RNA-Seq analysis of sulfur-deprived chlamydomonas cells reveals aspects of acclimation critical for cell survival

Plant Cell

Volumn 22, Issue 6, 2010, Pages 2058-2084

  González Ballester, David ^a   Casero, David ^b   Cokus, Shawn ^b   Pellegrini, Matteo ^b   Merchant, Sabeeha S ^b   Grossman, Arthur R ^a  

^a GEOPHYSICAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL RNA; MESSENGER RNA; SULFUR;

AMINO ACID SEQUENCE; CHLAMYDOMONAS REINHARDTII; COMPARATIVE STUDY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOLECULAR GENETICS; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; CHLAMYDOMONAS REINHARDTII; GENE EXPRESSION PROFILING; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, ALGAL; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, RNA; SULFUR;

EID: 77955686486     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.071167     Document Type: Article

References (114)

1. Apel, K., and Hirt, H. (2004). Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55: 373-399.
2. Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141: 391-396.
3. Audic, S., and Claverie, J.M. (1997). The significance of digital gene expression profiles. Genome Res. 7: 986-995.
4. Bentley, R., and Chasteen, T.G. (2004). Environmental VOSCs-formation and degradation of dimethyl sulfide, methanethiol and related materials. Chemosphere 55: 291-317.
5. Billheimer, J.T., Cornvale, H.N., Leisinger, T., Eckhardt, T., and Jones, E.E. (1976). Ornithine d-transaminase in Escherichia coli: Its identity with acetylornithine d-transaminase. J. Bacteriol. 127: 1315-1323.
6. Bolling, C., and Fiehn, O. (2005). Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiol. 139: 1995-2005.
7. Bordo, D., and Bork, P. (2002). The rhodanese/Cdc25 phosphatase superfamily. Sequence-structure-function relations. EMBO Rep. 3: 741-746.
8. Chang, C.W., Moseley, J.L., Wykoff, D., and Grossman, A.R. (2005). The LPB1 gene is important for acclimation of Chlamydomonas reinhardtii to phosphorus and sulfur deprivation. Plant Physiol. 138: 319-329.
9. Chen, H.C., Newton, A.J., and Melis, A. (2005). Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H2 evolution in Chlamydomonas reinhardtii. Photosynth. Res. 84: 289-296.
10. Collier, J.L., and Grossman, A.R. (1992). Chlorosis induced by nutrient deprivation in Synechococcus sp. Strain PCC 7942: Not all bleaching is the same. J. Bacteriol. 174: 4718-4726.
11. Colnaghi, R., Cassinelli, G., Drummond, M., Forlani, F., and Pagani, S. (2001). Properties of the Escherichia coli rhodanese-like protein SseA: Contribution of the active-site residue Ser240 to sulfur donor recognition. FEBS Lett. 500: 153-156.
12. Couee, I., Sulmon, C., Gouesbet, G., and El Amrani, A. (2006). Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J. Exp. Bot. 57: 449-459.
13. Davies, J., Yildiz, F., and Grossman, A.R. (1996). Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J. 15: 2150-2159.
14. Davies, J.P., Yildiz, F., and Grossman, A.R. (1994). Mutants of Chlamydomonas reinhardtii with aberrant responses to sulfur deprivation. Plant Cell 6: 53-63.
15. Davies, J.P., Yildiz, F.H., and Grossman, A.R. (1999). Sac3, an Snf1- like serine/threonine kinase that positively and negatively regulates the responses of Chlamydomonas to sulfur limitation. Plant Cell 11: 1179-1190.
16. Dayer, R., Fischer, B.B., Eggen, R.I., and Lemaire, S.D. (2008). The peroxiredoxin and glutathione peroxidase families in Chlamydomonas reinhardtii. Genetics 179: 41-57.
17. de Hostos, E.L., Schilling, J., and Grossman, A.R. (1989). Structure and expression of the gene encoding the periplasmic arylsulfatase of Chlamydomonas reinhardtii. Mol. Gen. Genet. 218: 229-239.
18. de Hostos, E.L., Togasaki, R.K., and Grossman, A.R. (1988). Purification and biosynthesis of a derepressible periplasmic arylsulfatase from Chlamydomonas reinhardtii. J. Cell Biol. 106: 29-37.
19. Del Duca, S., Beninati, S., and Serafini-Fracassini, D. (1995). Polyamines in chloroplasts: Identification of their glutamyl and acetyl derivatives. Biochem. J. 305: 233-237.
20. Della Mea, M., Di Sandro, A., Dondini, L., Del Duca, S., Vantini, F., Bergamini, C., Bassi, R., and Serafini-Fracassini, D. (2004). A Zea mays 39-kDa thylakoid transglutaminase catalyses the modification by polyamines of light-harvesting complex II in a light-dependent way. Planta 219: 754-764.
21. Dembitsky, V.M. (2003). Oxidation, epoxidation and sulfoxidation reactions catalyzed by haloperoxidases. Tetrahedron 59: 4701-4720.
22. Dominy, J.E., Jr., Simmons, C.R., Karplus, P.A., Gehring, A.M., and Stipanuk, M.H. (2006). Identification and characterization of bacterial cysteine dioxygenases: A new route of cysteine degradation for eubacteria. J. Bacteriol. 188: 5561-5569.
23. Eberhard, S., Jain, M., Im, C.S., Pollock, S., Shrager, J., Lin, Y., Peek, A.S., and Grossman, A.R. (2006). Generation of an oligonucleotide array for analysis of gene expression in Chlamydomonas reinhardtii. Curr. Genet. 49: 106-124.
24. Eichhorn, E., van der Ploeg, J.R., Kertesz, M.A., and Leisinger, T. (1997). Characterization of alpha-ketoglutarate-dependent taurine dioxygenase from Escherichia coli. J. Biol. Chem. 272: 23031-23036.
25. Elrad, D., and Grossman, A.R. (2004). A genome's-eye view of the light-harvesting polypeptides of Chlamydomonas reinhardtii. Curr. Genet. 45: 61-75.
26. Fauchon, M., Lagniel, G., Aude, J.C., Lombardia, L., Soularue, P., Petat, C., Marguerie, G., Sentenac, A., Werner, M., and Labarre, J. (2002). Sulfur sparing in the yeast proteome in response to sulfur demand. Mol. Cell 9: 713-723.
27. Ghirardi, M.L., Posewitz, M.C., Maness, P.C., Dubini, A., Yu, J., and Seibert, M. (2007). Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Annu. Rev. Plant Biol. 58: 71-91.
28. Giovanelli, J., Mudd, S.H., and Datko, A.H. (1985). Quantitative analysis of pathways of methionine metabolism and their regulation in Lemna. Plant Physiol. 78: 555-560.
29. González-Ballester, D., and Grossman, A.R. (2009). Sulfur: From aquisition to assimilation. In The Chlamydomonas Sourcebook, D. Stern, E.H. Harris, and G.B. Witman, eds (Amsterdam, The Netherlands: Elsevier), pp. 159-188.
30. González-Ballester, D., Pollock, S.V., Pootakham, W., and Grossman, A.R. (2008). The central role of a SNRK2 kinase in sulfur deprivation responses. Plant Physiol. 147: 216-227.
31. Goyer, A., Haslekas, C., Miginiac-Maslow, M., Klein, U., le Marechal, P., Jacquot, J.P., and Decottignies, P. (2002). Isolation and characterization of a thioredoxin-dependent peroxidase from Chlamydomonas reinhardtii. Eur. J. Biochem. 269: 272-282.
32. Groppa, M.D., and Benavides, M.P. (2008). Polyamines and abiotic stress: Recent advances. Amino Acids 34: 35-45.
33. Hansch, R., Lang, C., Rennenberg, H., and Mendel, R.R. (2007). Significance of plant sulfite oxidase. Plant Biol. 9: 589-595.
34. Hanson, A.D., and Roje, S. (2001). One-carbon metabolism in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 119-137.
35. Harris, E.H. (1989). The Chlamydomonas Sourcebook. A Comprehensive Guide to Biology and Laboratory Use. (San Diego: Academic Press).
36. Heifetz, P.B., Forster, B., Osmond, C.B., Giles, L.J., and Boynton, J.E. (2000). Effects of acetate on facultative autotrophy in Chlamydomonas reinhardtii assessed by photosynthetic measurements and stable isotope analyses. Plant Physiol. 122: 1439-1445.
37. Heimberg, H., Boyen, A., Crabeel, M., and Glansdorff, N. (1990). Escherichia coli and Saccharomyces cerevisiae acetylornithine aminotransferase: Evolutionary relationship with ornithine aminotransferase. Gene 90: 69-78.
38. Hemrika, W., Renirie, R., Dekker, H.L., Barnett, P., and Wever, R. (1997). From phosphatases to vanadium peroxidases: A similar architecture of the active site. Proc. Natl. Acad. Sci. USA 94: 2145-2149.
39. Hirai, M.Y., Fujiwara, T., Awazuhara, M., Kimura, T., Noji, M., and Saito, K. (2003). Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 33: 651-663.
40. Hogan, D.A., Auchtung, T.A., and Hausinger, R.P. (1999). Cloning and characterization of a sulfonate/alpha-ketoglutarate dioxygenase from Saccharomyces cerevisiae. J. Bacteriol. 181: 5876-5879.
41. Ioannidis, N.E., and Kotzabasis, K. (2007). Effects of polyamines on the functionality of photosynthetic membrane in vivo and in vitro. Biochim. Biophys. Acta 1767: 1372-1382.
42. Ioannidis, N.E., Sfichi, L., and Kotzabasis, K. (2006). Putrescine stimulates chemiosmotic ATP synthesis. Biochim. Biophys. Acta 1757: 821-828.
43. Irihimovitch, V., and Stern, D.B. (2006). The sulfur acclimation SAC3 kinase is required for chloroplast transcriptional repression under sulfur limitation in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 103: 7911-7916.
44. Kahnert, A., Vermeij, P., Wietek, C., James, P., Leisinger, T., and Kertesz, M.A. (2000). The ssu locus plays a key role in organosulfur metabolism in Pseudomonas putida S-313. J. Bacteriol. 182: 2869-2878.
45. Kent, W.J. (2002). BLAT - The BLAST-like alignment tool. Genome Res. 12: 656-664.
46. Kessler, D. (2006). Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol. Rev. 30: 825-840.
47. Kirk, D.L., and Kirk, M.M. (1978). Carrier-mediated uptake of arginine and urea by Chlamydomonas reinhardtii. Plant Physiol. 61: 556-560.
48. Kopriva, S., Mugford, S.G., Matthewman, C., and Koprivova, A. (2009). Plant sulfate assimilation genes: Redundancy versus specialization. Plant Cell Rep. 28: 1769-1780.
49. Ledford, H.K., Chin, B.L., and Niyogi, K.K. (2007). Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii. Eukaryot. Cell 6: 919-930.
50. Ledwidge, R., and Blanchard, J.S. (1999). The dual biosynthetic capability of N-acetylornithine aminotransferase in arginine and lysine biosynthesis. Biochemistry 38: 3019-3024.
51. Lemaire, S., Keryer, E., Stein, M., Schepens, I., Issakidis-Bourguet, E., Gérard-Hirne, C., Miginiac-Maslow, M., and Jacquot, J.P. (1999). Heavy-metal regulation of thioredoxin gene expression in Chlamydomonas reinhardtii. Plant Physiol. 120: 773-778.
52. Lewandowska, M., and Sirko, A. (2008). Recent advances in understanding plant response to sulfur-deficiency stress. Acta Biochim. Pol. 55: 457-471.
53. Li, R., Li, Y., Kristiansen, K., and Wang, J. (2008). SOAP: Short oligonucleotide alignment program. Bioinformatics 24: 713-714.
54. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
55. Lunde, C., Zygadlo, A., Simonsen, H.T., Nielsen, P.L., Blennow, A., and Haldrup, A. (2008). Sulfur starvation in rice: The effect on photosynthesis, carbohydrate metabolism, and oxidative stress protective pathways. Physiol. Plant. 134: 508-521.
56. Marioni, J.C., Mason, C.E., Mane, S.M., Stephens, M., and Gilad, Y. (2008). RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 18: 1509-1517.
57. Mariscal, V., Moulin, P., Orsel, M., Miller, A.J., Fernandez, E., and Galvan, A. (2006). Differential regulation of the Chlamydomonas Nar1 gene family by carbon and nitrogen. Protist 157: 421-433.
58. Maruyama-Nakashita, A., Inoue, E., Watanabe-Takahashi, A., Yamaya, T., and Takahashi, H. (2003). Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol. 132: 597-605.
59. Maruyama-Nakashita, A., Nakamura, Y., Tohge, T., Saito, K., and Takahashi, H. (2006). Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18: 3235-3251.
60. Mazel, D., and Marliere, P. (1989). Adaptive eradication of methionine and cysteine from cyanobacterial light-harvesting proteins. Nature 341: 245-248.
61. Merchant, S.S., et al. (2007). The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250.
62. Michelet, L., Zaffagnini, M., Marchand, C., Collin, V., Decottignies, P., Tsan, P., Lancelin, J.M., Trost, P., Miginiac-Maslow, M., Noctor, G., and Lemaire, S.D. (2005). Glutathionylation of chloroplast thioredoxin f is a redox signaling mechanism in plants. Proc. Natl. Acad. Sci. USA 102: 16478-16483.
63. Michelet, L., Zaffagnini, M., Vanacker, H., Le Marechal, P., Marchand, C., Schroda, M., Lemaire, S.D., and Decottignies, P. (2008). In vivo targets of S-thiolation in Chlamydomonas reinhardtii. J. Biol. Chem. 283: 21571-21578.
64. Moharikar, S., D'Souza, J., Kulkarni, A.B., and Rao, B.J. (2006). UV-C induced apoptotic-like cell death process in the unicellular chlorophyte Chlamydomonas reinhardtii. J. Phycol. 42: 423-433.
65. Moharikar, S., D'Souza, J.S., and Rao, B.J. (2007). A homologue of the defender against the apoptotic death gene (dad1) in UVexposed Chlamydomonas cells is downregulated with the onset of programmed cell death. J. Biosci. 32: 261-270.
66. Moroney, J.V., and Ynalvez, R.A. (2007). Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot. Cell 6: 1251-1259.
67. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNASeq. Nat. Methods 5: 621-628.
68. Moseley, J., and Grossman, A.R. (2009). Phosphorus limitation from the physiological to the genomic. In The Chlamydomonas Sourcebook, E.H. Harris, D. Stern, and G.B. Witman, eds (Amsterdam: Elsevier), pp. 189-216.
69. Moseley, J.L., González-Ballester, D., Pootakham, W., Bailey, S., and Grossman, A.R. (2009). Genetic interactions between regulators of Chlamydomonas phosphorus and sulfur deprivation responses. Genetics 181: 889-905.
70. Mueller, E.G. (2006). Trafficking in persulfides: Delivering sulfur in biosynthetic pathways. Nat. Chem. Biol. 2: 185-194.
71. 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.
72. Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M., and Snyder, M. (2008). The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349.
73. Navakoudis, E., Vrentzou, K., and Kotzabasis, K. (2007). A polyamine- and LHCII protease activity-based mechanism regulates the plasticity and adaptation status of the photosynthetic apparatus. Biochim. Biophys. Acta 1767: 261-271.
74. Nguyen, A.V., Thomas-Hall, S.R., Malnoe, A., Timmins, M., Mussgnug, J.H., Rupprecht, J., Kruse, O., Hankamer, B., and Schenk, P.M. (2008). The transcriptome of photo-biological hydrogen production induced by sulphur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot. Cell 7: 1965-1979.
75. Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H., and Hoefgen, R. (2003). Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: Interlacing of biosynthetic pathways provides response specificity. Plant J. 33: 633-650.
76. Nikiforova, V.J., Daub, C.O., Hesse, H., Willmitzer, L., and Hoefgen, R. (2005a). Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. J. Exp. Bot. 56: 1887-1896.
77. Nikiforova, V.J., Kopka, J., Tolstikov, V., Fiehn, O., Hopkins, L., Hawkesford, M.J., Hesse, H., and Hoefgen, R. (2005b). Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol. 138: 304-318.
78. Ogasawara, Y., Lacourciere, G.M., Ishii, K., and Stadtman, T.C. (2005). Characterization of potential selenium-binding proteins in the selenophosphate synthetase system. Proc. Natl. Acad. Sci. USA 102:1012-1016.
79. Okazaki, Y., Shimojima, M., Sawada, Y., Toyooka, K., Narisawa, T., Mochida, K., Tanaka, H., Matsuda, F., Hirai, A., Hirai, M.Y., Ohta, H., and Saito, K. (2009). A chloroplastic UDP-glucose yrophosphorylase from Arabidopsis is the committed enzyme for the first step of sulfolipid biosynthesis. Plant Cell 21: 892-909.
80. Ortiz-Bermudez, P., Hirth, K.C., Srebotnik, E., and Hammel, K.E. (2007). Chlorination of lignin by ubiquitous fungi has a likely role in global organochlorine production. Proc. Natl. Acad. Sci. USA 104: 3895-3900.
81. Peers, G., Truong, T.B., Ostendorf, E., Elrad, D., Grossman, A.R., Hippler, M., and Niyogi, K.K. (2009). An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Science 462: 518-521.
82. Pereira, Y., Lagniel, G., Godat, E., Baudouin-Cornu, P., Junot, C., and Labarre, J. (2008). Chromate causes sulfur starvation in yeast. Toxicol. Sci. 106: 400-412.
83. Perez-Alegre, M., and Franco, A.R. (1998). Resistance to L-methionine- S-sulfoximine in Chlamydomonas reinhardtii is due to an alteration in a general amino acid transport system. Planta 207: 20-26.
84. 2 atmosphere. Plant Physiol. 133: 1854-1861.
85. Pollock, S.V., Pootakham, W., Shibagaki, N., Moseley, J.L., and Grossman, A.R. (2005). Insights into the acclimation of Chlamydomonas reinhardtii to sulfur deprivation. Photosynth. Res. 86: 475-489.
86. Pootakham, W., González-Ballester, D., and Grossman, A.R. (2010). Identification and regulation of plasma membrane sulfate transporters in Chlamydomonas reinhardtii. Plant Physiol. http://dx.doi.org/10.1104/pp.110.157875.
87. Ravina, C.G., Barroso, C., Vega, J.M., and Gotor, C. (1999). Cysteine biosynthesis in Chlamydomonas reinhardtii. Molecular cloning and regulation of O-acetylserine(thiol)lyase. Eur. J. Biochem. 264: 848-853.
88. Ravina, C.G., Chang, C.I., Tsakraklides, G.P., McDermott, J.P., Vega, J.M., Leustek, T., Gotor, C., and Davies, J.P. (2002). The sac mutants of Chlamydomonas reinhardtii reveal transcriptional and posttranscriptional control of cysteine biosynthesis. Plant Physiol. 130: 2076-2084.
89. Richard, C., Ouellet, H., and Guertin, M. (2000). Characterization of the LI818 polypeptide from the green unicellular alga Chlamydomonas reinhardtii. Plant Mol. Biol. 42: 303-316.
90. Riemenschneider, A., Wegele, R., Schmidt, A., and Papenbrock, J. (2005). Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J. 272: 1291-1304.
91. Rouhier, N., Lemaire, S.D., and Jacquot, J.P. (2008). The role of glutathione in photosynthetic organisms: Emerging functions for glutaredoxins and glutathionylation. Annu. Rev. Plant Biol. 59:143-166.
92. Sarkar, N., Lemaire, S., Wu-Scharf, D., Issakidis-Bourguet, E., and Cerutti, H. (2005). Functional specialization of Chlamydomonas reinhardtii cytosolic thioredoxin h1 in the response to alkylationinduced DNA damage. Eukaryot. Cell 4: 262-273.
93. Sato, N., Tsuzuki, M., Matsuda, Y., Ehara, T., Osafune, T., and Kawaguchi, A. (1995). Isolation and characterization of mutants affected in lipid metabolism of Chlamydomonas reinhardtii. Eur. J. Biochem. 230: 987-993.
94. Schloss, J.A., Silflow, C.D., and Rosenbaum, J.L. (1984). mRNA abundance changes during flagellar regeneration in Chlamydomonas reinhardtii. Mol. Cell. Biol. 4: 424-434.
95. Scott, J., Rébeillé, F., and Fletcher, J.J. (2000). Folic acid and folates: The feasibility for nutritional enhancement in plant foods. J. Sci. Food Agric. 80: 795-824.
96. Sfichi-Duke, L., Ioannidis, N.E., and Kotzabasis, K. (2008). Fast and reversible response of thylakoid-associated polyamines during and after UV-B stress: A comparative study of the wild type and a mutant lacking chlorophyll b of unicellular green alga Scenedesmus obliquus. Planta 228: 341-353.
97. Slesak, I., Libik, M., Karpinska, B., Karpinski, S., and Miszalski, Z. (2007). The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses. Acta Biochim. Pol. 54: 39-50.
98. Slocum, R.D. (2005). Genes, enzymes and regulation of arginine biosynthesis in plants. Plant Physiol. Biochem. 43: 729-745.
99. Sugimoto, K., Sato, N., and Tsuzuki, M. (2007). Utilization of a chloroplast membrane sulfolipid as a major internal sulfur source for protein synthesis in the early phase of sulfur starvation in Chlamydomonas reinhardtii. FEBS Lett. 581: 4519-4522.
100. Sugimoto, K., Tsuzuki, M., and Sato, N. (2009). Regulation of synthesis and degradation of a sulfolipid under sulfur-starved conditions and its physiological significance in Chlamydomonas reinhardtii. New Phytol. 185: 676-686.
101. Takahashi, H., Braby, C.E., and Grossman, A.R. (2001). Sulfur economy and cell wall biosynthesis during sulfur limitation of Chlamydomonas reinhardtii. Plant Physiol. 127: 665-673.
102. Torkelson, J.D., Lynnes, J.A., and Weger, H.G. (1995). Extracellular peroxidase-mediated oxygen consumption in Chlamydomonas reinhardtii (Chlorophyta). J. Phycol. 31: 562-567.
103. Triantaphylides, C., and Havaux, M. (2009). Singlet oxygen in plants: Production, detoxification and signaling. Trends Plant Sci. 14: 219-228.
104. Triantaphylides, C., Krischke, M., Hoeberichts, F.A., Ksas, B., Gresser, G., Havaux, M., Van Breusegem, F., and Mueller, M.J. (2008). Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol. 148: 960-968.
105. Voigt, J., Deinert, B., and Bohley, P. (2000). Subcellular localization and light-dark control of ornithine decarboxylase in the unicellular green alga Chlamydomonas reinhardtii. Physiol. Plant. 108: 353-360.
106. Vreeland, V., Waite, J.H., and Epstein, L. (1998). Polyphenols and oxidases in sbustratum adhesion by marine algae and mussels. J. Phycol. 34: 1-8.
107. Wang, Z., Gerstein, M., and Snyder, M. (2009). RNA-Seq: A revolutionary tool for transcriptomics. Nat. Rev. Genet. 10: 57-63.
108. Williams, B., and Dickman, M. (2008). Plant programmed cell death: Can't live with it; can't live without it. Mol. Plant Pathol. 9: 531-544.
109. Wykoff, D., Davies, J., and Grossman, A. (1998). The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol. 117: 129-139.
110. Yildiz, F., Davies, J.P., and Grossman, A.R. (1994). Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol. 104: 981-987.
111. Yoda, H., Yamaguchi, Y., and Sano, H. (2003). Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol. 132: 1973-1981.
112. Zhang, L., Happe, T., and Melis, A. (2002). Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214: 552-561.
113. Zhang, L., and Melis, A. (2002). Probing green algal hydrogen production. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357: 1499-1507.
114. Zhang, Z., Shrager, J., Jain, M., Chang, C.W., Vallon, O., and Grossman, A.R. (2004). Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot. Cell 3: 1331-1348.