RNA silencing of hydrogenase(-like) genes and investigation of their physiological roles in the green alga Chlamydomonas reinhardtii

Biochemical Journal

Volumn 431, Issue 3, 2010, Pages 345-351

  Godman, James E ^a   Molnár, Attila ^a   Baulcombe, David C ^a   Balk, Janneke ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Gene silencing; Hypoxia; Iron only hydrogenase like protein; Iron sulfur protein; Molybdenum cofactor enzyme; Nar1 protein

Indexed keywords

ALDEHYDES; CELL CULTURE; CHLOROPHYLL; ENZYMES; GALLIUM ALLOYS; GENETIC ENGINEERING; HYDROGEN PRODUCTION; MOLYBDENUM; RNA; SULFUR;

GENE SILENCING; HYPOXIA; IRON-SULFUR PROTEIN; MOLYBDENUM COFACTOR ENZYME; NAR1 PROTEIN;

GENE EXPRESSION;

ALDEHYDE OXIDASE; HYDROGENASE; HYPOXANTHINE; MICRORNA; XANTHINE DEHYDROGENASE; ALGAL PROTEIN; HYDROGEN; IRON SULFUR PROTEIN;

ARTICLE; CELL FUNCTION; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; DOWN REGULATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE SILENCING; GREEN ALGA; HYPOXIA; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; ANAEROBIC GROWTH; BIOSYNTHESIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; RNA INTERFERENCE;

CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; EUKARYOTA;

ALGAL PROTEINS; ANAEROBIOSIS; CHLAMYDOMONAS REINHARDTII; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HYDROGEN; HYDROGENASE; IRON-SULFUR PROTEINS; RNA INTERFERENCE; TRANSCRIPTION, GENETIC;

EID: 78049255865     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100932     Document Type: Article

References (41)

1. Beinert, H. (2000) Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5, 2-15
2. Nicolet, Y., Cavazza, C. and Fontecilla-Camps, J. (2002) Fe-only hydrogenases: structure, function and evolution. J. Inorg. Biochem. 91, 1-8
3. Forestier, M., King, P., Zhang, L., Posewitz, M. C., Schwarzer, S., Happe, T., Ghirardi, M. L. and Seibert, M. (2003) Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur. J. Biochem. 270, 2750-2758
4. Lill, R. (2009) Function and biogenesis of iron-sulphur proteins. Nature 460, 831-838
5. Balk, J. and Lobréaux, S. (2005) Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci. 10, 324-331
6. Bych, K., Netz, D., Vigani, G., Bill, E., Lill, R., Pierik, A. and Balk, J. (2008) The essential cytosolic iron-sulfur protein Nbp35 acts without Cfd1 partner in the green lineage. J. Biol. Chem. 283, 35797-35804
7. Kohbushi, H., Nakai, Y., Kikuchi, S., Yabe, T., Hori, H. and Nakai, M. (2009) Arabidopsis cytosolic Nbp35 homodimer can assemble both [2Fe-2S] and [4Fe-4S] clusters in two distinct domains. Biochem. Biophys. Res. Commun. 378, 810-815
8. Meyer, J. (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell. Mol. Life Sci. 64, 1063-1084
9. Horner, D., Heil, B., Happe, T. and Embley, T. (2002) Iron hydrogenases: ancient enzymes in modern eukaryotes. Trends Biochem. Sci. 27, 148-153
10. Balk, J., Pierik, A. J., Netz, D. J., Mühlenhoff, U. and Lill, R. (2004) The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J. 23, 2105-2115
11. Urzica, E., Pierik, A., Mühlenhoff, U. and Lill, R. (2009) Crucial role of conserved cysteine residues in the assembly of two iron-sulfur clusters on the CIA protein Nar1. Biochemistry 48, 4946-4958
12. Cavazza, C., Martin, L., Mondy, S., Gaillard, J., Ratet, P. and Fontecilla-Camps, J. (2008) The possible role of an [FeFe]-hydrogenase-like protein in the plant responses to changing atmospheric oxygen levels. J. Inorg. Biochem. 102, 1359-1365
13. Posewitz, M., King, P., Smolinski, S., Zhang, L., Seibert, M. and Ghirardi, M. (2004) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J. Biol. Chem. 279, 25711-25720
14. Huang, J., Song, D., Flores, A., Zhao, Q., Mooney, S., Shaw, L. and Lee, F. (2007) IOP1, a novel hydrogenase-like protein that modulates hypoxia-inducible factor-1α activity. Biochem. J. 401, 341-352
15. Song, D. and Lee, F. (2008) A role for IOP1 in mammalian cytosolic iron-sulfur protein biogenesis. J. Biol. Chem. 283, 9231-9238
16. Fujii, M., Adachi, N., Shikatani, K. and Ayusawa, D. (2009) [FeFe]-hydrogenase-like gene is involved in the regulation of sensitivity to oxygen in yeast and nematode. Genes Cells 14, 457-468
17. Merchant, S., Prochnik, S., Vallon, O., Harris, E., Karpowicz, S., Witman, G. B., Terry, A., Salamov, A., Fritz-Laylin, L. K., Maréchal- Drouard, L. et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250
18. Molnár, A., Schwach, F., Studholme, D., Thuenemann, E. and Baulcombe, D. (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447, 1126-1129
19. Molnár, A., Bassett, A., Thuenemann, E., Schwach, F., Karkare, S., Ossowski, S., Weigel, D. and Baulcombe, D. (2009) Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J. 58, 165-174
20. Zhao, T., Li, G., Mi, S., Li, S., Hannon, G., Wang, X. and Qi, Y. (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev. 21, 1190-1203
21. Zhao, T., Wang, W., Bai, X. and Qi, Y. (2009) Gene silencing by artificial microRNAs in Chlamydomonas. Plant J. 58, 157-164
22. Gorman, D. S. and Levine, R. P. (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc. Natl. Acad. Sci. U. S. A. 54, 1665-1669
23. Nichols, G. L. and Syrett, P. J. (1978) Nitrate reductase deficient mutants of Chlamydomonas reinhardii: isolation and genetics. J. Gen. Microbiol. 108, 71-77
24. ΔΔCT method. Methods 25, 402-408
25. Hemschemeier, A., Melis, A. and Happe, T. (2009) Analytical approaches to photobiological hydrogen production in unicellular green algae. Photosynthesis Res. 102, 523-540
26. Koshiba, T., Saito, E., Ono, N., Yamamoto, N. and Sato, M. (1996) Purification and properties of flavin- and molybdenum-containing aldehyde oxidase from coleoptiles of maize. Plant Physiol. 110, 781-789
27. Lichtenthaler, H. K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 148, 350-382
28. Abramoff, M. D., Magelhaes, P. J. and Ram, S. J. (2004) Image processing with ImageJ. Biophotonics Int. 11, 36-42
29. Mus, F., Dubini, A., Seibert, M., Posewitz, M. C. and Grossman, A. R. (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J. Biol. Chem. 282, 25475-25486
30. Jacobs, J., Pudollek, S., Hemschemeier, A. and Happe, T. (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett. 583, 325-329
31. Lezhneva, L., Amann, K. and Meurer, J. (2004) The universally conserved HCF101 protein is involved in assembly of [4Fe-4S]-cluster-containing complexes in Arabidopsis thaliana chloroplasts. Plant J. 37, 174-185
32. Van Hoewyk, D., Abdel-Ghany, S. E., Cohu, C. M., Herbert, S. K., Kugrens, P., Pilon, M. and Pilon-Smits, E. A. (2007) Chloroplast iron-sulfur cluster protein maturation requires the essential cysteine desulfurase CpNifS. Proc. Natl. Acad. Sci. U. S. A. 104, 5686-5691
33. Frazzon, A. P., Ramirez, M. V., Warek, U., Balk, J., Frazzon, J., Dean, D. R. and Winkel, B. S. (2007) Functional analysis of Arabidopsis genes involved in mitochondrial iron-sulfur cluster assembly. Plant Mol. Biol. 64, 225-240
34. Bernard, D. G., Cheng, Y., Zhao, Y. and Balk, J. (2009) An allelic mutant series of ATM3 reveals its key role in the biogenesis of cytosolic iron-sulfur proteins in Arabidopsis. Plant Physiol. 151, 590-602
35. Fosset, C., Chauveau, M. J., Guillon, B., Canal, F., Drapier, J. C. and Bouton, C. (2006) RNA silencing of mitochondrial m-Nfs1 reduces Fe-S enzyme activity both in mitochondria and cytosol of mammalian cells. J. Biol. Chem. 281, 25398-25406
36. Martelli, A., Wattenhofer-Donzé, M., Schmucker, S., Bouvet, S., Reutenauer, L. and Puccio, H. (2007) Frataxin is essential for extramitochondrial Fe-S cluster proteins in mammalian tissues. Hum. Mol. Genet. 16, 2651-2658
37. Cain, B. J. (1965) Nitrogen utilization in 38 freshwater Chlamydomonad algae. Can. J. Bot. 43, 1367-1378
38. Terashima, M., Specht, M., Naumann, B. and Hippler, M. (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtiiby quantitative proteomics. Mol. Cell. Proteomics 9, 1514-1532
39. Netz, D. J., Pierik, A. J., Stümpfig, M., Mühlenhoff, U. and Lill, R. (2007) The Cfd1-Nbp35 complex acts as a scaffold for iron-sulfur protein assembly in the yeast cytosol. Nat. Chem. Biol. 3, 278-286
40. Lenz, O., Bernhard, M., Buhrke, T., Schwartz, E. and Friedrich, B. (2002) The hydrogen-sensing apparatus in Ralstonia eutropha. J. Mol. Microbiol. Biotechnol. 4, 255-262
41. Bailey-Serres, J. and Chang, R. (2005) Sensing and signalling in response to oxygen deprivation in plants and other organisms. Annals Bot. 96, 507-518