Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1988 May;7(5):1289–1297. doi: 10.1002/j.1460-2075.1988.tb02943.x

Light-dependent changes in psbD and psbC transcripts of barley chloroplasts: accumulation of two transcripts maintains psbD and psbC translation capability in mature chloroplasts.

P E Gamble 1, T B Sexton 1, J E Mullet 1
PMCID: PMC458376  PMID: 3044778

Abstract

The psbD and psbC genes encode two polypeptides of Photosystem II. These genes are adjacent in the barley chloroplast genome and are part of a 5.7 kbp transcription unit. In dark-grown barley, four large transcripts hybridize to psbD and psbC; two additional transcripts hybridize to psbC. Illumination of 4.5-day-old dark-grown seedlings causes a decrease in the six psbD--psbC transcripts found in etioplasts and the accumulation of two different transcripts of 4.0 and 3.2 kb which hybridize to psbD and psbC. The light-induced transcripts have a common 5' end approximately 600 nt upstream of psbD and 3' ends 1175 and 175 nt downstream of psbC. The shift in psbD--psbC transcript population occurs during a phase of chloroplast maturation when transcript levels and translation of chloroplast genes such as psaA--psaB and psbB decline approximately 3- to 5-fold. In contrast, translation of the psbD and psbC gene products declines to a lesser extent, suggesting that the light-induced accumulation of the 4.0 and 3.2 kb psbD--psbC transcripts is required to maintain psbD and psbC gene product translation in mature chloroplasts.

Full text

PDF
1289

Images in this article

1290Image
on p.1290
1291Image
on p.1291
1292Image
on p.1292
1293Image
on p.1293
1294Image
on p.1294
1294Image
on p.1294
1294Image
on p.1294

Selected References

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

  1. Altman A., Cohen B. N., Weissbach H., Brot N. Transcriptional activity of isolated maize chloroplasts. Arch Biochem Biophys. 1984 Nov 15;235(1):26–33. doi: 10.1016/0003-9861(84)90251-0. [DOI] [PubMed] [Google Scholar]
  2. Apel K. Phytochrome-induced appearance of mRNA activity for the apoprotein of the light-harvesting chlorophyll a/b protein of barley (Hordeum vulgare). Eur J Biochem. 1979 Jun;97(1):183–188. doi: 10.1111/j.1432-1033.1979.tb13101.x. [DOI] [PubMed] [Google Scholar]
  3. Bedbrook J. R., Link G., Coen D. M., Bogorad L. Maize plastid gene expressed during photoregulated development. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3060–3064. doi: 10.1073/pnas.75.7.3060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bennett J. Biosynthesis of the light-harvesting chlorophyll a/b protein. Polypeptide turnover in darkness. Eur J Biochem. 1981 Aug;118(1):61–70. doi: 10.1111/j.1432-1033.1981.tb05486.x. [DOI] [PubMed] [Google Scholar]
  5. Berends T., Gamble P. E., Mullet J. E. Characterization of the barley chloroplast transcription units containing psaA-psaB and psbD-psbC. Nucleic Acids Res. 1987 Jul 10;15(13):5217–5240. doi: 10.1093/nar/15.13.5217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Translational regulation of light-induced ribulose 1,5-bisphosphate carboxylase gene expression in amaranth. Mol Cell Biol. 1986 Jul;6(7):2347–2353. doi: 10.1128/mcb.6.7.2347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  8. Crossland L. D., Rodermel S. R., Bogorad L. Single gene for the large subunit of ribulosebisphosphate carboxylase in maize yields two differentially regulated mRNAs. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4060–4064. doi: 10.1073/pnas.81.13.4060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deisenhofer J., Epp O., Miki K., Huber R., Michel H. X-ray structure analysis of a membrane protein complex. Electron density map at 3 A resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol. 1984 Dec 5;180(2):385–398. doi: 10.1016/s0022-2836(84)80011-x. [DOI] [PubMed] [Google Scholar]
  10. Ellis R. J. Photoregulation of plant gene expression. Biosci Rep. 1986 Feb;6(2):127–136. doi: 10.1007/BF01114998. [DOI] [PubMed] [Google Scholar]
  11. Erickson J. M., Rahire M., Malnoë P., Girard-Bascou J., Pierre Y., Bennoun P., Rochaix J. D. Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects photosystem II stability and D1 expression. EMBO J. 1986 Aug;5(8):1745–1754. doi: 10.1002/j.1460-2075.1986.tb04422.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fromm H., Devic M., Fluhr R., Edelman M. Control of psbA gene expression: in mature Spirodela chloroplasts light regulation of 32-kd protein synthesis is independent of transcript level. EMBO J. 1985 Feb;4(2):291–295. doi: 10.1002/j.1460-2075.1985.tb03628.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gollmer I., Apel K. The phytochrome-controlled accumulation of mRNA sequences encoding the light-harvesting chlorophyll a/b protein of barley (Hordeum vulgare L.). Eur J Biochem. 1983 Jun 15;133(2):309–313. doi: 10.1111/j.1432-1033.1983.tb07463.x. [DOI] [PubMed] [Google Scholar]
  14. Gounaris K., Barber J., Harwood J. L. The thylakoid membranes of higher plant chloroplasts. Biochem J. 1986 Jul 15;237(2):313–326. doi: 10.1042/bj2370313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hanley-Bowdoin L., Orozco E. M., Jr, Chua N. H. In vitro synthesis and processing of a maize chloroplast transcript encoded by the ribulose 1,5-bisphosphate carboxylase large subunit gene. Mol Cell Biol. 1985 Oct;5(10):2733–2745. doi: 10.1128/mcb.5.10.2733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Holschuh K., Bottomley W., Whitfeld P. R. Structure of the spinach chloroplast genes for the D2 and 44 kd reaction-centre proteins of photosystem II and for tRNASer (UGA). Nucleic Acids Res. 1984 Dec 11;12(23):8819–8834. doi: 10.1093/nar/12.23.8819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Klein R. R., Mullet J. E. Control of gene expression during higher plant chloroplast biogenesis. Protein synthesis and transcript levels of psbA, psaA-psaB, and rbcL in dark-grown and illuminated barley seedlings. J Biol Chem. 1987 Mar 25;262(9):4341–4348. [PubMed] [Google Scholar]
  18. Klein R. R., Mullet J. E. Regulation of chloroplast-encoded chlorophyll-binding protein translation during higher plant chloroplast biogenesis. J Biol Chem. 1986 Aug 25;261(24):11138–11145. [PubMed] [Google Scholar]
  19. Kreuz K., Dehesh K., Apel K. The light-dependent accumulation of the P700 chlorophyll a protein of the photosystem I reaction center in barley. Evidence for translational control. Eur J Biochem. 1986 Sep 15;159(3):459–467. doi: 10.1111/j.1432-1033.1986.tb09908.x. [DOI] [PubMed] [Google Scholar]
  20. Kyle D. J., Ohad I., Arntzen C. J. Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4070–4074. doi: 10.1073/pnas.81.13.4070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Link D. P., Lantz B. M. Vasodilator response in the lower extremity induced by contrast medium. I Canine model. Acta Radiol Diagn (Stockh) 1982;23(2):81–86. doi: 10.1177/028418518202300201. [DOI] [PubMed] [Google Scholar]
  22. Mattoo A. K., Hoffman-Falk H., Marder J. B., Edelman M. Regulation of protein metabolism: Coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1380–1384. doi: 10.1073/pnas.81.5.1380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  24. Mullet J. E., Klein R. R., Grossman A. R. Optimization of protein synthesis in isolated higher plant chloroplasts. Identification of paused translation intermediates. Eur J Biochem. 1986 Mar 3;155(2):331–338. doi: 10.1111/j.1432-1033.1986.tb09495.x. [DOI] [PubMed] [Google Scholar]
  25. Mullet J. E., Klein R. R. Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J. 1987 Jun;6(6):1571–1579. doi: 10.1002/j.1460-2075.1987.tb02402.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mösinger E., Batschauer A., Schäfer E., Apel K. Phytochrome control of in vitro transcription of specific genes in isolated nuclei from barley (Hordeum vulgare). Eur J Biochem. 1985 Feb 15;147(1):137–142. doi: 10.1111/j.1432-1033.1985.tb08729.x. [DOI] [PubMed] [Google Scholar]
  27. Nanba O., Satoh K. Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci U S A. 1987 Jan;84(1):109–112. doi: 10.1073/pnas.84.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nelson T., Harpster M. H., Mayfield S. P., Taylor W. C. Light-regulated gene expression during maize leaf development. J Cell Biol. 1984 Feb;98(2):558–564. doi: 10.1083/jcb.98.2.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ohad I., Kyle D. J., Hirschberg J. Light-dependent degradation of the Q(B)-protein in isolated pea thylakoids. EMBO J. 1985 Jul;4(7):1655–1659. doi: 10.1002/j.1460-2075.1985.tb03833.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rodermel S. R., Bogorad L. Maize plastid photogenes: mapping and photoregulation of transcript levels during light-induced development. J Cell Biol. 1985 Feb;100(2):463–476. doi: 10.1083/jcb.100.2.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Silverthorne J., Tobin E. M. Demonstration of transcriptional regulation of specific genes by phytochrome action. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1112–1116. doi: 10.1073/pnas.81.4.1112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vierling E., Alberte R. S. Regulation of synthesis of the photosystem I reaction center. J Cell Biol. 1983 Dec;97(6):1806–1814. doi: 10.1083/jcb.97.6.1806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Westhoff P., Farchaus J. W., Herrmann R. G. The gene for the Mr 10,000 phosphoprotein associated with photosystem II is part of the psbB operon of the spinach plastid chromosome. Curr Genet. 1986;11(3):165–169. doi: 10.1007/BF00420602. [DOI] [PubMed] [Google Scholar]
  35. Zhu Y. S., Kung S. D., Bogorad L. Phytochrome control of levels of mRNA complementary to plastid and nuclear genes of maize. Plant Physiol. 1985 Oct;79(2):371–376. doi: 10.1104/pp.79.2.371. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES