Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1995 Nov;109(3):787–795. doi: 10.1104/pp.109.3.787

Redox Regulation of Light-Harvesting Complex II and cab mRNA Abundance in Dunaliella salina.

D P Maxwell 1, D E Laudenbach 1, NPA Huner 1
PMCID: PMC161378  PMID: 12228633

Abstract

We demonstrate that photosynthetic adjustment at the level of the light-harvesting complex associated with photosystem II (LCHII) in Dunaliella salina is a response to changes in the redox state of intersystem electron transport as estimated by photosystem II (PSII) excitation pressure. To elucidate the molecular basis of this phenomenon, LHCII apoprotein accumulation and cab mRNA abundance were examined. Growth regimes that induced low, but equivalent, excitation pressures (either 13[deg]C/20 [mu]mol m-2 s-1 or 30[deg]C/150 ([mu]mol m-2 s-1) resulted in increased LHCII apoprotein and cab mRNA accumulation relative to algal cultures grown under high excitation pressures (either 13[deg]C/150 [mu]mol m-2 s-1 or 30[deg]C/2500 [mu]mol m-2 s-1). Thermodynamic relaxation of high excitation pressures, accomplished by shifting cultures from a 13 to a 30[deg]C growth regime at constant irradiance for 12 h, resulted in a 6- and 8-fold increase in LHCII apoprotein and cab mRNA abundance, respectively. Similarly, photodynamic relaxation of high excitation pressure, accomplished by a shift from a light to a dark growth regime at constant temperature, resulted in a 2.4- to 4-fold increase in LHCII apoprotein and cab mRNA levels, respectively. We conclude that photosynthetic adjustment to temperature mimics adjustment to high irradiance through a common redox sensing/signaling mechanism. Both temperature and light modulate the redox state of the first, stable quinone electron acceptor of PSII, which reflects the redox poise of intersystem electron transport. Changes in redox poise signal the nucleus to regulate cab mRNA abundance, which, in turn, determines the accumulation of light-harvesting apoprotein. This redox mechanism may represent a general acclimation mechanism for photosynthetic adjustment to environmental stimuli.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

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

  1. Aro E. M., Virgin I., Andersson B. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta. 1993 Jul 5;1143(2):113–134. doi: 10.1016/0005-2728(93)90134-2. [DOI] [PubMed] [Google Scholar]
  2. Bowler C., Chua N. H. Emerging themes of plant signal transduction. Plant Cell. 1994 Nov;6(11):1529–1541. doi: 10.1105/tpc.6.11.1529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bradbury M., Baker N. R. Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of photosystem II electron acceptors and fluorescence emission from photosystems I and II. Biochim Biophys Acta. 1981 May 13;635(3):542–551. doi: 10.1016/0005-2728(81)90113-4. [DOI] [PubMed] [Google Scholar]
  4. Cline K., Werner-Washburne M., Lubben T. H., Keegstra K. Precursors to two nuclear-encoded chloroplast proteins bind to the outer envelope membrane before being imported into chloroplasts. J Biol Chem. 1985 Mar 25;260(6):3691–3696. [PubMed] [Google Scholar]
  5. Dahlin C., Cline K. Developmental Regulation of the Plastid Protein Import Apparatus. Plant Cell. 1991 Oct;3(10):1131–1140. doi: 10.1105/tpc.3.10.1131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dreyfuss B. W., Thornber J. P. Assembly of the Light-Harvesting Complexes (LHCs) of Photosystem II (Monomeric LHC IIb Complexes Are Intermediates in the Formation of Oligomeric LHC IIb Complexes). Plant Physiol. 1994 Nov;106(3):829–839. doi: 10.1104/pp.106.3.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ellis R. J. Photoregulation of plant gene expression. Biosci Rep. 1986 Feb;6(2):127–136. doi: 10.1007/BF01114998. [DOI] [PubMed] [Google Scholar]
  8. Gao J., Kaufman L. S. Blue-Light Regulation of the Arabidopsis thaliana Cab1 Gene. Plant Physiol. 1994 Apr;104(4):1251–1257. doi: 10.1104/pp.104.4.1251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gilmartin P. M., Sarokin L., Memelink J., Chua N. H. Molecular light switches for plant genes. Plant Cell. 1990 May;2(5):369–378. doi: 10.1105/tpc.2.5.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hermsmeier D., Mala E., Schulz R., Thielmann J., Galland P., Senger H. Antagonistic blue- and red-light regulation of cab-gene expression during photosynthetic adaptation in Scenedesmus obliquus. J Photochem Photobiol B. 1991 Nov;11(2):189–202. doi: 10.1016/1011-1344(91)80260-o. [DOI] [PubMed] [Google Scholar]
  11. Jansson S. The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta. 1994 Feb 8;1184(1):1–19. doi: 10.1016/0005-2728(94)90148-1. [DOI] [PubMed] [Google Scholar]
  12. Jasper F., Quednau B., Kortenjann M., Johanningmeier U. Control of cab gene expression in synchronized Chlamydomonas reinhardtii cells. J Photochem Photobiol B. 1991 Nov;11(2):139–150. doi: 10.1016/1011-1344(91)80256-h. [DOI] [PubMed] [Google Scholar]
  13. Johanningmeier U., Howell S. H. Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardi. Possible involvement of chlorophyll synthesis precursors. J Biol Chem. 1984 Nov 10;259(21):13541–13549. [PubMed] [Google Scholar]
  14. Johanningmeier U. Possible control of transcript levels by chlorophyll precursors in Chlamydomonas. Eur J Biochem. 1988 Nov 1;177(2):417–424. doi: 10.1111/j.1432-1033.1988.tb14391.x. [DOI] [PubMed] [Google Scholar]
  15. Król M., Spangfort M. D., Huner N. P., Oquist G., Gustafsson P., Jansson S. Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutant. Plant Physiol. 1995 Mar;107(3):873–883. doi: 10.1104/pp.107.3.873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Laroche J., Mortain-Bertrand A., Falkowski P. G. Light Intensity-Induced Changes in cab mRNA and Light Harvesting Complex II Apoprotein Levels in the Unicellular Chlorophyte Dunaliella tertiolecta. Plant Physiol. 1991 Sep;97(1):147–153. doi: 10.1104/pp.97.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Laudenbach D. E., Reith M. E., Straus N. A. Isolation, sequence analysis, and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2. J Bacteriol. 1988 Jan;170(1):258–265. doi: 10.1128/jb.170.1.258-265.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Leheny E. A., Theg S. M. Apparent Inhibition of Chloroplast Protein Import by Cold Temperatures Is Due to Energetic Considerations Not Membrane Fluidity. Plant Cell. 1994 Mar;6(3):427–437. doi: 10.1105/tpc.6.3.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Long Z. F., Wang S. Y., Nelson N. Cloning and nucleotide sequence analysis of genes coding for the major chlorophyll-binding protein of the moss Physcomitrella patens and the halotolerant alga Dunaliella salina. Gene. 1989;76(2):299–312. doi: 10.1016/0378-1119(89)90170-4. [DOI] [PubMed] [Google Scholar]
  20. Maxwell D. P., Falk S., Huner NPA. Photosystem II Excitation Pressure and Development of Resistance to Photoinhibition (I. Light-Harvesting Complex II Abundance and Zeaxanthin Content in Chlorella vulgaris). Plant Physiol. 1995 Mar;107(3):687–694. doi: 10.1104/pp.107.3.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Maxwell D. P., Falk S., Trick C. G., Huner NPA. Growth at Low Temperature Mimics High-Light Acclimation in Chlorella vulgaris. Plant Physiol. 1994 Jun;105(2):535–543. doi: 10.1104/pp.105.2.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pearson C. K., Wilson S. B., Schaffer R., Ross A. W. NAD turnover and utilisation of metabolites for RNA synthesis in a reaction sensing the redox state of the cytochrome b6f complex in isolated chloroplasts. Eur J Biochem. 1993 Dec 1;218(2):397–404. doi: 10.1111/j.1432-1033.1993.tb18389.x. [DOI] [PubMed] [Google Scholar]
  23. Qian K. X., Pi K. D., Wang Y. P., Zhao M. J. Toward an implantable impeller total heart. ASAIO Trans. 1987 Jul-Sep;33(3):704–707. [PubMed] [Google Scholar]
  24. Smith B. M., Morrissey P. J., Guenther J. E., Nemson J. A., Harrison M. A., Allen J. F., Melis A. Response of the Photosynthetic Apparatus in Dunaliella salina (Green Algae) to Irradiance Stress. Plant Physiol. 1990 Aug;93(4):1433–1440. doi: 10.1104/pp.93.4.1433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Thomas P. S. Hybridization of denatured RNA transferred or dotted nitrocellulose paper. Methods Enzymol. 1983;100:255–266. doi: 10.1016/0076-6879(83)00060-9. [DOI] [PubMed] [Google Scholar]
  26. Vasilikiotis C., Melis A. Photosystem II reaction center damage and repair cycle: chloroplast acclimation strategy to irradiance stress. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7222–7226. doi: 10.1073/pnas.91.15.7222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Webb M. R., Melis A. Chloroplast Response in Dunaliella salina to Irradiance Stress (Effect on Thylakoid Membrane Protein Assembly and Function). Plant Physiol. 1995 Mar;107(3):885–893. doi: 10.1104/pp.107.3.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yamamoto N., Mukai Y., Matsuoka M., Kano-Murakami Y., Tanaka Y., Ohashi Y., Ozeki Y., Odani K. Light-Independent Expression of cab and rbcS Genes in Dark-Grown Pine Seedlings. Plant Physiol. 1991 Feb;95(2):379–383. doi: 10.1104/pp.95.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES