ABA suppression action has been pinpointed to be upstream from the formation of functional GAMyb but downstream from the site of action of SLN1 (SLR1).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  • RJ Anderberg MK Walker-Simmons (1992) ArticleTitleIsolation of a wheat cDNA clone for abscisic acid-inducible transcript with homology to protein kinase. Proc Natl Acad Sci USA 89 10183–10187 Occurrence Handle1:CAS:528:DyaK3sXit1Kqt70%3D Occurrence Handle1438207

    CAS  PubMed  Google Scholar 

  • PC Bethke JE Longsdale A Fath RL Jones (1999) ArticleTitleHormonally regulated programmed cell death in barley aleurone cells. Plant Cell 11 1033–1045 Occurrence Handle10.1105/tpc.11.6.1033 Occurrence Handle1:CAS:528:DyaK1MXksFOmtbo%3D Occurrence Handle10368175

    Article  CAS  PubMed  Google Scholar 

  • J Casaretto T-HD Ho (2003) ArticleTitleThe transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell 15 271–284

    Google Scholar 

  • M Cercos A Gomez-Cadenas T-HD Ho (1999) ArticleTitleHormonal regulation of a cysteine proteinase gene, EPB-1, in barley aleurone layers: cis- and trans-acting elements involved in the co-coordinated gene expression regulated by gibberellins and abscisic acid. Plant J 19 107–118 Occurrence Handle10.1046/j.1365-313X.1999.00499.x Occurrence Handle10476058

    Article  PubMed  Google Scholar 

  • PM Chandler (1988) ArticleTitleHormonal regulation of gene expression in the “slender” mutant of barley (Hordeum vulgare L.). Planta 175 115–120 Occurrence Handle1:CAS:528:DyaL1cXkslSnur0%3D

    CAS  Google Scholar 

  • PM Chandler A Marion-Poll M Ellis F Gubler (2002) ArticleTitleMutants at the Slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol 129 181–190 Occurrence Handle10.1104/pp.010917 Occurrence Handle1:CAS:528:DC%2BD38XjvFSnu7Y%3D Occurrence Handle12011349

    Article  CAS  PubMed  Google Scholar 

  • MJ Chrispeels JE Varner (1965) ArticleTitleInhibition of gibberellin induced α-amylase formation by abscissin II. Nature 212 1066–1067

    Google Scholar 

  • L Dure III (1993) ArticleTitleA repeating 11-mer amino acid motif and plant desiccation. Plant J 3 363–369

    Google Scholar 

  • GB Fincher (1989) ArticleTitleMolecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu Rev Plant Physiol Plant Mol Biol 40 305–346 Occurrence Handle1:CAS:528:DyaL1MXktlKmurc%3D

    CAS  Google Scholar 

  • RR Finkelstein TJ Lynch (2000) ArticleTitleThe Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12 599–609

    Google Scholar 

  • RR Finkelstein ML Wang TJ Lynch S Rao HM Goodman (1998) ArticleTitleThe Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10 1043–1054

    Google Scholar 

  • X Fu DE Richards T Ait-Ali LW Hynes H Ougham J Peng NP Harberd (2002) ArticleTitleGibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14 3191–3200

    Google Scholar 

  • Y Fugisawa T Kato S Ohki A Ishikawa H Kitano T Sasaki T Asahi Y Iwasaki (1999) ArticleTitleSuppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice. Proc Natl Acad Sci 96 7575–7580 Occurrence Handle10.1073/pnas.96.13.7575 Occurrence Handle10377457

    Article  PubMed  Google Scholar 

  • L Gilbert J Tata G Atkinson (1996) Metamorphosis: postembryonic preprogramming of gene expression in amphibian and insect cells. Academic Press San Diego, CA

    Google Scholar 

  • S Gilroy RL Jones (1994) ArticleTitlePerception of gibberellin and abscisic acid at the external face of the plasma membrane of barley (Hordeum vulgare L.) aleurone protoplasts. Plant Physiol 104 1185–1192 Occurrence Handle1:CAS:528:DyaK2cXjtF2mtL0%3D Occurrence Handle12232156

    CAS  PubMed  Google Scholar 

  • GF Gocal AT Poole F Gubler RJ Watts C Blundell RW King (1999) ArticleTitleLong-day up-regulation of a GAMYB gene during Lolium temulentum inflorescence formation. Plant Physiol 119 1271–1278 Occurrence Handle10.1104/pp.119.4.1271 Occurrence Handle1:CAS:528:DyaK1MXisFymu7c%3D Occurrence Handle10198085

    Article  CAS  PubMed  Google Scholar 

  • A Gomez-Cadenas SD Verhey LD Holappa Q Shen T-HD Ho MK Walker-Simmons (1999) ArticleTitleAn abscisic acid-induced protein kinase, PKABA1, mediates abscisic acid-suppressed gene expression in barley aleurone layers. Proc Natl Acad Sci USA 96 1767–1772 Occurrence Handle1:CAS:528:DyaK1MXhsFSqtro%3D Occurrence Handle9990099

    CAS  PubMed  Google Scholar 

  • A Gomez-Cadenas R Zentella MK Walker-Simmons T-HD Ho (2001) ArticleTitleGibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules. Plant Cell 13 667–679 Occurrence Handle1:CAS:528:DC%2BD3MXis1akt7w%3D Occurrence Handle11251104

    CAS  PubMed  Google Scholar 

  • F Gubler JV Jacobsen (1992) ArticleTitleGibberellin-responsive elements in the promoter of a barley high-pI alpha-amylase gene. Plant Cell 4 1435–1441

    Google Scholar 

  • F Gubler R Kalla JK Roberts JV Jacobsen (1995) ArticleTitleGibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. Plant Cell 7 1879–1891

    Google Scholar 

  • F Gubler D Raventos M Keys R Watts J Mundy JV Jacobsen (1999) ArticleTitleTarget genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J 17 1–9 Occurrence Handle1:CAS:528:DyaK1MXhsVWrurw%3D Occurrence Handle10069063

    CAS  PubMed  Google Scholar 

  • F Gubler PM Chandler RG White DJ Llewellyn JV Jacobsen (2002) ArticleTitleGibberellin signaling in barley aleurone cells. Control of SLN1 and GAMyb expression. Plant Physiol 129 191–200 Occurrence Handle10.1104/pp.010918 Occurrence Handle1:CAS:528:DC%2BD38XjvFSnu7c%3D Occurrence Handle12011350

    Article  CAS  PubMed  Google Scholar 

  • T Hattori V Vasil L Rosenkrans LC Hannah DR McCarty IK Vasil (1992) ArticleTitleThe Viviparous-1 gene and abscisic acid activate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maize. Genes Dev 6 609–618 Occurrence Handle1:CAS:528:DyaK38Xit12mt70%3D Occurrence Handle1532784

    CAS  PubMed  Google Scholar 

  • T-HD Ho (1980) Hormonal and genetic regulation of α-amylase synthesis in barley aleurone cells. CJ Leaver (Eds) Genome organization and expression in plants. Plenum Press New York 147–158

    Google Scholar 

  • T Hobo Y Kowyama T Hattori (1999a) ArticleTitleA bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96 15348–15353 Occurrence Handle1:CAS:528:DC%2BD3cXhtFehtQ%3D%3D

    CAS  Google Scholar 

  • T Hobo M Asada Y Kowyama T Hattori (1999b) ArticleTitleACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19 679–689 Occurrence Handle1:CAS:528:DyaK1MXntFOnsbw%3D

    CAS  Google Scholar 

  • B Hong SJ Uknes T-HD Ho (1988) ArticleTitleCloning and characterization of a cDNA encoding an mRNA, rapidly induced by ABA in barley aleurone layers. Plant Mol Biol 11 495–506 Occurrence Handle1:CAS:528:DyaL1MXksFWgu78%3D

    CAS  Google Scholar 

  • H Itoh M Ueguchi-Tanaka Y Sato M Ashikari M Matsuoka (2002) ArticleTitleGibberellin signaling is regulated by the appearance and disappearance of SLENDER RICE 1 in the nucleus. Plant Cell 14 57–70

    Google Scholar 

  • A Ikeda M Ueguchi-Tanaka Y Sonoda H Kitano M Koshioka Y Futsuhara M Matsuoka J Yamaguchi (2001) ArticleTitleSlender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13 999–1010 Occurrence Handle1:CAS:528:DC%2BD3MXktVSlurk%3D Occurrence Handle11340177

    CAS  PubMed  Google Scholar 

  • RR Johnson RL Wagner SD Verhey MK Walker-Simmons (2002) ArticleTitleThe abscisic acid-responsive kinase PKABA1 interacts with a seed-specific abscisic acid response element-binding factor, TaABF, and phosphorylates TaABF peptide sequences. Plant Physiol 130 837–846 Occurrence Handle10.1104/pp.001354 Occurrence Handle12376648

    Article  PubMed  Google Scholar 

  • HD Jones SJ Smith R Desikan S Plakidou-Dymock A Lovegrove R Hooley (1998) ArticleTitleHeterotrimeric G proteins are implicated in gibberellin induction of α-amylase gene expression in wild oat aleurone. Plant Cell 10 245–254

    Google Scholar 

  • Y Kagaya T Hobo M Murata A Ban T Hattori (2002) ArticleTitleAbscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid-response element-binding factor, TRAB1. Plant Cell 14 3177–3189

    Google Scholar 

  • MB Lanahan T-HD Ho (1988) ArticleTitleSlender barley: a constitutive gibberellin-response mutant. Planta 175 107–114 Occurrence Handle1:CAS:528:DyaL1cXlsVKnsrk%3D

    CAS  Google Scholar 

  • MB Lanahan TH Ho SW Rogers JC Rogers (1992) ArticleTitleA gibberellin response complex in cereal alpha-amylase gene promoters. Plant Cell 4 203–211 Occurrence Handle1:CAS:528:DyaK38Xks1Cjtr4%3D Occurrence Handle1386000

    CAS  PubMed  Google Scholar 

  • L Lopez-Molina S Mongrand NH Chua (2001) ArticleTitleA postgermination arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci 98 4782–4787 Occurrence Handle10.1073/pnas.081594298 Occurrence Handle1:CAS:528:DC%2BD3MXjtVantLc%3D Occurrence Handle11287670

    Article  CAS  PubMed  Google Scholar 

  • S Lee H Cheng KE King W Wang Y He A Hussain J Lo NP Harberd J Peng (2002) ArticleTitleGibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16 646–658 Occurrence Handle10.1101/gad.969002 Occurrence Handle1:CAS:528:DC%2BD38XitVWltbY%3D Occurrence Handle11877383

    Article  CAS  PubMed  Google Scholar 

  • S Nakamura TJ Lynch RR Finkelstein (2001) ArticleTitlePhysical interactions between ABA response loci in Arabidopsis. Plant Physiol 26 627–635 Occurrence Handle10.1046/j.1365-313x.2001.01069.x Occurrence Handle1:CAS:528:DC%2BD3MXmtVGrsbg%3D

    Article  CAS  Google Scholar 

  • E Nambara R Hayama Y Tsuchiya M Nishimura H Kawaide Y Kamiya S Naito (2000) ArticleTitleThe role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Dev Biol 220 412–423

    Google Scholar 

  • X Niu T Helentjaris NJ Bate (2002) ArticleTitleMaize ABI4 binds coupling element 1 in abscisic acid and sugar response genes. Plant Cell 14 2565–2575

    Google Scholar 

  • OA Olsen (2001) ArticleTitleEndosperm development: cellularization and cell fate specification. Annu Rev Plant Physiol Plant Mol Biol 52 233–267 Occurrence Handle10.1146/annurev.arplant.52.1.233 Occurrence Handle1:CAS:528:DC%2BD3MXkslWgsLg%3D Occurrence Handle11337398

    Article  CAS  PubMed  Google Scholar 

  • N Olszewski TP Sun F Gubler (2002) ArticleTitleGibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14 IssueIDsuppl S61–S80

    Google Scholar 

  • J Peng P Carol DE Richards KE King RJ Cowling GP Murphy NP Harberd (1997) ArticleTitleThe Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11 3194–3205 Occurrence Handle1:CAS:528:DyaK1cXntlKr Occurrence Handle9389651

    CAS  PubMed  Google Scholar 

  • S Ritchie S Gilroy (1998) ArticleTitleAbscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity. Proc Natl Acad Sci USA 95 2697–2702 Occurrence Handle10.1073/pnas.95.5.2697 Occurrence Handle1:CAS:528:DyaK1cXhslenu7c%3D Occurrence Handle9482950

    Article  CAS  PubMed  Google Scholar 

  • R Roach Y Cao C Corbett R DePaoli I Farkas C Fiol H Flotow P Graves T Hardy T Hrubey (1991) ArticleTitleGlycogen metabolism and signal transduction in mammals and yeast. Adv Enzyme Regul 31 101–120 Occurrence Handle1652188

    PubMed  Google Scholar 

  • A Sasaki M Ashikari M Ueguchi-Tanaka H Itoh A Nishimura D Swapan K Ishiyama T Saito M Kobayashi GS Khush H Kitano M Matsuoka (2002) ArticleTitleGreen revolution: a mutant gibberellin-synthesis gene in rice. Nature 416 701–702 Occurrence Handle10.1038/416701a Occurrence Handle1:CAS:528:DC%2BD38XjtVKks78%3D Occurrence Handle11961544

    Article  CAS  PubMed  Google Scholar 

  • Q Shen A Gomez-Cadenas P Zhang MK Walker-Simmons J Sheen T-HD Ho (2001) ArticleTitleDissection of abscisic acid signal transduction pathways in barley aleurone layers. Plant Mol Biol 47 437–448 Occurrence Handle10.1023/A:1011667312754 Occurrence Handle1:CAS:528:DC%2BD3MXntlGju7g%3D Occurrence Handle11587514

    Article  CAS  PubMed  Google Scholar 

  • Q Shen T-HD Ho (1995) ArticleTitleFunctional dissection of an abscisic 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 Occurrence Handle1:CAS:528:DyaK2MXks1ChsLY%3D Occurrence Handle7734964

    CAS  PubMed  Google Scholar 

  • Q Shen P Zhang T-HD Ho (1996) ArticleTitleModular 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 Occurrence Handle1:CAS:528:DyaK28XksFKkur8%3D Occurrence Handle8768371

    CAS  PubMed  Google Scholar 

  • AL Silverstone CN Ciampaglio T-p Sun (1998) ArticleTitleThe Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10 155–169 Occurrence Handle1:CAS:528:DyaK1cXhsF2mtr8%3D Occurrence Handle9490740

    CAS  PubMed  Google Scholar 

  • K Skriver J Mundy (1990) ArticleTitleGene expression in response to abscisic acid and osmotic stress. Plant Cell 2 503–512 Occurrence Handle1:CAS:528:DyaK3MXlvVyitw%3D%3D Occurrence Handle2152172

    CAS  PubMed  Google Scholar 

  • EM Söderman IM Brocard TJ Lynch RR Finkelstein (2001) ArticleTitleRegulation and function of the Arabidopsis ABA insensitive 4 in seed and abscisic acid response signaling networks. Plant Physiol 124 1752–1765 Occurrence Handle10.1104/pp.124.4.1752

    Article  Google Scholar 

  • L Srivastava (2002) Plant growth and development: hormones and environment. Academic Press San Diego, CA

    Google Scholar 

  • M Ueguchi-Tanaka Y Fujisawa M Kobayashi M Ashikari Y Iwasaki H Kitano M Matsuoka (2000) ArticleTitleRice dwarf mutant d1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc Natl Acad Sci USA 97 11638–11643 Occurrence Handle10.1073/pnas.97.21.11638 Occurrence Handle1:CAS:528:DC%2BD3cXnsF2qtr8%3D Occurrence Handle11027362

    Article  CAS  PubMed  Google Scholar 

  • FL Woodger A Millar F Murray JV Jacobsen F Gubler (2003) ArticleTitleThe role of GAMYB transcription factors in GA-regulated gene expression. J Plant Growth Regul 22

    Google Scholar 

  • S Yamaguchi MW Smith RG Brown Y Kamiya T Sun (1998) ArticleTitlePhytochrome regulation and differential expression of gibberellin 3beta-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10 2115–2126

    Google Scholar 

  • D Yamauchi R Zentella T-HD Ho (2002) ArticleTitleMolecular analysis of the barley (Hordeum vulgare L.) gene encoding the protein kinase PKABA1 capable of suppressing gibberellin action in aleurone layers. Planta 215 319–326 Occurrence Handle10.1007/s00425-002-0740-6 Occurrence Handle1:CAS:528:DC%2BD38Xjsl2rt7c%3D Occurrence Handle12029482

    Article  CAS  PubMed  Google Scholar 

  • JAD Zeevaart RA Creelmann (1988) ArticleTitleMetabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol 39 439–473 Occurrence Handle10.1146/annurev.pp.39.060188.002255 Occurrence Handle1:CAS:528:DyaL1cXltVOltrc%3D

    Article  CAS  Google Scholar 

  • R Zentella D Yamauchi T-HD Ho (2002) ArticleTitleMolecular dissection of the gibberellin/abscisic acid signaling pathways by transiently expressed RNA interference in barley aleurone cells. Plant Cell 14 2289–2301

    Google Scholar 

Download references

Acknowledgements

The work from the authors’ lab was supported by grants from the US National Science Foundation, United States Department of Agriculture, and Monsanto Company.

Author information

Authors and Affiliations

  1. Department of Biology, Washington University, St. Louis, MO 63130, USA

    Tuan-hua David Ho, Rodolfo Zentella & Jose Casaretto

  2. Departamento de Ciencias Experimentales, Campus Riu Sec (E.S.T.C.E.), Universitat Jaume I, Castello de la Plana 12071, Spain

    Aurelio Gomez-Cadenas

Authors
  1. Tuan-hua David Ho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aurelio Gomez-Cadenas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rodolfo Zentella
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jose Casaretto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tuan-hua David Ho.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ho, Th., Gomez-Cadenas, A., Zentella, R. et al. Crosstalk Between Gibberellin and Abscisic Acid in Cereal Aleurone . J Plant Growth Regul 22, 185–194 (2003). https://doi.org/10.1007/s00344-003-0026-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-003-0026-7

Keywords

Search

Navigation