Tiered regulation of sulfur deprivation responses in Chlamydomonas reinhardtii and identification of an associated regulatory factor

Plant Physiology

Volumn 162, Issue 1, 2013, Pages 195-211

  Aksoy, Munevver ^a   Pootakham, Wirulda ^a,b   Pollock, Steve V ^a,c   Moseley, Jeffrey L ^a,d   González Ballester, David ^a,e   Grossman, Arthur R ^a  

^a GEOPHYSICAL LABORATORY   (United States)

^b NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^c LOUISIANA STATE UNIVERSITY   (United States)

^d Solazyme Inc   (United States)

^e UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL DNA; ALGAL PROTEIN; ARYLSULFATASE; CHLORAMPHENICOL; CYCLOHEXIMIDE; DACTINOMYCIN; MESSENGER RNA; SULFATE; SULFUR;

ARTICLE; BIOLOGICAL MODEL; CHLAMYDOMONAS REINHARDTII; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC LINKAGE; GENETICS; METABOLISM; PHENOTYPE; PHYSIOLOGY;

ALGAL PROTEINS; ARYLSULFATASES; CHLAMYDOMONAS REINHARDTII; CHLORAMPHENICOL; CYCLOHEXIMIDE; DACTINOMYCIN; DNA, ALGAL; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENETIC LINKAGE; MODELS, BIOLOGICAL; MUTAGENESIS, INSERTIONAL; PHENOTYPE; RNA, MESSENGER; SULFATES; SULFUR;

ALGAE; CHLAMYDOMONAS REINHARDTII;

EID: 84877071826     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.214593     Document Type: Article

References (42)

1. Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24: 1-15.
2. Atanesyan L, Günther V, Dichtl B, Georgiev O, Schaffner W (2012) Polyglutamine tracts as modulators of transcriptional activation from yeast to mammals. Biol Chem 393: 63-70.
3. Chang CW, Moseley JL, Wykoff D, Grossman AR (2005) The LPB1 gene is important for acclimation of Chlamydomonas reinhardtii to phosphorus and sulfur deprivation. Plant Physiol 138: 319-329.
4. Davies JP, Yildiz F, Grossman AR (1994) Mutants of Chlamydomonas reinhardtii with aberrant responses to sulfur deprivation. Plant Cell 6: 53-63.
5. Davies JP, Yildiz FH, Grossman AR (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15: 2150-2159.
6. Davies JP, Yildiz FH, Grossman AR (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
7. de Hostos EL, Schilling J, Grossman AR (1989) Structure and expression of the gene encoding the periplasmic arylsulfatase of Chlamydomonas reinhardtii. Mol Gen Genet 218: 229-239
8. de Hostos EL, Togasaki RK, Grossman A (1988) Purification and biosynthesis of a derepressible periplasmic arylsulfatase from Chlamydomonas reinhardtii. J Cell Biol 106: 29-37.
9. DeWitt ND, dos Santos CF, Allen KE, Slayman CW (1998) Phosphorylation region of the yeast plasma-membrane H+-ATPase: role in protein folding and biogenesis. J Biol Chem 273: 21744-21751.
10. Ding YH, Liu NY, Tang ZS, Liu J, Yang WC (2006) Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 18: 815-830.
11. Fauchon M, Lagniel G, Aude JC, Lombardia L, Soularue P, Petat C, Marguerie G, Sentenac A, Werner M, Labarre J (2002) Sulfur sparing in the yeast proteome in response to sulfur demand. Mol Cell 9: 713-723.
12. Ferreira RMB, Teixeira ARN (1992) Sulfur starvation in Lemna leads to degradation of ribulose-bisphosphate carboxylase without plant death. J Biol Chem 267: 7253-7257.
13. González E, Solano R, Rubio V, Leyva A, Paz-Ares J (2005) PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12- related protein that enables the endoplasmic reticulum exit of a highaffinity phosphate transporter in Arabidopsis. Plant Cell 17: 3500-3512.
14. González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR (2010) RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 22: 2058-2084.
15. González-Ballester D, Pollock SV, Pootakham W, Grossman AR (2008) The central role of a SNRK2 kinase in sulfur deprivation responses. Plant Physiol 147: 216-227.
16. Grossman A, Takahashi H (2001) Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annu Rev Plant Physiol Plant Mol Biol 52: 163-210.
17. Gruenbaum Y, Naveh-Many T, Cedar H, Razin A (1981) Sequence specificity of methylation in higher plant DNA. Nature 292: 860-862.
18. Harris EH (1989). The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego
19. Huettel B, Kanno T, Daxinger L, Bucher E, van der Winden J, Matzke AJ, Matzke M (2007) RNA-directed DNA methylation mediated by DRD1 and Pol IVb: a versatile pathway for transcriptional gene silencing in plants. Biochim Biophys Acta 1769: 358-374.
20. Irihimovitch V, Stern DB (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.
21. Kawazoe R, Hwang S, Herrin DL (2000) Requirement for cytoplasmic protein synthesis during circadian peaks of transcription of chloroplastencoded genes in Chlamydomonas. Plant Mol Biol 44: 699-709.
22. Kim DH, Kim GS, Yun CH, Lee YC (2008) Functional conservation of the glutamine-rich domains of yeast Gal11 and human SRC-1 in the transactivation of glucocorticoid receptor Tau 1 in Saccharomyces cerevisiae. Mol Cell Biol 28: 913-925.
23. Landeras-Bueno S, Jorba N, Pérez-Cidoncha M, Ortín J (2011) The splicing factor proline-glutamine rich (SFPQ/PSF) is involved in influenza virus transcription. PLoS Pathog 7: e1002397.
24. Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51: 141-165.
25. Lopez PJ, Marchand I, Yarchuk O, Dreyfus M(1998) Translation inhibitors stabilize Escherichia coli mRNAs independently of ribosome protection. Proc Natl Acad Sci USA 95: 6067-6072.
26. Lumbreras V, Stevens DR, Purton S (1998) Efficient foreign gene expression in Chlamydomonas reinhardtii mediated by an endogenous intron. Plant J 14: 441-447.
27. Moseley JL, González-Ballester D, Pootakham W, Bailey S, Grossman AR (2009) Genetic interactions between regulators of Chlamydomonas phosphorus and sulfur deprivation responses. Genetics 181: 889-905.
28. Navarro FJ, Martín Y, Siverio JM (2008) Phosphorylation of the yeast nitrate transporter Ynt1 is essential for delivery to the plasma membrane during nitrogen limitation. J Biol Chem 283: 31208-31217.
29. Nguyen AV, Thomas-Hall SR, Malnoë A, Timmins M, Mussgnug JH, Rupprecht J, Kruse O, Hankamer B, Schenk PM (2008) Transcriptome for photobiological hydrogen production induced by sulfur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot Cell 7: 1965-1979.
30. Pollock SV, Colombo SL, Prout DL Jr, Godfrey AC, Moroney JV (2003) Rubisco activase is required for optimal photosynthesis in the green alga Chlamydomonas reinhardtii in a low-CO2 atmosphere. Plant Physiol 133: 1854-1861.
31. Pollock SV, Pootakham W, Shibagaki N, Moseley JL, Grossman AR (2005) Insights into the acclimation of Chlamydomonas reinhardtii to sulfur deprivation. Photosynth Res 86: 475-489.
32. Pootakham W, González-Ballester D, Grossman AR (2010) Identification and regulation of plasma membrane sulfate transporters in Chlamydomonas. Plant Physiol 153: 1653-1668.
33. Ravina CG, Chang C-I, Tsakraklides GP, McDermott JP, Vega JM, Leustek T, Gotor C, Davies J (2002) The sac mutants of Chlamydomonas reinhardtii reveal transcriptional and posttranscriptional control of cysteine biosynthesis. Plant Physiol 130: 2076-2084.
34. Sambrook J, Fritsch EF, Maniatis T (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
35. Shimogawara K, Fujiwara S, Grossman AR, Usuda H (1998) Highefficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148: 1821-1828.
36. Sugimoto K, Sato N, 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.
37. Takahashi H, Braby CE, Grossman AR (2001) Sulfur economy and cell wall biosynthesis during sulfur limitation of Chlamydomonas reinhardtii. Plant Physiol 127: 665-673.
38. Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62: 157-184.
39. Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117: 129-139.
40. Yildiz FH, Davies JP, Grossman AR (1994) Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfursufficient growth. Plant Physiol 104: 981-987.
41. Yildiz FH, Davies JP, Grossman AR (1996) Sulfur availability and the SAC1 gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii. Plant Physiol 112: 669-675.
42. Zhang Z, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3: 1331-1348