Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1996 Jul;8(7):1107–1119. doi: 10.1105/tpc.8.7.1107

Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley.

Q Shen 1, P Zhang 1, T H Ho 1
PMCID: PMC161185  PMID: 8768371

Abstract

The modular nature of the abscisic acid response complex (ABRC), the promoter unit necessary and sufficient for abscisic acid (ABA) induction of gene expression in barley, is defined in this study. We investigated ABA induction of a barley late embrogenesis abundant (Lea) gene, HVA1, and found that the ABRC of this gene consists of a 10-bp box with an ACGT core (ACGT-box) and the 11 bp directly upstream, named coupling element 3 (CE3). Only one copy of this ABRC is sufficient to confer ABA induction when linked to a minimal promoter. Because we previously reported another ABRC in the barley HVA22 gene, which consists of an ACGT-box with a distal coupling element (CE1), exchange experiments were conducted to study the interaction among modular elements in these ABRCs. We show that ACGT-boxes in these ABRCs are interchangeable, indicating that an ACGT-box can interact with either a distal or a proximal coupling element to confer ABA response. However, the two coupling elements are not fully exchangeable. Although CE3 can function either proximal or distal to the ACGT-box, CE1 is only functional at the distal position. The presence of both the distal and the proximal coupling elements has a synergistic effect on the absolute level of expression as well as on ABA induction. These ABRCs function in both seed and vegetative tissues. In seeds, ABA induction of the ABRC containing the proximal CE3, but not the ABRC with the distal CE1, is enhanced in the presence of the transcription regulator Viviparous1, indicating that these two ABRCs are mediated by different ABA signal transduction pathways.

Full Text

The Full Text of this article is available as a PDF (1.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allan A. C., Fricker M. D., Ward J. L., Beale M. H., Trewavas A. J. Two Transduction Pathways Mediate Rapid Effects of Abscisic Acid in Commelina Guard Cells. Plant Cell. 1994 Sep;6(9):1319–1328. doi: 10.1105/tpc.6.9.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson B. E., Ward J. M., Schroeder J. I. Evidence for an Extracellular Reception Site for Abscisic Acid in Commelina Guard Cells. Plant Physiol. 1994 Apr;104(4):1177–1183. doi: 10.1104/pp.104.4.1177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Armstrong G. A., Weisshaar B., Hahlbrock K. Homodimeric and heterodimeric leucine zipper proteins and nuclear factors from parsley recognize diverse promoter elements with ACGT cores. Plant Cell. 1992 May;4(5):525–537. doi: 10.1105/tpc.4.5.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bartels D., Engelhardt K., Roncarati R., Schneider K., Rotter M., Salamini F. An ABA and GA modulated gene expressed in the barley embryo encodes an aldose reductase related protein. EMBO J. 1991 May;10(5):1037–1043. doi: 10.1002/j.1460-2075.1991.tb08042.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Block A., Dangl J. L., Hahlbrock K., Schulze-Lefert P. Functional borders, genetic fine structure, and distance requirements of cis elements mediating light responsiveness of the parsley chalcone synthase promoter. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5387–5391. doi: 10.1073/pnas.87.14.5387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chaloupková K., Smart C. C. The abscisic acid induction of a novel peroxidase is antagonized by cytokinin in Spirodela polyrrhiza L. Plant Physiol. 1994 Jun;105(2):497–507. doi: 10.1104/pp.105.2.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Donald R. G., Cashmore A. R. Mutation of either G box or I box sequences profoundly affects expression from the Arabidopsis rbcS-1A promoter. EMBO J. 1990 Jun;9(6):1717–1726. doi: 10.1002/j.1460-2075.1990.tb08295.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Foster R., Izawa T., Chua N. H. Plant bZIP proteins gather at ACGT elements. FASEB J. 1994 Feb;8(2):192–200. doi: 10.1096/fasebj.8.2.8119490. [DOI] [PubMed] [Google Scholar]
  9. Giuliano G., Pichersky E., Malik V. S., Timko M. P., Scolnik P. A., Cashmore A. R. An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7089–7093. doi: 10.1073/pnas.85.19.7089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Guiltinan M. J., Marcotte W. R., Jr, Quatrano R. S. A plant leucine zipper protein that recognizes an abscisic acid response element. Science. 1990 Oct 12;250(4978):267–271. doi: 10.1126/science.2145628. [DOI] [PubMed] [Google Scholar]
  11. Hattori T., Vasil V., Rosenkrans L., Hannah L. C., McCarty D. R., Vasil I. K. The Viviparous-1 gene and abscisic acid activate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maize. Genes Dev. 1992 Apr;6(4):609–618. doi: 10.1101/gad.6.4.609. [DOI] [PubMed] [Google Scholar]
  12. Hong B., Barg R., Ho T. H. Developmental and organ-specific expression of an ABA- and stress-induced protein in barley. Plant Mol Biol. 1992 Feb;18(4):663–674. doi: 10.1007/BF00020009. [DOI] [PubMed] [Google Scholar]
  13. Izawa T., Foster R., Chua N. H. Plant bZIP protein DNA binding specificity. J Mol Biol. 1993 Apr 20;230(4):1131–1144. doi: 10.1006/jmbi.1993.1230. [DOI] [PubMed] [Google Scholar]
  14. Khursheed B., Rogers J. C. Barley alpha-amylase genes. Quantitative comparison of steady-state mRNA levels from individual members of the two different families expressed in aleurone cells. J Biol Chem. 1988 Dec 15;263(35):18953–18960. [PubMed] [Google Scholar]
  15. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
  16. Lanahan M. B., Ho T. H., Rogers S. W., Rogers J. C. A gibberellin response complex in cereal alpha-amylase gene promoters. Plant Cell. 1992 Feb;4(2):203–211. doi: 10.1105/tpc.4.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Liu Z. B., Ulmasov T., Shi X., Hagen G., Guilfoyle T. J. Soybean GH3 promoter contains multiple auxin-inducible elements. Plant Cell. 1994 May;6(5):645–657. doi: 10.1105/tpc.6.5.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Loake G. J., Faktor O., Lamb C. J., Dixon R. A. Combination of H-box [CCTACC(N)7CT] and G-box (CACGTG) cis elements is necessary for feed-forward stimulation of a chalcone synthase promoter by the phenylpropanoid-pathway intermediate p-coumaric acid. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9230–9234. doi: 10.1073/pnas.89.19.9230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Marcotte W. R., Jr, Russell S. H., Quatrano R. S. Abscisic acid-responsive sequences from the em gene of wheat. Plant Cell. 1989 Oct;1(10):969–976. doi: 10.1105/tpc.1.10.969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mason H. S., DeWald D. B., Mullet J. E. Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell. 1993 Mar;5(3):241–251. doi: 10.1105/tpc.5.3.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McCarty D. R., Hattori T., Carson C. B., Vasil V., Lazar M., Vasil I. K. The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell. 1991 Sep 6;66(5):895–905. doi: 10.1016/0092-8674(91)90436-3. [DOI] [PubMed] [Google Scholar]
  22. Meyer K., Leube M. P., Grill E. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science. 1994 Jun 3;264(5164):1452–1455. doi: 10.1126/science.8197457. [DOI] [PubMed] [Google Scholar]
  23. Mundy J., Chua N. H. Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J. 1988 Aug;7(8):2279–2286. doi: 10.1002/j.1460-2075.1988.tb03070.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pla M., Gómez J., Goday A., Pagès M. Regulation of the abscisic acid-responsive gene rab28 in maize viviparous mutants. Mol Gen Genet. 1991 Dec;230(3):394–400. doi: 10.1007/BF00280296. [DOI] [PubMed] [Google Scholar]
  25. Qin X. F., Holuigue L., Horvath D. M., Chua N. H. Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element. Plant Cell. 1994 Jun;6(6):863–874. doi: 10.1105/tpc.6.6.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rogers J. C., Rogers S. W. Definition and functional implications of gibberellin and abscisic acid cis-acting hormone response complexes. Plant Cell. 1992 Nov;4(11):1443–1451. doi: 10.1105/tpc.4.11.1443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schulze-Lefert P., Becker-André M., Schulz W., Hahlbrock K., Dangl J. L. Functional architecture of the light-responsive chalcone synthase promoter from parsley. Plant Cell. 1989 Jul;1(7):707–714. doi: 10.1105/tpc.1.7.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schwartz A., Wu W. H., Tucker E. B., Assmann S. M. Inhibition of inward K+ channels and stomatal response by abscisic acid: an intracellular locus of phytohormone action. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):4019–4023. doi: 10.1073/pnas.91.9.4019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shen Q., Ho T. H. Functional 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. 1995 Mar;7(3):295–307. doi: 10.1105/tpc.7.3.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shen Q., Uknes S. J., Ho T. H. Hormone response complex in a novel abscisic acid and cycloheximide-inducible barley gene. J Biol Chem. 1993 Nov 5;268(31):23652–23660. [PubMed] [Google Scholar]
  31. Skriver K., Olsen F. L., Rogers J. C., Mundy J. cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7266–7270. doi: 10.1073/pnas.88.16.7266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Straub P. F., Shen Q., Ho T. D. Structure and promoter analysis of an ABA- and stress-regulated barley gene, HVA1. Plant Mol Biol. 1994 Oct;26(2):617–630. doi: 10.1007/BF00013748. [DOI] [PubMed] [Google Scholar]
  33. Tarczynski M. C., Jensen R. G., Bohnert H. J. Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science. 1993 Jan 22;259(5094):508–510. doi: 10.1126/science.259.5094.508. [DOI] [PubMed] [Google Scholar]
  34. Vasil V., Marcotte W. R., Jr, Rosenkrans L., Cocciolone S. M., Vasil I. K., Quatrano R. S., McCarty D. R. Overlap of Viviparous1 (VP1) and abscisic acid response elements in the Em promoter: G-box elements are sufficient but not necessary for VP1 transactivation. Plant Cell. 1995 Sep;7(9):1511–1518. doi: 10.1105/tpc.7.9.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Williams M. E., Foster R., Chua N. H. Sequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding. Plant Cell. 1992 Apr;4(4):485–496. doi: 10.1105/tpc.4.4.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Williamson J. D., Scandalios J. G. Differential response of maize catalases to abscisic acid: Vp1 transcriptional activator is not required for abscisic acid-regulated Cat1 expression. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8842–8846. doi: 10.1073/pnas.89.18.8842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yamaguchi-Shinozaki K., Mundy J., Chua N. H. Four tightly linked rab genes are differentially expressed in rice. Plant Mol Biol. 1990 Jan;14(1):29–39. doi: 10.1007/BF00015652. [DOI] [PubMed] [Google Scholar]
  38. Zhang B., Singh K. B. ocs element promoter sequences are activated by auxin and salicylic acid in Arabidopsis. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2507–2511. doi: 10.1073/pnas.91.7.2507. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES