The chloroplast sulfate transport system in the green alga Chlamydomonas reinhardtii

Planta

Volumn 228, Issue 6, 2008, Pages 951-961

  Lindberg, Pia ^a   Melis, Anastasios ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chlamydomonas reinhardtii; Chloroplast envelope; Green algae; Sabc gene; Sbp gene; Sulfate transport; SulP gene; SulP2 gene

Indexed keywords

ALGAL PROTEIN; SULFATE; SULFUR;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; SEQUENCE ANALYSIS; TRANSPORT AT THE CELLULAR LEVEL;

ALGAL PROTEINS; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; CONSERVED SEQUENCE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION REGULATION; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, PROTEIN; SULFATES; SULFUR;

CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

EID: 55849089918     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-008-0795-0     Document Type: Article

References (55)

1. J Abe T Kubo Y Takagi T Saito K Miura H Fukuzawa Y Matsuda 2004 The transcriptional program of synchronous gametogenesis in Chlamydomonas reinhardtii Curr Genet 46 304 315
2. TK Antal P Lindblad 2005 Production of H2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH J Appl Microbiol 98 114 120
3. DI Arnon 1949 Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris Plant Physiol 24 1 15
4. Borza T, Rajeswaran A, Lee RW (2006) Unpublished results. GenBank accession no. DQ782794
5. G Candiano M Bruschi L Musante L Santucci GM Ghiggeri B Carnemolla P Orecchia L Zardi PG Righetti 2004 Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis Electrophoresis 25 1327 1333
6. HC Chen A Melis 2004 Localization and function of SulP, a nuclear-encoded chloroplast sulfate permease in Chlamydomonas reinhardtii Planta 220 198 210
7. HC Chen AJ Newton A Melis 2005 Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H-2 evolution in Chlamydomonas reinhardtii Photosynth Res 84 289 296
8. HC Chen K Yokthongwattana AJ Newton A Melis 2003 SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii Planta 218 98 106
9. K Cline H Mori 2001 Thylakoid DeltapH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport J Cell Biol 154 719 729
10. JC de Cambiaire C Otis M Turmel C Lemieux 2007 The chloroplast genome sequence of the green alga Leptosira terrestris: multiple losses of the inverted repeat and extensive genome rearrangements within the Trebouxiophyceae BMC Genomics 8 213
11. AP de Koning PJ Keeling 2006 The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured BMC Biol 4 12
12. K Diederichs J Diez G Greller C Muller J Breed C Schnell C Vonrhein W Boos W Welte 2000 Crystal structure of MalK, the ATPase subunit of the trehalose/maltose ABC transporter of the archaeon Thermococcus litoralis EMBO J 19 5951 5961
13. O Emanuelsson H Nielsen G von Heijne 1999 ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites Protein Sci 8 978 984
14. R Gaudet DC Wiley 2001 Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing EMBO J 20 4964 4972
15. DS Gorman RP Levine 1965 Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardii Proc Natl Acad Sci USA 54 1665 1669
16. MJ Hawkesford 2003 Transporter gene families in plants: the sulphate transporter gene family-redundancy or specialization? Physiol Plant 117 155 163
17. R Hell 1997 Molecular physiology of plant sulfur metabolism Planta 202 138 148
18. A Hemschemeier S Fouchard L Cournac G Peltier T Happe 2008 Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks Planta 227 397 407
19. MY Hirai T Fujiwara M Awazuhara T Kimura M Noji K Saito 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
20. K Hofmann W Stoffel 1993 TMbase-a database of membrane spanning proteins segments Biol Chem Hoppe-Seyler 374 166
21. T Kataoka A Watanabe-Takahashi N Hayashi M Ohnishi T Mimura P Buchner MJ Hawkesford T Yamaya H Takahashi 2004 Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis Plant Cell 16 2693 2704
22. U Knauf W Hachtel 2002 The genes encoding subunits of ATP synthase are conserved in the reduced plastid genome of the heterotrophic alga Prototheca wickerhamii Mol Genet Genomics 267 492 497
23. M Kugita A Kaneko Y Yamamoto Y Takeya T Matsumoto K Yoshinaga 2003 The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into the earliest land plants Nucleic Acids Res 31 716 721
24. UK Laemmli 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680 685
25. DE Laudenbach AR Grossman 1991 Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for function in sulfate transport J Bacteriol 173 2739 2750
26. C Lemieux C Otis M Turmel 2000 Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution Nature 403 649 652
27. C Lemieux C Otis M Turmel 2007 A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies BMC Biol 5 2
28. T Leustek MN Martin JA Bick JP Davies 2000 Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies Annu Rev Plant Physiol Plant Mol Biol 51 141 165
29. T Leustek K Saito 1999 Sulfate transport and assimilation in plants Plant Physiol 120 637 644
30. M Matsuzaki O Misumi IT Shin S Maruyama M Takahara SY Miyagishima T Mori K Nishida F Yagisawa K Nishida Y Yoshida Y Nishimura S Nakao T Kobayashi Y Momoyama T Higashiyama A Minoda M Sano H Nomoto K Oishi H Hayashi F Ohta S Nishizaka S Haga S Miura T Morishita Y Kabeya K Terasawa Y Suzuki Y Ishii S Asakawa H Takano N Ohta H Kuroiwa K Tanaka N Shimizu S Sugano N Sato H Nozaki N Ogasawara Y Kohara T Kuroiwa 2004 Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D Nature 428 653 657
31. A Melis 2007 Photosynthetic H-2 metabolism in Chlamydomonas reinhardtii (unicellular green algae) Planta 226 1075 1086
32. A Melis HC Chen 2005 Chloroplast sulfate transport in green algae-genes, proteins and effects Photosynth Res 86 299 307
33. A Melis T Happe 2001 Hydrogen production. Green algae as a source of energy Plant Physiol 127 740 748
34. A Melis M Spangfort B Andersson 1987 Light-Absorption and electron-transport balance between photosystem-II and photosystem-I in spinach-chloroplasts Photochem Photobiol 45 129 136
35. SS Merchant SE Prochnik O Vallon EH Harris SJ Karpowicz GB Witman A Terry A Salamov LK Fritz-Laylin L Marechal-Drouard WF Marshall LH Qu DR Nelson AA Sanderfoot MH Spalding VV Kapitonov Q Ren P Ferris E Lindquist H Shapiro SM Lucas J Grimwood J Schmutz P Cardol H Cerutti G Chanfreau CL Chen V Cognat MT Croft R Dent S Dutcher E Fernandez H Fukuzawa D Gonzalez-Ballester D Gonzalez-Halphen A Hallmann M Hanikenne M Hippler W Inwood K Jabbari M Kalanon R Kuras PA Lefebvre SD Lemaire AV Lobanov M Lohr A Manuell I Meier L Mets M Mittag T Mittelmeier JV Moroney J Moseley C Napoli AM Nedelcu K Niyogi SV Novoselov IT Paulsen G Pazour S Purton JP Ral DM Riano-Pachon W Riekhof L Rymarquis M Schroda D Stern J Umen R Willows N Wilson SL Zimmer J Allmer J Balk K Bisova CJ Chen M Elias K Gendler C Hauser MR Lamb H Ledford JC Long J Minagawa MD Page J Pan W Pootakham S Roje A Rose E Stahlberg AM Terauchi P Yang S Ball C Bowler CL Dieckmann VN Gladyshev P Green R Jorgensen S Mayfield B Mueller-Roeber S Rajamani RT Sayre P Brokstein I Dubchak D Goodstein L Hornick YW Huang J Jhaveri Y Luo D Martinez WC Ngau B Otillar A Poliakov A Porter L Szajkowski G Werner K Zhou IV Grigoriev DS Rokhsar AR Grossman 2007 The Chlamydomonas genome reveals the evolution of key animal and plant functions Science 318 245 250
36. V Nikiforova J Freitag S Kempa M Adamik H Hesse R Hoefgen 2003 Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity Plant J 33 633 650
37. N Ohta M Matsuzaki O Misumi SY Miyagishima H Nozaki K Tanaka IT Shin Y Kohara T Kuroiwa 2003 Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae DNA Res 10 67 77
38. K Ohyama H Fukuzawa T Kohchi H Shirai T Sano S Sano K Umesono Y Shiki M Takeuchi Z Chang S Aota H Inokuchi H Ozeki 1986 Chloroplast gene organization deduced from complete sequence of liverwort Marchantia-Polymorpha chloroplast DNA Nature 322 572 574
39. K Saito 2004 Sulfur assimilatory metabolism. The long and smelling road Plant Physiol 136 2443 2450
40. H Schagger G von Jagow 1991 Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form Anal Biochem 199 223 231
41. N Shibagaki A Rose JP McDermott T Fujiwara H Hayashi T Yoneyama JP Davies 2002 Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots Plant J 29 475 486
42. EL Sonnhammer G von Heijne A Krogh 1998 A hidden Markov model for predicting transmembrane helices in protein sequences Proc Int Conf Intell Syst Mol Biol 6 175 182
43. R Surzycki L Cournac G Peltier JD Rochaix 2007 Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas Proc Natl Acad Sci USA 104 17548 17553
44. H Takahashi A Watanabe-Takahashi FW Smith M Blake-Kalff MJ Hawkesford K Saito 2000 The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana Plant J 23 171 182
45. H Tomatsu J Takano H Takahashi A Watanabe-Takahashi N Shibagaki T Fujiwara 2007 An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil Proc Natl Acad Sci USA 104 18807 18812
46. M Turmel C Otis C Lemieux 1999 The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes Proc Natl Acad Sci USA 96 10248 10253
47. M Turmel C Otis C Lemieux 2005 The complete chloroplast DNA sequences of the charophycean green algae Staurastrum and Zygnema reveal that the chloroplast genome underwent extensive changes during the evolution of the Zygnematales BMC Biol 3 22
48. M Turmel C Otis C Lemieux 2006 The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants Mol Biol Evol 23 1324 1338
49. T Wakasugi T Nagai M Kapoor M Sugita M Ito S Ito J Tsudzuki K Nakashima T Tsudzuki Y Suzuki A Hamada T Ohta A Inamura K Yoshinaga M Sugiura 1997 Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division Proc Natl Acad Sci USA 94 5967 5972
50. AL White A Melis 2006 Biochemistry of hydrogen metabolism in Chlamydomonas reinhardtii wild type and a Rubisco-less mutant Int J Hydrogen Energy 31 455 464
51. Yokthongwattana K, Melis A (2006) Photoinhibition and recovery in oxygenic photosynthesis: mechanism of a photosystem II damage and repair cycle. In: Govindjee (ed) Photoprotection, photoinhibition, gene regulation, and environment, advances in photosynthesis and respiration. Springer, The Netherlands, pp 175-191
52. N Yoshimoto E Inoue K Saito T Yamaya H Takahashi 2003 Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis Plant Physiol 131 1511 1517
53. N Yoshimoto E Inoue A Watanabe-Takahashi K Saito H Takahashi 2007 Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition Plant Physiol 145 378 388
54. N Yoshimoto H Takahashi FW Smith T Yamaya K Saito 2002 Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots Plant J 29 465 473
55. LP Zhang T Happe A Melis 2002 Biochemical and morphological characterization of sulfur-deprived and H-2-producing Chlamydomonas reinhardtii (green alga) Planta 214 552 561