Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus

EMBO Journal

Volumn 21, Issue 24, 2002, Pages 6709-6720

  Moseley, Jeffrey L ^a   Allinger, Tanja ^b   Herzog, Sebastian ^c   Hoerth, Patric ^c   Wehinger, Elke ^a   Merchant, Sabeeha ^a   Hippler, Michael ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Chlamydomonas reinhardtii; Fe deficiency; Light harvesting proteins; Photosystem I; Proteomics

Indexed keywords

ARTICLE; CHLOROSIS; CONTROLLED STUDY; ELECTRON TRANSPORT; IRON DEFICIENCY; MOLECULAR MECHANICS; NONHUMAN; NUTRITIONAL STATUS; PHOTOOXIDATION; PHOTOSYNTHESIS; PHOTOSYSTEM I; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; STOICHIOMETRY; TRANSPORT KINETICS;

ANIMALS; CHLAMYDOMONAS REINHARDTII; CHLORINE; CHLOROPHYLL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION; IMMUNOBLOTTING; IRON; LIGHT-HARVESTING PROTEIN COMPLEXES; MASS SPECTROMETRY; PEPTIDES; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PLANT PROTEINS; PLASTIDS; PROTEOME; RNA; SPECTROMETRY, FLUORESCENCE; TIME FACTORS;

CHLAMYDOMONAS REINHARDTII;

EID: 12244262259     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf666     Document Type: Article

References (47)

1. Bassi, R., Soen, S.Y., Frank, G., Zuber, H. and Rochaix, J.D. (1992) Characterization of chlorophyll a/b proteins of photosystem I from Chlamydomonas reinhardtii. J. Biol. Chem., 267, 25714-25721.
2. Bennoun, P. and Delepelaire, P. (1982) Isolation of photosynthesis mutants in Chlamydomonas. In Edelman, M., Hallick, R.B. and Chua, N.-H. (eds), Methods in Chloroplast Molecular Biology. Elsevier Biomedical Press, Amsterdam, The Netherlands, pp. 25-38.
3. Bibby, T.S., Nield, J. and Barber, J. (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature, 412, 743-745.
4. Boekema, E.J., Hifney, A., Yakushevska, A.E., Piotrowski, M., Keegstra, W., Berry, S., Michel, K.P., Pistorius, E.K. and Kruip, J. (2001) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature, 412, 745-748
5. Burnap, R.L., Troyan, T. and Sherman, L.A. (1993) The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43′) is encoded by the isiA gene. Plant Physiol., 103, 893-902.
6. Chereskin, B.M. and Castelfranco, P.A. (1982) Effects of iron and oxygen on chlorophyll biosynthesis. II. Observations on the biosynthetic pathway in isolated etiochloroplasts. Plant Physiol., 68, 112-116.
7. Chua, N.H. and Bennoun, P. (1975) Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: Wild-type and mutant strains deficient in photosystem II reaction center. Proc. Natl. Acad. Sci. USA, 72, 2175-2179.
8. Farah, J., Rappaport, F., Choquet, Y., Joliot, P. and Rochaix, J.D. (1995) Isolation of a psaF-deficient mutant of Chlamydomonas reinhardtii: Efficient interaction of plastocyanin with the photosystem I reaction center is mediated by the PsaF subunit. EMBO J., 14, 4976-4984.
9. Fleischmann, M.M., Ravanel, S., Delosme, R., Olive, J., Zito, F., Wollman, F.A. and Rochaix, J.D. (1999) Isolation and characterization of photoautotrophic mutants of Chlamydomonas reinhardtii deficient in state transition. J. Biol. Chem., 274, 30987-30994.
10. Franzen, L.G., Frank, G., Zuber, H. and Rochaix, J.D. (1989) Isolation and characterization of cDNA clones encoding photosystem I subunits with molecular masses 11.0, 10.0 and 8.4 kDa from Chlamydomonas reinhardtii. Mol. Gen. Genet., 219, 137-144.
11. Guikema, J.A. and Straus, N.A. (1983) Influence of iron deprivation on the membrane composition of Anacystis nidulans. Plant Physiol., 74, 90-95.
12. Harris, E.H. (1989) The Chlamydomonas Sourcebook. A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego, CA.
13. Hippler, M., Drepper, F., Farah, J. and Rochaix, J.D. (1997) Fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochemistry, 36, 6343-6349.
14. Hippler, M., Biehler, K., Krieger-Liszkay, A., van Dillewjin, J. and Rochaix, J.D. (2000) Limitation in electron transfer in photosystem I donor side mutants of Chlamydomonas reinhardtii. Lethal photooxidative damage in high light is overcome in a suppressor strain deficient in the assembly of the light harvesting complex. J. Biol. Chem., 275, 5852-5859.
15. Hippler, M., Klein, J., Fink, T., Allinger, T. and Hoerth, P. (2001) Towards functional proteomics of membrane protein complexes: Analysis of thylakoid membranes from Chlamydomonas reinhardtii. Plant J., 28, 595-606.
16. Jansson, S., Andersen, B. and Scheller, H.V. (1996) Nearest-neighbor analysis of higher-plant photosystem I holocomplex. Plant Physiol., 112, 409-420
17. Jensen, P.E., Gilpin, M., Knoetzel, J. and Scheller, H.V. (2000) The PSI-K subunit of photosystem I is involved in the interaction between light-harvesting complex I and the photosystem I reaction center core. J. Biol. Chem., 275, 24701-24708.
18. Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W. and Krauss, N. (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature, 411, 909-917.
19. Krause, G.H. and Weise, E. (1991) Chlorophyll fluorescence and photosynthesis: The basics. Annu. Rev. Plant Physiol. Plant Mol. Biol., 42, 313-349.
20. La Fontaine, S., Quinn, J., Nakamoto, S., Page, M.D., Göhre, V., Moseley, J.L., Kropat, J. and Merchant, S. (2002) A copper-dependent iron assimilation pathway in the model photosynthetic eukaryote, Chlamydomonas reinhardtii. Eukaryot. Cell, 1, 736-757.
21. Laudenbach, D.E. and Straus, N.A. (1988) Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J. Bacteriol., 170, 5018-5026.
22. Li, X.P., Bjorkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S. and Niyogi, K.K. (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature, 403, 391-395.
23. Lindahl, M., Yang, D.H. and Andersson, B. (1995) Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein of photosystem II by a light-induced membrane-associated enzymic system. Eur. J. Biochem., 231, 503-509.
24. Malnoe, P., Mayfield, S.P. and Rochaix, J.D. (1988) Comparative analysis of the biogenesis of photosystem II in the wild-type and Y-1 mutant of Chlamydomonas reinhardtii. J. Cell Biol., 106, 609-616.
25. Marschner, H. (1995) Mineral Nutrition of Higher Plants. Academic Press, San Diego, CA.
26. Moseley, J., Quinn, J., Eriksson, M. and Merchant, S. (2000) The Crd1 gene encodes a putative di-iron enzyme required for photosystem I accumulation in copper deficiency and hypoxia in Chlamydomonas reinhardtii. EMBO J., 19, 2139-2151.
27. Moseley, J.L., Page, M.D., Pergam, N., Eriksson, M., Quinn, J., Soto, J., Theg, S., Hippler, M. and Merchant, S. (2002) Reciprocal expression of two di-iron enzymes affecting photosystem I and light-harvesting complex accumulation. Plant Cell, 14, 673-688.
28. Mullet, J.E., Klein, P.G. and Klein, R.R. (1990) Chlorophyll regulates accumulation of the plastid-encoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stability. Proc. Natl. Acad. Sci. USA, 87, 4038-4042.
29. Pinta, V., Picaud, M., Reiss-Husson, F. and Astier, C. (2002) Rubrivivax gelatinosus acsF (previously orf358) codes for a conserved, putative binuclear-iron-cluster-containing protein involved in aerobic oxidative cyclization of Mg-protoporphyrin IX monomethylester. J. Bacteriol., 184, 746-753.
30. Porra, R.J., Thompson, W.A. and Kriedemann, P.E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta, 975, 384-394.
31. Quinn, J.M. and Merchant, S. (1998) Copper-responsive gene expression during adaptation to copper deficiency. Methods Enzymol., 297, 263-279.
32. Quinn, J.M., Nakamoto, S.S. and Merchant, S. (1999) Induction of coproporphyrinogen oxidase in Chlamydomonas chloroplasts occurs via transcriptional regulation of Cpx1 mediated by copper response elements and increased translation from a copper deficiency-specific form of the transcript. J. Biol. Chem., 274, 14444-14454.
33. 2 photoproduction in Chlamydomonas reinhardtii. J. Biol. Chem., 274, 10466-10473.
34. Sandstrom, S., Park, Y.I., Oquist, G. and Gustafsson, P. (2001) CP43′, the isiA gene product, functions as an excitation energy dissipator in the cyanobacterium Synechococcus sp. PCC 7942. Photochem. Photobiol., 74, 431-437.
35. Schägger, H. and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa, Anal, Biochem., 166, 368-379.
36. Schmid, V.H.R., Paulsen, H. and Rupprecht, J. (2002) Identification of N-and C-terminal amino acids of Lhcal and Lhca4 required for formation of the heterodimeric photosystem I antenna LHCI-730. Biochemistry, 41, 9126-9131.
37. Spiller, S. and Terry, N. (1980) Limiting factors in photosynthesis. II. Iron stress diminishes photochemical capacity by reducing the number of photosynthetic units. Plant Physiol., 65, 121-125.
38. Spiller, S.C., Castelfranco, A.M. and Castelfranco, P.A. (1982) Effects of iron and oxygen on chlorophyll biosynthesis I. In vivo observations on iron and oxygen-deficient plants. Plant Physiol., 69, 107-111.
39. Spreitzer, R.J. and Mets, L. (1981) Photosynthesis-deficient mutants of Chlamydomonas reinhardtii with associated light-sensitive phenotypes. Plant Physiol., 67, 565-569.
40. Straus, N.A. (1994) Iron Deprivation: Physiology and Gene Regulation. Kluwer Academic Publisher, Dordrecht, The Netherlands.
41. Sutton, A., Sieburth, L.E. and Bennett, J. (1987) Light-dependent accumulation and localization of photosystem II proteins in maize. Eur. J. Biochem., 164, 571-578.
42. Taiz, L. and Zeiger, E. (1998) Plant Physiology. Sinauer Associates, Inc., Sunderland, MA.
43. Terry, N. (1980) Limiting factors in photosynthesis. I. Use of iron stress to control photochemical capacity in vivo. Plant Physiol., 65, 114-120.
44. Wilm, M., Neubauer, G. and Mann, M. (1996) Parent ion scans of unseparated peptide mixtures. Anal. Chem., 68, 527-533.
45. Wollman, F.-A. and Bennoun, P. (1982) A new chlorophyll-protein complex related to photosystem I in Chlamydomonas reinhardtii. Biochim. Biophys. Acta, 680, 352-360.
46. Wollman, F.A. and Delepelaire, P. (1984) Correlation between changes in light energy distribution and changes in thylakoid membrane polypeptide phosphorylation in Chlamydomonas reinhardtii. J. Cell Biol., 98, 1-7.
47. Yang, D.H., Webster, J., Adam, Z., Lindahl, M. and Andersson, B. (1998) Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of photosystem II in response to elevated light intensities. Plant Physiol., 118, 827-834.