Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1995 Dec;7(12):2187–2196. doi: 10.1105/tpc.7.12.2187

Phytochrome A and phytochrome B mediate the hypocotyl-specific downregulation of TUB1 by light in arabidopsis.

W M Leu 1, X L Cao 1, T J Wilson 1, D P Snustad 1, N H Chua 1
PMCID: PMC161072  PMID: 8718628

Abstract

Arabidopsis contains six alpha-tubulin and nine beta-tubulin genes that are expressed in a tissue-specific and developmentally regulated manner. We analyzed the effects of light on tubulin mRNA abundance in Arabidopsis seedlings using RNA gel blot hybridizations and gene-specific probes. Transcript levels of all 15 tubulin genes were decreased by continuous white light, although to different degrees. Detailed analysis was performed with the beta-tubulin TUB1 gene. The transcript level of TUB1 was high in etiolated seedlings and decreased to approximately 20% of the dark mRNA level after 2 to 6 hr of white light treatment. We showed that this downregulation requires high-irradiance light treatment and that multiple photoreceptors are involved. In particular, using phytochrome mutants and narrow wave band light, we demonstrated that both the phytochrome A (phyA)-mediated far-red light high-irradiance response and the phytochrome B (phyB)-mediated red light high-irradiance response are involved in the downregulation of TUB1 expression by white light. Histochemical analysis of transgenic plants expressing a TUB1-beta-glucuronidase chimeric transgene indicated that the downregulation observed only in hypocotyls and not in roots is controlled transcriptionally.

Full Text

The Full Text of this article is available as a PDF (3.3 MB).

Selected References

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

  1. Bachurski C. J., Theodorakis N. G., Coulson R. M., Cleveland D. W. An amino-terminal tetrapeptide specifies cotranslational degradation of beta-tubulin but not alpha-tubulin mRNAs. Mol Cell Biol. 1994 Jun;14(6):4076–4086. doi: 10.1128/mcb.14.6.4076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bowler C., Neuhaus G., Yamagata H., Chua N. H. Cyclic GMP and calcium mediate phytochrome phototransduction. Cell. 1994 Apr 8;77(1):73–81. doi: 10.1016/0092-8674(94)90236-4. [DOI] [PubMed] [Google Scholar]
  3. Bowler C., Yamagata H., Neuhaus G., Chua N. H. Phytochrome signal transduction pathways are regulated by reciprocal control mechanisms. Genes Dev. 1994 Sep 15;8(18):2188–2202. doi: 10.1101/gad.8.18.2188. [DOI] [PubMed] [Google Scholar]
  4. Brierley H. L., Webster P., Long S. R. The Pisum sativum TubA1 gene, a member of a small family of alpha-tubulin sequences. Plant Mol Biol. 1995 Feb;27(4):715–727. doi: 10.1007/BF00020225. [DOI] [PubMed] [Google Scholar]
  5. Bruce W. B., Deng X. W., Quail P. H. A negatively acting DNA sequence element mediates phytochrome-directed repression of phyA gene transcription. EMBO J. 1991 Oct;10(10):3015–3024. doi: 10.1002/j.1460-2075.1991.tb07852.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bustos M. M., Guiltinan M. J., Cyr R. J., Ahdoot D., Fosket D. E. Light Regulation of beta-Tubulin Gene Expression during Internode Development in Soybean (Glycine max [L.] Merr.). Plant Physiol. 1989 Nov;91(3):1157–1161. doi: 10.1104/pp.91.3.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carpenter J. L., Ploense S. E., Snustad D. P., Silflow C. D. Preferential expression of an alpha-tubulin gene of Arabidopsis in pollen. Plant Cell. 1992 May;4(5):557–571. doi: 10.1105/tpc.4.5.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Casal J. J. Coupling of phytochrome B to the control of hypocotyl growth in Arabidopsis. Planta. 1995;196(1):23–29. doi: 10.1007/BF00193213. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Colbert J. T., Costigan S. A., Zhao Z. Photoregulation of beta-Tubulin mRNA Abundance in Etiolated Oat and Barley Seedlings. Plant Physiol. 1990 Jul;93(3):1196–1202. doi: 10.1104/pp.93.3.1196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cyr R. J. Microtubules in plant morphogenesis: role of the cortical array. Annu Rev Cell Biol. 1994;10:153–180. doi: 10.1146/annurev.cb.10.110194.001101. [DOI] [PubMed] [Google Scholar]
  12. Davies J. P., Grossman A. R. Sequences controlling transcription of the Chlamydomonas reinhardtii beta 2-tubulin gene after deflagellation and during the cell cycle. Mol Cell Biol. 1994 Aug;14(8):5165–5174. doi: 10.1128/mcb.14.8.5165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dehesh K., Franci C., Sharrock R. A., Somers D. E., Welsch J. A., Quail P. H. The Arabidopsis phytochrome A gene has multiple transcription start sites and a promoter sequence motif homologous to the repressor element of monocot phytochrome A genes. Photochem Photobiol. 1994 Mar;59(3):379–384. doi: 10.1111/j.1751-1097.1994.tb05051.x. [DOI] [PubMed] [Google Scholar]
  14. Dixon D. C., Seagull R. W., Triplett B. A. Changes in the Accumulation of [alpha]- and [beta]-Tubulin Isotypes during Cotton Fiber Development. Plant Physiol. 1994 Aug;105(4):1347–1353. doi: 10.1104/pp.105.4.1347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Han I. S., Jongewaard I., Fosket D. E. Limited expression of a diverged beta-tubulin gene during soybean (Glycine max [L.] Merr.) development. Plant Mol Biol. 1991 Feb;16(2):225–234. doi: 10.1007/BF00020554. [DOI] [PubMed] [Google Scholar]
  16. Jabben M., Shanklin J., Vierstra R. D. Ubiquitin-phytochrome conjugates. Pool dynamics during in vivo phytochrome degradation. J Biol Chem. 1989 Mar 25;264(9):4998–5005. [PubMed] [Google Scholar]
  17. Kang M. S., Choi Y. J., Kim M. C., Lim C. O., Hwang I., Cho M. J. Isolation and characterization of two beta-tubulin cDNA clones from rice. Plant Mol Biol. 1994 Dec;26(6):1975–1979. doi: 10.1007/BF00019507. [DOI] [PubMed] [Google Scholar]
  18. Kopczak S. D., Haas N. A., Hussey P. J., Silflow C. D., Snustad D. P. The small genome of Arabidopsis contains at least six expressed alpha-tubulin genes. Plant Cell. 1992 May;4(5):539–547. doi: 10.1105/tpc.4.5.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Millar A. J., McGrath R. B., Chua N. H. Phytochrome phototransduction pathways. Annu Rev Genet. 1994;28:325–349. doi: 10.1146/annurev.ge.28.120194.001545. [DOI] [PubMed] [Google Scholar]
  20. Mösinger E., Batschauer A., Apel K., Schäfer E., Briggs W. R. Phytochrome regulation of greening in barley : effects on mRNA abundance and on transcriptional activity of isolated nuclei. Plant Physiol. 1988 Mar;86(3):706–710. doi: 10.1104/pp.86.3.706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nagatani A., Reed J. W., Chory J. Isolation and Initial Characterization of Arabidopsis Mutants That Are Deficient in Phytochrome A. Plant Physiol. 1993 May;102(1):269–277. doi: 10.1104/pp.102.1.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Neuhaus G., Bowler C., Kern R., Chua N. H. Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell. 1993 Jun 4;73(5):937–952. doi: 10.1016/0092-8674(93)90272-r. [DOI] [PubMed] [Google Scholar]
  23. Oppenheimer D. G., Haas N., Silflow C. D., Snustad D. P. The beta-tubulin gene family of Arabidopsis thaliana: preferential accumulation of the beta 1 transcript in roots. Gene. 1988;63(1):87–102. doi: 10.1016/0378-1119(88)90548-3. [DOI] [PubMed] [Google Scholar]
  24. Parks B. M., Quail P. H. hy8, a new class of arabidopsis long hypocotyl mutants deficient in functional phytochrome A. Plant Cell. 1993 Jan;5(1):39–48. doi: 10.1105/tpc.5.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Reed J. W., Nagatani A., Elich T. D., Fagan M., Chory J. Phytochrome A and Phytochrome B Have Overlapping but Distinct Functions in Arabidopsis Development. Plant Physiol. 1994 Apr;104(4):1139–1149. doi: 10.1104/pp.104.4.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Reed J. W., Nagpal P., Poole D. S., Furuya M., Chory J. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell. 1993 Feb;5(2):147–157. doi: 10.1105/tpc.5.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Snustad D. P., Haas N. A., Kopczak S. D., Silflow C. D. The small genome of Arabidopsis contains at least nine expressed beta-tubulin genes. Plant Cell. 1992 May;4(5):549–556. doi: 10.1105/tpc.4.5.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Somers D. E., Quail P. H. Phytochrome-Mediated Light Regulation of PHYA- and PHYB-GUS Transgenes in Arabidopsis thaliana Seedlings. Plant Physiol. 1995 Feb;107(2):523–534. doi: 10.1104/pp.107.2.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Takahashi T., Gasch A., Nishizawa N., Chua N. H. The DIMINUTO gene of Arabidopsis is involved in regulating cell elongation. Genes Dev. 1995 Jan 1;9(1):97–107. doi: 10.1101/gad.9.1.97. [DOI] [PubMed] [Google Scholar]
  31. Tonoike H., Han I. S., Jongewaard I., Doyle M., Guiltinan M., Fosket D. E. Hypocotyl expression and light downregulation of the soybean tubulin gene, tubB1. Plant J. 1994 Mar;5(3):343–351. doi: 10.1111/j.1365-313x.1994.00343.x. [DOI] [PubMed] [Google Scholar]
  32. Tsai F. Y., Coruzzi G. M. Dark-induced and organ-specific expression of two asparagine synthetase genes in Pisum sativum. EMBO J. 1990 Feb;9(2):323–332. doi: 10.1002/j.1460-2075.1990.tb08114.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Villemur R., Haas N. A., Joyce C. M., Snustad D. P., Silflow C. D. Characterization of four new beta-tubulin genes and their expression during male flower development in maize (Zea mays L.). Plant Mol Biol. 1994 Jan;24(2):295–315. doi: 10.1007/BF00020169. [DOI] [PubMed] [Google Scholar]
  35. Whitelam G. C., Johnson E., Peng J., Carol P., Anderson M. L., Cowl J. S., Harberd N. P. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell. 1993 Jul;5(7):757–768. doi: 10.1105/tpc.5.7.757. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES