Chlamydomonas reinhardtii as a eukaryotic photosynthetic model for studies of heavy metal homeostasis and tolerance

New Phytologist

Volumn 159, Issue 2, 2003, Pages 331-340

  Hanikenne, M ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Cadmium (Cd); Chlamydomonas; Copper (Cu); Heavy metal homeostasis; Heavy metal tolerance; Iron (Fe)

Indexed keywords

HEAVY METAL; HOMEOSTASIS; PHYTOTOXICITY; TOLERANCE;

ALGAE; BACTERIA (MICROORGANISMS); CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; EUKARYOTA; PROTISTA;

EID: 0042964867     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1469-8137.2003.00788.x     Document Type: Review

References (92)

1. Adam M, Lentz KE, Loppes R. 1993. Insertional mutagenesis to isolate acetate-requiring mutants in Chlamydomonas reinhardtii. FEMS Microbiology Letters 110: 265-268.
2. 2 adapted cells of Chlamydomonas reinhardtii. DNA Research 7: 305-307.
3. Asamizu E, Nakamura Y, Sato S, Fukuzawa H, Tahata S. 1999. A large scale structural analysis of cDNAs in a unicellular green alga, Chlamydomonas reinhardtii. I. Generation of 3433 non-redundant expressed sequence tags. DNA Research 6: 369-373.
4. Askwith C, Kaplan J. 1998. Iron and copper transport in yeast and its relevance to human disease. Trends in Biochemical Sdence 23: 135-138.
5. Ben-Bassat D, Shelef G, Gruner N, Shuval HI. 1972. Growth of Chlamydomonas in a medium containing mercury. Nature 240: 43-44.
6. Boswell C, Sharma NC, Sahi SV. 2002. Copper tolerance and accumulation potential of Chlamydomonas reinhardtii. Bulletin of Environmental Contamination and Toxicology 69: 546-553.
7. Cerutti H, Johnson AM, Gillham NW, Boynton JE. 1997. A eubacterial gene conferring spectinomycin resistance on Chlamydomonas reinhardtii: integration into the nuclear genome and gene expression. Genetics 145: 97-110.
8. Clemens S. 2001. Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212: 475-486.
9. Clemens S, Palmgren MG, Kraemer U. 2002. A long way ahead: understanding and engineering plant metal accumulation. Trends in Plant Science 7: 309-315.
10. Cobbett CS. 2000. Phytochelatin biosynthesis and function in heavy-metal detoxification. Current Opinion in Plant Biology 3: 211-216.
11. Cobbett C, Goldsbrough P. 2002. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Physiology and Plant Molecular Biology 53: 159-182.
12. Collard JM, Matagne RF. 1990. Isolation and genetic analysis of Chlamydomonas reinhardtii strains resistant to cadmium. Applied and Environmental Microbiology 56: 2051-2055.
13. 2+ resistance in wild-type and mutant strains of Chlamydomonas reinhardtii. Environmental and Experimental Botany 34: 235-244.
14. Davies JP, Grossman A. 1998. The use of Chlamydomonas (Chlorophyta: Volvocales) as a model algal system for genome studies and the elucidation of photosynthetic processes. Journal of Phycology 34: 907-917.
15. Davies JP, Yildiz F, Grossman A. 1994. Mutants of Chlamydomonas with aberrant responses to sulfur deprivation. Plant Cell 6: 53-63.
16. Dent RM, Han M, Niyogi KK. 2001. Functional genomics of plant photosynthesis in the fast lane using Chlamydomonas reinhardtii. Trends in Plant Science 6: 364-371.
17. Devriese M, Tsakaloudi V, Garbayo I, Leon R, Vilchez C, Vigara J. 2001. Effect of heavy metals on nitrate assimilation in the eukaryotic microalga Chlamydomonas reinhardtii. Plant Physiology and Biochemistry 39: 443-448.
18. Eckhardt U, Buckhout TJ. 1998. Iron assimilation in Chlamydomonas reinhardtii involves ferric reduction and is similar to strategy I higher plants. Journal of Experimental Botany 49: 1219-1226.
19. Fuhrmann M. 2002. Expanding the molecular toolkit for Chlamydomonas reinhardtii - from history to new frontiers. Protist 153: 357-364.
20. Fuhrmann M, Oertel W, Hegemann P. 1999. A synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii. Plant Journal 19: 353-361.
21. Fuhrmann M, Stahlberg A, Govorunova E, Rank S, Hegemann P. 2001. The abundant retinal protein of the Chlamydomonaseye is not the photoreceptor for phototaxis and photophobic responses. Journal of Cell Science 114: 3857-3863.
22. Fujiwara S, Kobayashi I, Hoshino S, Kaise T, Shimogawara K, Usuda H, Tsuzuki M. 2000. Isolation and characterization of arsenate-sensitive and resistant mutants of Chlamydomonas reinhardtii. Plant and Cell Physiology 41: 77-83.
23. Gekeler W, Grill E, Winnacker EL, Zenk MH. 1989. Algae sequester heavy metals via synthesis of phytochelatin complexes. Archives of Microbiology 150: 197-202.
24. Goldschmidt-Clermont M. 1998. Chloroplast transformation and reverse genetics. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S, eds. The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Dordrecht, The Netherlands: Kluwer Academic Publishers, 139-149.
25. Goyer RA. 1997. Toxic and essential metal interactions. Annual Review of Nutrition 17: 37-50.
26. Grossman AR. 2000. Chlamydomonas reinhardtii and photosynthesis: genetics to genomics. Current Opinion in Plant Biology 3: 132-137.
27. Gumpel NJ, Purton S. 1994. Playing tag with Chlamydomonas. Trends in Cell Biology 4: 299-301.
28. Hanikenne M, Matagne RF, Loppes R. 2001. Pleiotropic mutants hypersensitive to heavy metals and to oxidative stress in Chlamydomonas reinhardtii. FEMS Microbiology Letters 196: 107-111.
29. Harris EH. 1989. The Chlamydomonas sourcebook, a comprehensive guide to biology and laboratory use. New York, USA: Academic Press, Inc.
30. Harris EH. 2001. Chlamydomonas as a model organism. Annual Review of Plant Physiology and Plant Molecular Biology 52: 363-406.
31. Herbik A, Bolling C, Buckhout TJ. 2002. The involvement of a multicopper oxidase in iron uptake by the green alga Chlamydomonas reinhardtii. Plant Physiology 130: 2039-2048.
32. Hill KL, Hassett R, Kosman D, Merchant S. 1996. Regulated copper uptake in Chlamydomonas reinhardtii in response to copper availability. Plant Physiology 112: 697-704.
33. 6 in the green alga Chlamydomonas reinhardtii in response to changes in copper availability. EMBO Journal 14: 857-865.
34. Howe G, Merchant S. 1992. Heavy metal-activated synthesis of peptides in Chlamydomonas reinhardtii. Plant Physiology 98: 127-136.
35. Hu S, Lau KWK, Wu M. 2001. Cadmium sequestration in Chlamydomonas reinhardtii. Plant Science 161: 987-996.
36. Hua CX, Brown C, Adhiya J, Traina S, Sayre RT, Cai X. 1999. Growth and heavy metal binding properties of transgenic Chlamydomonas expressing a foreign metallothionein gene. International Journal of Phytoremediation 1: 53-65.
37. Irmer U, Wachholz I, Schafer H, Lorch DW. 1986. Influence of lead on Chlamydomonas reinhardtii dangeard (Volvocales, Chlorophyta): accumulation and uitrastructure changes. Environmental and Experimental Botany 26: 97-105.
38. Jacquot JP, Stein M, Lemaire S, Decottignies P, Le Maréchal P, Lancelin J-M. 1998. Molecular aspects of components of the ferredoxin/thioredoxin systems. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S, eds. The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Dordrecht, The Netherlands: Kluwer Academic Publishers, 501-514.
39. Kindle KL. 1998. Nudear transformation: technology and applications. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S, eds. The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Dordrecht, The Netherlands: Kluwer Academic Publishers, 41-61.
40. 2-inducible, periplasmic polypeptide in a unicellular green alga Chlamydomonas reinhardtii. Plant Physiology 114: 112.
41. Kovar JL, Zhang J, Funke RP, Weeks DP. 2002. Molecular analysis of the acetolactate synthase gene of Chlamydomonas reinhardtii and development of a genetically engineered gene as a dominant selectable marker for genetic transformation. Plant Journal 29: 109-117.
42. La Fontaine S, Quinn JM, Nakamoto SS, Page MD, Gohre V, Moseley JL, Kropat J, Merchant S. 2002. Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryotic Cell 1: 736-757.
43. Lefebvre PA, Silflow CD. 1999. Chlamydomonas: the cell and its genomes. Genetics 151: 9-14.
44. Lemaire S, Keryer E, Stein M, Schepens II, Issakidis-Bourguet E, Gerard-Hirne C, Miginiac-Maslow M, Jacquot JP. 1999. Heavy-metal regulation of thioredoxin gene expression in Chlamydomonas reinhardtii. Plant Physiology 120: 773-778.
45. Lemaire SD, Miginiac-Maslow M, Jacquot JP. 2002. Plant thioredoxin gene expression: control by light, circadian clock, and heavy metals. Methods in Enzymology 347: 412-421.
46. Li ZS, Lu YP, Zhen RG, Szczypka M, Thiele DJ, Rea PA. 1997. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae. YCF1-catalyzed transport of bis (glutathionato) cadmium. Proceedings of National Academy of Sciences, USA 94: 42-47.
47. Lumbreras V, Stevens DR, Purton S. 1998. Efficient foreign gene expression in Chlamydomonas reinhardtii mediated by an endogenous intron. Plant Journal 14: 441-447.
48. Lynnes JA, Derzaph TLM, Weger HG. 1998. Iron limitation results in induction of ferricyanide reductase and ferric chelate reductase activities in Chlamydomonas reinhardtii. Planta 204: 360-365.
49. MacFie SM, Tarmohamed Y, Welbourn PM. 1994. Effect of cadmium, cobalt, copper and nickel on growth of the green alga Chlamydomonas reinhardtii: the influence of the cell wall and pH. Archives of Environmental Contamination and Toxicology 27: 454-458.
50. Maul JE, Lilly JW, Cui L, dePamphilis CW, Miller W, Harris EH, Stern DB. 2002. The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14: 2659-2679.
51. Meagher RB. 2000. Phytoremediation of toxic elemental and organic pollutants. Current Opinion in Plant Biology 3: 153-162.
52. Merchant S. 1998. Synthesis ofmetalloproteins involved in photosynthesis: plastoscyanin and cytochromes. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S, eds. The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Dordrecht, The Netherlands: Kluwer Academic Publishers, 597-611.
53. Minko I, Holloway SP, Nikaido S, Carter M, Odom OW, Johnson CH, Herrin DL. 1999. Renilla luciferase as a vital reporter for chloroplast gene expression in Chlamydomonas. Molecular and General Genetics 262: 421-425.
54. Momose Y, Iwahashi H. 2001. Bioassay of cadmium using a DNA microarray: genome-wide expression patterns of Saccharomyces cerevisiae response to cadmium. Environmental Toxicology and Chemistry 20: 2353-2360.
55. Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M. 2002a. Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. Embo Journal 21: 6709-6720.
56. Moseley JL, Page MD, Alder NP, Eriksson M, Quinn J, Soto F, Theg SM, Hippler M, Merchant S. 2002b. Reciprocal expression of two candidate di-iron enzymes affecting photosystem I and light-harvesting complex accumulation. Plant Cell 14: 673-688.
57. Moseley J, Quinn J, Eriksson M, 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 Journal 19: 2139-2151.
58. Nagel K, Voigt J. 1995. Impaired photosynthesis in a cadmium-tolerant Chlamydomonas mutant strain. Microbiology Research 150: 105-110.
59. Ohresser M, Matagne RF, Loppes R. 1997. Expression of the arylsulphatase reporter gene under the control of the nitl promoter in Chlamydomonas reinhardtii. Current Genetics 31: 264-271.
60. Ortiz DF, Kreppel L, Speiser DM, Scheel G, McDonald G, Ow DW. 1992. Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter. Embo Journal 11: 3491-3499.
61. Ordz DF, Ruscitti T, McCue KF, Ow DW. 1995. Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. Journal of Biological Chemistry 270: 4721-4728.
62. Pfeifer McHugh J, Spanier JG. 1994. Isolation of cadmium sensitive mutants in Chlamydomonas reinhardtii by transformation/insertional mutagenesis. FEMS Microbiology Letters 124: 239-244.
63. Pinta V, Picaud M, Reiss-Husson F, Astier C. 2002. Rubrivivax gelatinosus acsF (previously orf358) codes for a conserved, putative binudear-iron-cluster-containing protein involved in aerobic oxidative cycllzation of Mg-protoporphyrin IX monomethylester. Journal of Bacteriology 184: 746-753.
64. Prasad MN, Drej K, Skawinska A, Strzalka K, Stralka K. 1998. Toxicity of cadmium and copper in Chlamydomonas reinhardtii wild-type (WT 2137) and cell wall deficient mutant strain (CW 15). Bulletin of Environmental Contamination and Toxicology 60: 306-311.
65. Purton S, Rochaix JD. 1994. Complementation of a Chlamydomonas reinhardtii mutant using a genomic cosmid library. Plant Molecular Biology 24: 533-537.
66. Quinn JM, Barraco P, Eriksson M, Merchant S. 2000. Coordinate copper- and oxygen-responsive Cyc6 and Cpx1 expression in Chlamydomonas is mediated by the same element. Journal of Biological Chemistry 275: 6080-6089.
67. Quinn JM, Eriksson M, Moseley JL, Merchant S. 2002. Oxygen deficiency responsive gene expression in Chlamydomonas reinhardtii through a copper-sensing signal transduction pathway. Plant Physiology 128: 463-471.
68. Quinn JM, Nakamoto SS, 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. Journal of Biological Chemistry 274: 14444-14454.
69. Randolph-Anderson BL, Boynton JE, Gillham NW, Harris EH, Johnson AM, Dorthu MP, Matagne RF. 1993. Further characterization of the respiratory deficient dum-1 mutation of Chlamydomonas reinhardtii and its use as a recipient for mitochondrial transformation. Molecular and General Genetics 236: 235-244.
70. Randolph-Anderson BL, Sato R, Johnson AM, Harris EH, Hanser CR, Oeda K, Ishige F, Nishio S, Gillham NW, Boynton JE. 1998. Isolation and characterization of a mutant protoporphyrinogen oxidase geue from Chlamydomonas reinhardtii conferring resistance to porphyric herbicides. Plant Molecular Biology 38: 839-859.
71. Rauser WE. 1999. Structure and function of metal chelators produced by plants: the case for organic acids, amino acids, phytin, and metallothioneins. Cell Biochemistry and Biophysisics 31: 19-48.
72. Remade C, Matagne RF. 1998. Mitochondrial genetics. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S, eds. The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Dordrecht, The Netherlands: Kluwer Academic Publishers, 661-674.
73. Rochaix JD, Goldschmidt-Clermont M, Merchant S. 1998. The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Dordrecht, The Netherlands: Kluwer Academic Publishers.
74. Rubinelli P, Siripomadulsil S, Gao-Rubinelli F, Sayre RT. 2002. Cadmium- and iron-stress-inducible gene expression in the green alga Chlamydomonas reinhardtii: evidence for H43 protein function in iron assimilation. Planta 215: 1-13.
75. 2 concentration and iron deficiency on the gene expression. Plant Cell and Physiology 39: 131-138.
76. Schroda M, Vallon O, Wollman FA, Beck CF. 1999. A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair ofphotosystem II during and after photoinhibition. Plant Cell 11: 1165-1178.
77. Shrager J, Hauser C, Chang CW, Harris EH, Davies J, McDermott J, Tamse R, Zhang Z, Grossman AR. 2003. Chlamydomonas reinhardtii genome project. A guide to the generation and use of cDNA information. Plant Physiology 131: 401-408.
78. Silflow CD. 1998. Organization of the nuclear genome. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S, eds. The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Dordrecht, The Netherlands: Kluwer Academic Publishers, 25-40.
79. Silflow CD, Lefebvre PA. 2001. Assembly and motility of eukaryotic cilia and flagella. Lessons from Chlamydomonas reinhardtii. Plant Physiology 127: 1500-1507.
80. Siripornadulsil S, Traina S, Verma DP, Sayre RT. 2002. Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14: 2837-2847.
81. Sizova I, Fuhrmann M, Hegemann P. 2001. A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. Gene 277: 221-229.
82. Stohs SJ, Bagchi D. 1995. Oxidative mechanisms in the toxicity of metal ions. Free Radical in Biology and Medecine 18: 321-336.
83. Strauss C, Mussgnug JH, Kruse O. 2001. Ligation-mediated suppression-PCR as a powerful tool to analyse nuclear gene sequences in the green alga Chlamydomonas reinhardtii. Photosynthesis Research 70: 311-320.
84. Tam LW, Lefebvre PA. 1993. Cloning of flagellar genes in Chlamydomonas reinhardtii by DNA insertional mutagenesis. Genetics 135: 375-384.
85. Vashishtha M, Segil G, Hall JL. 1996. Direct complementation of Chlamydomonas mutants with amplified YAC DNA. Genomics 36: 459-467.
86. 2+-tolerant mutant strain of the unicellular green alga Chlamydomonas reinhardtii. Journal of Plant Physiology 159: 941-950.
87. Voigt J, Nagel K, Wrann D. 1998. A cadmium-tolerant Chlamydomonas mutant strain impaired in photosystem II activity. Journal of Plant Physiology 153: 566-573.
88. Warren HV. 1989. Geology, trace elements and health. Social Science and Medecine 29: 923-926.
89. Weger HG. 1999. Ferric and cupric reductase activities in the green alga Chlamydomonas reinhardtii: experiments using iron-limited chemostats. Planta 207: 377-384.
90. Weiss-Magasic C, Lustigman B, Lee LH. 1997. Effect of mercury on the growth of Chlamydomonas reinhardtii. Bulletin of Environmental Contamination and Toxicology 59: 828-833.
91. Wemmie JA, Szczypka MS, Thiele DJ, Moye-Rowley WS. 1994. Cadmium tolerance mediated by the yeast AP-1 protein requires the presence of an ATP-binding cassette transporter-encodinggene Ycf1. Journal of Biological Chemistry 269: 32592-32597.
92. Zhang H, Herman PL, Weeks DP. 1994. Gene isolation through genomic complementation using an indexed library of Chlamydomonas rdnhardtii DNA. Plant Molecular Biology 24: 663-672.