Copper-Dependent Iron Assimilation Pathway in the Model Photosynthetic EukaryoteChlamydomonas reinhardtii

American Society for Microbiology - Tập 1 Số 5 - Trang 736-757 - 2002
Sharon La Fontaine1,2, Jeanette Quinn1, Stacie S. Nakamoto1, M. Dudley Page1, Vera Göhre1, Jeffrey L. Moseley1, Janette Kropat1, Sabeeha Merchant1,3
1Department of Chemistry and Biochemistry
2The Centre for Cellular and Molecular Biology, School of Biological and Chemical Sciences, Deakin University, Melbourne, Victoria, Australia
3Molecular Biology Institute, University of California, Los Angeles, Los Angeles, California 90095-1569

Tóm tắt

ABSTRACTThe unicellular green algaChlamydomonas reinhardtiiis a valuable model for studying metal metabolism in a photosynthetic background. A search of theChlamydomonasexpressed sequence tag database led to the identification of several components that form a copper-dependent iron assimilation pathway related to the high-affinity iron uptake pathway defined originally forSaccharomyces cerevisiae. They include a multicopper ferroxidase (encoded byFox1), an iron permease (encoded byFtr1), a copper chaperone (encoded byAtx1), and a copper-transporting ATPase. A cDNA,Fer1, encoding ferritin for iron storage also was identified. Expression analysis demonstrated thatFox1andFtr1were coordinately induced by iron deficiency, as wereAtx1andFer1, although to lesser extents. In addition, Fox1 abundance was regulated at the posttranscriptional level by copper availability. Each component exhibited sequence relationship with its yeast, mammalian, or plant counterparts to various degrees; Atx1 ofC. reinhardtiiis also functionally related with respect to copper chaperone and antioxidant activities. Fox1 is most highly related to the mammalian homologues hephaestin and ceruloplasmin; its occurrence and pattern of expression inChlamydomonasindicate, for the first time, a role for copper in iron assimilation in a photosynthetic species. Nevertheless, growth ofC. reinhardtiiunder copper- and iron-limiting conditions showed that, unlike the situation in yeast and mammals, where copper deficiency results in a secondary iron deficiency, copper-deficientChlamydomonascells do not exhibit symptoms of iron deficiency. We propose the existence of a copper-independent iron assimilation pathway in this organism.

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Tài liệu tham khảo

10.1074/jbc.M000713200

10.1016/S1367-5931(99)80033-7

10.1016/S1357-2725(99)00065-5

10.1093/dnares/6.6.369

10.1016/0092-8674(94)90346-8

10.1016/S0968-0004(98)01192-X

10.1074/jbc.272.1.401

10.1042/bj3380499

10.1016/S1360-1385(97)85225-9

10.1007/s000180050014

10.1128/AEM.65.4.1762-1768.1999

10.1016/S0962-8924(00)01833-X

Bucher P. and A. Bairoch. 1994. A generalized profile syntax for biomolecular sequences motifs and its function in automatic sequence interpretation p. 53-61. In R. Altman D. Brutlag P. Karp R. Lanthrop and D. Searls (ed.) ISMB-94. Proceedings of the 2nd International Conference on Intelligent Systems for Molecular Biology. AAAI Press Menlo Park Calif.

Burke D. D. Dawson and T. Stearns. 2000. Methods in yeast genetics. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.

10.1074/jbc.M004611200

10.1023/A:1016710810701

10.1042/bj3470749

10.1038/35053080

10.1074/jbc.272.18.11770

10.1038/35001596

10.1099/00221287-145-9-2415

Eckhardt, U., and T. J. Buckout. 1998. Iron assimilation in Chlamydomonas reinhardtii involves ferric reduction and is similar to Strategy I higher plants. J. Exp. Bot.49:1219-1226.

10.1073/pnas.93.11.5624

Eisenstein, R. S. 2000. Discovery of the ceruloplasmin homologue hephaestin: new insight into the copper/iron connection. Nutr. Rev.58:22-26.

10.1016/0003-2697(90)90238-5

Esaka, M., J. Imagi, K. Suzuki, and K. Kubota. 1988. Formation of ascorbate oxidase in cultured pumpkin cells. Plant Cell Physiol.29:231-235.

10.1074/jbc.272.3.1565

10.1074/jbc.273.28.17553

10.1146/annurev.arplant.49.1.669

Gietz R. D. and R. A. Woods. 1994. High efficiency transformation in yeast p. 121-134. In J. A. Johnston (ed.) Molecular genetics of yeast: practical approaches. Oxford University Press Oxford United Kingdom.

Grossman A. J. Davies N. Federspiel E. Harris P. Lefebvre J. P. McDermott C. Silflow D. Stern and R. Surzycki. 2000. Analyses of the Chlamydomonas reinhardtii genome: a model unicellular system for analyzing gene function and regulation in vascular plants; project phase 2.

10.1016/S0005-2736(00)00138-3

Guerinot, M. L., N. Grotz, S. Hibbard, E. Rogers, E. Connolly, and D. J. Eide. 2001. Molecular characterization of the uptake of iron and other divalent cations in Arabidopsis. J. Exp. Bot.52(Suppl.):62.

Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser.41:95-98.

10.1099/00221287-146-4-869

Harris E. H. 1989. The chlamydomonas sourcebook: a comprehensive guide to biology and laboratory use. Academic Press San Diego Calif.

10.1042/bj3510477

10.1073/pnas.84.19.6730

Herbik, A., and T. J. Buckhout. 2001. Is a ferroxidase involved in the high-affinity iron uptake in Chlamydomonas? J. Exp. Bot.52(Suppl.):80.

10.1111/j.1574-6968.2000.tb09108.x

10.1023/A:1009252118050

10.1104/pp.112.2.697

10.1016/S0021-9258(18)98586-8

10.1016/S1369-5266(00)00065-0

10.1104/pp.117.4.1227

10.1093/pcp/41.5.548

10.1016/S0092-8674(00)80747-3

10.1093/nar/27.1.215

Hofmann, K., and W. Stoffel. 1993. TMbase—a database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler374:166.

10.1023/A:1006380125438

10.1146/annurev.biochem.70.1.677

10.1074/jbc.273.3.1749

Kaplan, J., and J. P. Kushner. 2000. Mining the genome for iron. Nature403:712-713.

10.1128/JB.183.16.4866-4875.2001

10.1074/jbc.272.14.9221

10.1099/00221287-148-1-29

10.1023/A:1026438615520

10.1016/0022-2836(82)90515-0

10.1016/S0021-9258(18)94113-X

10.1128/jb.176.1.173-188.1994

10.1073/pnas.88.18.8222

10.1099/00221287-147-2-289

10.1099/00221287-144-12-3455

10.1006/jmbi.1994.1325

10.1073/pnas.92.9.3784

10.1074/jbc.272.14.9215

10.1007/s004250050267

10.1074/jbc.273.37.23716

10.1126/science.1057206

10.1016/S1097-2765(00)80425-6

Merchant S. 1997. Reciprocal copper-responsive accumulation of plastocyanin and cytochrome c6 in algae and cyanobacteria: a model for metalloregulation of metalloprotein synthesis p. 450-467. In S. Silver and W. Walden (ed.) Metal ions in gene regulation. Chapman Hall New York N.Y.

Merchant S. 1998. Synthesis of metalloproteins involved in photosynthesis: plastocyanin and cytochromes p. 597-611. In J.-D. Rochaix M. Goldschmidt-Clermont and S. Merchant (ed.) Molecular biology of Chlamydomonas: chloroplasts and mitochondria. Kluwer Academic Publishers Dordrecht The Netherlands.

10.1016/S0021-9258(18)66641-4

10.1128/mcb.6.2.462-469.1986

10.1146/annurev.arplant.49.1.25

10.1002/j.1460-2075.1991.tb07658.x

10.1111/j.1432-1033.1990.tb15311.x

Minet, M., M.-E. Dufour, and F. Lacroute. 1992. Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J.2:417-422.

10.1093/emboj/19.10.2139

10.1093/protein/10.1.1

10.1073/pnas.86.4.1239

10.1002/j.1460-2075.1996.tb00720.x

10.1074/jbc.M104122200

10.1042/bj3590575

10.1074/jbc.274.21.15041

10.1074/jbc.M109220200

10.1016/S0022-5320(80)90087-8

10.1126/science.278.5339.853

10.1016/S0076-6879(98)97020-3

10.1074/jbc.274.20.14444

10.1074/jbc.274.8.4481

10.1126/science.288.5468.1062

10.1038/17800

10.1016/S0969-2126(99)80082-3

Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.

10.1007/BF00259410

10.1097/00075197-200007000-00005

10.1093/genetics/122.1.19

10.1074/jbc.270.3.1098

10.1126/science.271.5255.1552

10.1074/jbc.275.2.1023

10.1146/annurev.bi.56.070187.001445

10.1073/pnas.97.9.4991

10.1016/S1357-2725(99)00080-1

10.1074/jbc.M011243200

10.1074/jbc.M105857200

10.1006/jmbi.1995.0274

10.1046/j.1365-313X.1999.00349.x

10.1042/bj3050959

10.1016/0022-2836(92)90934-C

10.1038/5979

10.1016/S0014-5793(98)01431-8

10.1042/bj3370523

10.1007/s004250050495

10.1046/j.1365-313X.1996.10050835.x

10.1074/jbc.272.41.25787

10.1073/pnas.92.7.2632

10.1074/jbc.275.14.10709

10.1074/jbc.M001456200