Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1997 Apr;9(4):491–507. doi: 10.1105/tpc.9.4.491

A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene.

Z Y Wang 1, D Kenigsbuch 1, L Sun 1, E Harel 1, M S Ong 1, E M Tobin 1
PMCID: PMC156934  PMID: 9144958

Abstract

We have isolated the gene for a protein designated CCA1. This protein can bind to a region of the promoter of an Arabidopsis light-harvesting chlorophyll a/b protein gene, Lhcb1*3, which is necessary for its regulation by phytochrome. The CCA1 protein interacted with two imperfect repeats in the Lhcb1*3 promoter, AAA/cAATCT, a sequence that is conserved in Lhcb genes. A region near the N terminus of CCA1, which has some homology to the repeated sequence found in the DNA binding domain of Myb proteins, is required for binding to the Lhcb1*3 promoter. Lines of transgenic Arabidopsis plants expressing antisense RNA for CCA1 showed reduced phytochrome induction of the endogenous Lhcb1*3 gene, whereas expression of another phytochrome-regulated gene, rbcS-1A, which encodes the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase, was not affected. Thus, the CCA1 protein acts as a specific activator of Lhcb1*3 transcription in response to brief red illumination. The expression of CCA1 RNA was itself transiently increased when etiolated seedlings were transferred to light. We conclude that the CCA1 protein is a key element in the functioning of the phytochrome signal transduction pathway leading to increased transcription of this Lhcb gene in Arabidopsis.

Full Text

The Full Text of this article is available as a PDF (3.9 MB).

Selected References

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

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Anderson S. L., Kay S. A. Functional dissection of circadian clock- and phytochrome-regulated transcription of the Arabidopsis CAB2 gene. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1500–1504. doi: 10.1073/pnas.92.5.1500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson S. L., Teakle G. R., Martino-Catt S. J., Kay S. A. Circadian clock- and phytochrome-regulated transcription is conferred by a 78 bp cis-acting domain of the Arabidopsis CAB2 promoter. Plant J. 1994 Oct;6(4):457–470. doi: 10.1046/j.1365-313x.1994.6040457.x. [DOI] [PubMed] [Google Scholar]
  4. Argüello-Astorga G. R., Herrera-Estrella L. R. Ancestral multipartite units in light-responsive plant promoters have structural features correlating with specific phototransduction pathways. Plant Physiol. 1996 Nov;112(3):1151–1166. doi: 10.1104/pp.112.3.1151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baranowskij N., Frohberg C., Prat S., Willmitzer L. A novel DNA binding protein with homology to Myb oncoproteins containing only one repeat can function as a transcriptional activator. EMBO J. 1994 Nov 15;13(22):5383–5392. doi: 10.1002/j.1460-2075.1994.tb06873.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barnes S. A., Quaggio R. B., Chua N. H. Phytochrome signal-transduction: characterization of pathways and isolation of mutants. Philos Trans R Soc Lond B Biol Sci. 1995 Oct 30;350(1331):67–74. doi: 10.1098/rstb.1995.0139. [DOI] [PubMed] [Google Scholar]
  7. Brusslan J. A., Karlin-Neumann G. A., Huang L., Tobin E. M. An Arabidopsis mutant with a reduced level of cab140 RNA is a result of cosuppression. Plant Cell. 1993 Jun;5(6):667–677. doi: 10.1105/tpc.5.6.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brusslan J. A., Tobin E. M. Light-independent developmental regulation of cab gene expression in Arabidopsis thaliana seedlings. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7791–7795. doi: 10.1073/pnas.89.16.7791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Burk O., Mink S., Ringwald M., Klempnauer K. H. Synergistic activation of the chicken mim-1 gene by v-myb and C/EBP transcription factors. EMBO J. 1993 May;12(5):2027–2038. doi: 10.1002/j.1460-2075.1993.tb05852.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carabelli M., Sessa G., Baima S., Morelli G., Ruberti I. The Arabidopsis Athb-2 and -4 genes are strongly induced by far-red-rich light. Plant J. 1993 Sep;4(3):469–479. doi: 10.1046/j.1365-313x.1993.04030469.x. [DOI] [PubMed] [Google Scholar]
  11. Carre I. A., Kay S. A. Multiple DNA-Protein Complexes at a Circadian-Regulated Promoter Element. Plant Cell. 1995 Dec;7(12):2039–2051. doi: 10.1105/tpc.7.12.2039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chory J., Chatterjee M., Cook R. K., Elich T., Fankhauser C., Li J., Nagpal P., Neff M., Pepper A., Poole D. From seed germination to flowering, light controls plant development via the pigment phytochrome. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12066–12071. doi: 10.1073/pnas.93.22.12066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chory J., Peto C., Feinbaum R., Pratt L., Ausubel F. Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell. 1989 Sep 8;58(5):991–999. doi: 10.1016/0092-8674(89)90950-1. [DOI] [PubMed] [Google Scholar]
  14. Chou P. Y., Fasman G. D. Empirical predictions of protein conformation. Annu Rev Biochem. 1978;47:251–276. doi: 10.1146/annurev.bi.47.070178.001343. [DOI] [PubMed] [Google Scholar]
  15. Degenhardt J., Tobin E. M. A DNA binding activity for one of two closely defined phytochrome regulatory elements in an Lhcb promoter is more abundant in etiolated than in green plants. Plant Cell. 1996 Jan;8(1):31–41. doi: 10.1105/tpc.8.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Deng X. W. Fresh view of light signal transduction in plants. Cell. 1994 Feb 11;76(3):423–426. doi: 10.1016/0092-8674(94)90107-4. [DOI] [PubMed] [Google Scholar]
  17. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gilmartin P. M., Chua N. H. Localization of a phytochrome-responsive element within the upstream region of pea rbcS-3A. Mol Cell Biol. 1990 Oct;10(10):5565–5568. doi: 10.1128/mcb.10.10.5565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Goff S. A., Cone K. C., Chandler V. L. Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev. 1992 May;6(5):864–875. doi: 10.1101/gad.6.5.864. [DOI] [PubMed] [Google Scholar]
  20. Grotewold E., Drummond B. J., Bowen B., Peterson T. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell. 1994 Feb 11;76(3):543–553. doi: 10.1016/0092-8674(94)90117-1. [DOI] [PubMed] [Google Scholar]
  21. Harter K., Kircher S., Frohnmeyer H., Krenz M., Nagy F., Schäfer E. Light-regulated modification and nuclear translocation of cytosolic G-box binding factors in parsley. Plant Cell. 1994 Apr;6(4):545–559. doi: 10.1105/tpc.6.4.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hinnebusch A. G. Translational control of GCN4: an in vivo barometer of initiation-factor activity. Trends Biochem Sci. 1994 Oct;19(10):409–414. doi: 10.1016/0968-0004(94)90089-2. [DOI] [PubMed] [Google Scholar]
  23. Jackson D., Culianez-Macia F., Prescott A. G., Roberts K., Martin C. Expression patterns of myb genes from Antirrhinum flowers. Plant Cell. 1991 Feb;3(2):115–125. doi: 10.1105/tpc.3.2.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kao C. Y., Cocciolone S. M., Vasil I. K., McCarty D. R. Localization and interaction of the cis-acting elements for abscisic acid, VIVIPAROUS1, and light activation of the C1 gene of maize. Plant Cell. 1996 Jul;8(7):1171–1179. doi: 10.1105/tpc.8.7.1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Karlin-Neumann G. A., Sun L., Tobin E. M. Expression of Light-Harvesting Chlorophyll a/b-Protein Genes Is Phytochrome-Regulated in Etiolated Arabidopsis thaliana Seedlings. Plant Physiol. 1988 Dec;88(4):1323–1331. doi: 10.1104/pp.88.4.1323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kehoe D. M., Degenhardt J., Winicov I., Tobin E. M. Two 10-bp regions are critical for phytochrome regulation of a Lemna gibba Lhcb gene promoter. Plant Cell. 1994 Aug;6(8):1123–1134. doi: 10.1105/tpc.6.8.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kuwabara M. D., Sigman D. S. Footprinting DNA-protein complexes in situ following gel retardation assays using 1,10-phenanthroline-copper ion: Escherichia coli RNA polymerase-lac promoter complexes. Biochemistry. 1987 Nov 17;26(23):7234–7238. doi: 10.1021/bi00397a006. [DOI] [PubMed] [Google Scholar]
  28. Larkin J. C., Oppenheimer D. G., Lloyd A. M., Paparozzi E. T., Marks M. D. Roles of the GLABROUS1 and TRANSPARENT TESTA GLABRA Genes in Arabidopsis Trichome Development. Plant Cell. 1994 Aug;6(8):1065–1076. doi: 10.1105/tpc.6.8.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Leutwiler L. S., Meyerowitz E. M., Tobin E. M. Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucleic Acids Res. 1986 May 27;14(10):4051–4064. doi: 10.1093/nar/14.10.4051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Li S. F., Parish R. W. Isolation of two novel myb-like genes from Arabidopsis and studies on the DNA-binding properties of their products. Plant J. 1995 Dec;8(6):963–972. doi: 10.1046/j.1365-313x.1995.8060963.x. [DOI] [PubMed] [Google Scholar]
  31. Lohmer S., Maddaloni M., Motto M., Salamini F., Thompson R. D. Translation of the mRNA of the maize transcriptional activator Opaque-2 is inhibited by upstream open reading frames present in the leader sequence. Plant Cell. 1993 Jan;5(1):65–73. doi: 10.1105/tpc.5.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Majello B., Kenyon L. C., Dalla-Favera R. Human c-myb protooncogene: nucleotide sequence of cDNA and organization of the genomic locus. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9636–9640. doi: 10.1073/pnas.83.24.9636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Menkens A. E., Schindler U., Cashmore A. R. The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends Biochem Sci. 1995 Dec;20(12):506–510. doi: 10.1016/s0968-0004(00)89118-5. [DOI] [PubMed] [Google Scholar]
  34. Ogata K., Hojo H., Aimoto S., Nakai T., Nakamura H., Sarai A., Ishii S., Nishimura Y. Solution structure of a DNA-binding unit of Myb: a helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6428–6432. doi: 10.1073/pnas.89.14.6428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ogata K., Morikawa S., Nakamura H., Sekikawa A., Inoue T., Kanai H., Sarai A., Ishii S., Nishimura Y. Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell. 1994 Nov 18;79(4):639–648. doi: 10.1016/0092-8674(94)90549-5. [DOI] [PubMed] [Google Scholar]
  36. Oppenheimer D. G., Herman P. L., Sivakumaran S., Esch J., Marks M. D. A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell. 1991 Nov 1;67(3):483–493. doi: 10.1016/0092-8674(91)90523-2. [DOI] [PubMed] [Google Scholar]
  37. Paz-Ares J., Ghosal D., Wienand U., Peterson P. A., Saedler H. The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J. 1987 Dec 1;6(12):3553–3558. doi: 10.1002/j.1460-2075.1987.tb02684.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Pepper A., Delaney T., Washburn T., Poole D., Chory J. DET1, a negative regulator of light-mediated development and gene expression in arabidopsis, encodes a novel nuclear-localized protein. Cell. 1994 Jul 15;78(1):109–116. doi: 10.1016/0092-8674(94)90577-0. [DOI] [PubMed] [Google Scholar]
  40. Puente P., Wei N., Deng X. W. Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J. 1996 Jul 15;15(14):3732–3743. [PMC free article] [PubMed] [Google Scholar]
  41. Quaedvlieg N., Dockx J., Keultjes G., Kock P., Wilmering J., Weisbeek P., Smeekens S. Identification of a light-regulated MYB gene from an Arabidopsis transcription factor gene collection. Plant Mol Biol. 1996 Dec;32(5):987–993. doi: 10.1007/BF00020495. [DOI] [PubMed] [Google Scholar]
  42. Quail P. H., Boylan M. T., Parks B. M., Short T. W., Xu Y., Wagner D. Phytochromes: photosensory perception and signal transduction. Science. 1995 May 5;268(5211):675–680. doi: 10.1126/science.7732376. [DOI] [PubMed] [Google Scholar]
  43. Ruberti I., Sessa G., Lucchetti S., Morelli G. A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J. 1991 Jul;10(7):1787–1791. doi: 10.1002/j.1460-2075.1991.tb07703.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Scheffler B., Franken P., Schütt E., Schrell A., Saedler H., Wienand U. Molecular analysis of C1 alleles in Zea mays defines regions involved in the expression of this regulatory gene. Mol Gen Genet. 1994 Jan;242(1):40–48. doi: 10.1007/BF00277346. [DOI] [PubMed] [Google Scholar]
  45. Shinozaki K., Yamaguchi-Shinozaki K., Urao T., Koizumi M. Nucleotide sequence of a gene from Arabidopsis thaliana encoding a myb homologue. Plant Mol Biol. 1992 Jun;19(3):493–499. doi: 10.1007/BF00023398. [DOI] [PubMed] [Google Scholar]
  46. Singh H., Clerc R. G., LeBowitz J. H. Molecular cloning of sequence-specific DNA binding proteins using recognition site probes. Biotechniques. 1989 Mar;7(3):252–261. [PubMed] [Google Scholar]
  47. Singh K., Dennis E. S., Ellis J. G., Llewellyn D. J., Tokuhisa J. G., Wahleithner J. A., Peacock W. J. OCSBF-1, a maize ocs enhancer binding factor: isolation and expression during development. Plant Cell. 1990 Sep;2(9):891–903. doi: 10.1105/tpc.2.9.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sun L., Doxsee R. A., Harel E., Tobin E. M. CA-1, a novel phosphoprotein, interacts with the promoter of the cab140 gene in Arabidopsis and is undetectable in det1 mutant seedlings. Plant Cell. 1993 Jan;5(1):109–121. doi: 10.1105/tpc.5.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Teakle G. R., Kay S. A. The GATA-binding protein CGF-1 is closely related to GT-1. Plant Mol Biol. 1995 Dec;29(6):1253–1266. doi: 10.1007/BF00020466. [DOI] [PubMed] [Google Scholar]
  50. Tice-Baldwin K., Fink G. R., Arndt K. T. BAS1 has a Myb motif and activates HIS4 transcription only in combination with BAS2. Science. 1989 Nov 17;246(4932):931–935. doi: 10.1126/science.2683089. [DOI] [PubMed] [Google Scholar]
  51. Tobin E. M., Kehoe D. M. Phytochrome regulated gene expression. Semin Cell Biol. 1994 Oct;5(5):335–346. doi: 10.1006/scel.1994.1040. [DOI] [PubMed] [Google Scholar]
  52. Urao T., Yamaguchi-Shinozaki K., Urao S., Shinozaki K. An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell. 1993 Nov;5(11):1529–1539. doi: 10.1105/tpc.5.11.1529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Valvekens D., Van Montagu M., Van Lijsebettens M. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536–5540. doi: 10.1073/pnas.85.15.5536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Varagona M. J., Schmidt R. J., Raikhel N. V. Nuclear localization signal(s) required for nuclear targeting of the maize regulatory protein Opaque-2. Plant Cell. 1992 Oct;4(10):1213–1227. doi: 10.1105/tpc.4.10.1213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Von Arnim Albrecht, Deng Xing-Wang. LIGHT CONTROL OF SEEDLING DEVELOPMENT. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):215–243. doi: 10.1146/annurev.arplant.47.1.215. [DOI] [PubMed] [Google Scholar]
  56. Wei N., Deng X. W. The role of the COP/DET/FUS genes in light control of arabidopsis seedling development. Plant Physiol. 1996 Nov;112(3):871–878. doi: 10.1104/pp.112.3.871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Zachgo E. A., Wang M. L., Dewdney J., Bouchez D., Camilleri C., Belmonte S., Huang L., Dolan M., Goodman H. M. A physical map of chromosome 2 of Arabidopsis thaliana. Genome Res. 1996 Jan;6(1):19–25. doi: 10.1101/gr.6.1.19. [DOI] [PubMed] [Google Scholar]

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

RESOURCES