Responses to Macronutrient Deprivation

  • Arthur R. Grossman
  • David Gonzalez-Ballester
  • Nakako Shibagaki
  • Wirulda Pootakham
  • Jeffrey Moseley
Chapter

Summary

Photosynthetic organisms have developed elaborate mechanisms to acquire macronutrients and to adjust to conditions in which those nutrients become limiting to growth. Some of the responses of photosynthetic organisms to macronutrient limitation may be specific for a particular nutrient and involve the development of various mechanisms to scavenge the limiting nutrient from the external milieu, which may require elevated synthesis of high affinity transport systems, the redistribution of internal nutrient stores and the synthesis of hydrolytic enzymes that release the nutrient from organic substrates in the soil. Other responses may be of a more general nature, occurring during a number of different nutrient limitation conditions, and involve modifying the biosynthetic machinery of the cell, including the photosynthetic apparatus. In this review we focus on the acquisition of the macronutrients nitrogen, sulfur and phosphorus from the environment, and the ways in which the unicellular green alga Chlamydomonas reinhardtii acclimates to changes in its nutrient environment.

Keywords

ammonium assimilation macronutrients nitrate nutrient deprivation phosphate phosphorus sulfur transport 

Abbreviations

AAP

Arabiopsis amino acid permease

ABC transporter

ATP binding cassette transporter

AMP

adenosine monophosphate

AMT

ammonium transporter

AphVIII

gene encoding a protein that confers resistance to paromomycin

APK

adenosine 5′-phosphosulfate kinase

APR

adenosine 5′-phosphosulfate reductase

APS

adenosine 5′-phosphosulfate

ARG7

gene encoding an enzyme in the pathway for arginine biosynthesis(argininosuccinate lyase)

ARS

arylsulfatase

ars11

mutant in a serine threonine kinase associated with control of the responses of Chlamydomonas reinhardtii to sulfur deprivation

ASL

gene encoding O-acetylserine (thiol) lyase

ASQD

2′-O-acyl-sulfoquinovosodiacylglycerol

ATS

gene encoding ATP sulfurylase

CpDNA

chloroplast DNA

CpRNA

chloroplast RNA

CysT

membrane component of ABC transporter for sulfate

DMS

dimethylsulfide

DMSP

dimethyl sulfonio-proprionate

DRA

chloride/bicarbonate antiporter

ECP

extracellular polypeptide

EST

expressed sequence tag

FAR

regulatory locus involved in the utilization of nitrogen in Chlamydomonas reinhardtii

Fd

ferredoxin

FNR

Fd-NADP-oxidoreductase

GOGAT

glutamine-2-oxoglutarate amino-transferase

GS

glutamine synthetase

GSH

glutathione

HANiT

high affinity nitrite transporter

HANT

high affinity nitrate transporter

hf-2

high fluorescence mutant deficient for sulfolipids

HYDA

hydrogenase proteins

IMP

inosine monophosphate

IRL protein

isoflavone reductase-like protein in maize that has few sulfur amino acids

LANT

low affinity nitrate transporter

LHC

light harvesting complex

LHCSR2

light harvesting complex protein, stress related

LHT

lysine histidine transporter

LOV domain

domain that can be involved in sensing light, oxygen and voltage

LPB1

low phosphate bleaching phenotype

MYB domain

derived from myeloblastosis and often in regulatory proteins

NAR

nitrite-nitrate transporter genes

NIA1

nitrate reductase gene

NII1

nitrite reductase gene

NIT

nitrate assimilation/regulation loci in Chlamydomonas reinhardtii

NiR

nitrite reductase

NR

nitrate reductase

NRG

regulatory locus involved in the utilization of nitrogen in Chlamydomonas reinhardtii

NRT

nitrate transporter genes

OAS

O-acetylserine

OASTL

O-acetylserine (thiol) lyase

OPH

O-phosphohomoserine

PAPS

3′-phosphoadenosine 5′-phosphosulfate

PAS domain

protein domain involved in sensing and protein-protein interaction named from Per (period circadian protein), Arnt (Ah receptor nuclear translocator protein) and Sim (single-minded protein)

PC

phosphatidylcholine

PE

phosphatidylethanolamine

PG

phosphatidylglycerol

PHO2

phosphate regulatory E2 ubiquitin conjugase

PHOX

protein associated with extracellular phosphatase activity in Chlamydomonas reinhardtii and Volvox carteri

PHR1

involved in phosphorus deprivation responses in Arabidopsis thaliana

Pi

inorganic phosphate

Pi

phosphatidylinositol

PNP

polynucleotide Phosphate

PNPase

polynucleotide phosphorylase

PQ

plastoquinone pool

PTA

phosphate transporter, type A class

PTB

phosphate transporter, type B class

QA and QB

primary and secondary acceptors of photosystem II, respectively

RH

rhesus protein

ROS

reactive oxygen species

PSR1

regulator in Chlamydomonase reinhardtii associated with phosphate stress response

RuBP

ribulose-1,5-bisphosphate

SABC

nucleotide binding protein of ABC type transporter

SAC1

transporter-like proteins associated with control of the responses of Chlamydomonas reinhardtii to sulfur deprivation

sac1

mutant in the gene encoding SAC1

SAC3/SNRK2.2

serine threonine kinase associated with control of the responses of Chlamydomonas reinhardtii to sulfur deprivation

sac3

mutant in the gene encoding SAC3

SAM

S-adenosylmethionine

SAT

serine acetyltransferase

SBDP

selenenium binding protein

SBP

substrate binding protein of ABC type transporter

SERAT

gene encoding serine acetyltransferase

SGTE3

ubiquitiin ligase similar to Skp1-Cullin-F-box protein (SCF) ubiquitin ligases

SIR

sulfite reductase

SIZ1

sap interacting zinc finger protein which is plant SUMO E3 ligase

SLC26

family of anion transporters that include the sulfate transporters

SLT

sulfate transporter (animal type)

SNRK

SNF-related kinase

SpoIIAA

antisigma factor antagonist in Bacillus subitilis with similarity to STAS domain

SQD1

UDP-sulfoquinovose synthase

sqd1

mutant in the gene encoding SQD1

SQDG

sulfoquinovosodiacylglycerol

STAS

domain found attached to certain anion transporters such as the sulfate transporter that has homology to an antisigma factor antagonist in Bacillus subtilis; sulfate transporter and sigma factor domain

Sul

sulfate transporter in yeast

SULP

component of chloroplast sulfate transporter in Chlamydomonas reinhardtii

SULTR

sulfate transporters (plant type)

SUMO

small ubiquitin-like modifier

TMD

trans-membrane domain

Trk

domain of unknown function found associated with some transporters

UDP

uridine diphosphate

VTC

vacuolar transport chaperone

X-SO42−

5-bromo-4-chloro-3-indolyl sulfate

References

  1. Allen MD, Kropat J, Tottey S, Del Campo JA, Merchant SS (2007) Manganese deficiency in Chlamydomonas results in loss of Photosystem II and MnSOD function, sensitivity to peroxides, and secondary phosphorus and iron deficiency. Plant Physiol 143:263-277PubMedCrossRefGoogle Scholar
  2. Alloush GAZ, Zeto SK, Clark RB (2000) Phosphorus source, organic matter and arbuscular mycorrhiza effects on growth and mineral acquisition of chickpea grown in acidic soil. J Plant Nutr 23:1351-1369CrossRefGoogle Scholar
  3. Amarasinghe BHRR, deBruxelles GL, Braddon M, Onyeocha I, Forde BG, Udvardi MK (1998) Regulation of GmNRT2 expression and nitrate transport activity in roots of soybean (Glycine max). Planta 206:44-52PubMedCrossRefGoogle Scholar
  4. Anantharaman V, Koonin EV, Aravind L (2001) Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains. J Mol Biol 307:1271-1292PubMedCrossRefGoogle Scholar
  5. Andreae MO, Crutzen PJ (1997) Atmospheric aerosols: biogeochemical sources and role in atmospheric chemistry. Science 276:1052-1058CrossRefGoogle Scholar
  6. Andreae MO, Raemdonch H (1983) Dimethyl sulfide in the surface ocean and the marine atmosphere - a global view. Science 221:744-747PubMedCrossRefGoogle Scholar
  7. Aoki H, Ida S (1994) Nucleotide sequence of a rice root ferredoxin-NADP+ reductase cDNA and its induction by nitrate. Biochem Biophys Res Commun 1183:553-556Google Scholar
  8. Aparicio PJ, Quinones MA (1991) Blue light, a positive switch signal for nitrate and nitrite uptake by the green alga Monoraphidium braunii. Plant Physiol 95:374-378PubMedCrossRefGoogle Scholar
  9. Aravind L, Koonin EV (2000) The STAS domain - a link between anion transporters and antisigma-factor antagonists. Curr Biol 10:R53-55CrossRefGoogle Scholar
  10. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution and metabolism. Science 306:79-86PubMedCrossRefGoogle Scholar
  11. Arz HE, Gisselmann G, Schiffmann S, Schwenn JD (1994) A cDNA for adenylyl sulfate (APS)-kinase from Arabidopsis thaliana. Biochim Biophys Acta 1218:447-452PubMedCrossRefGoogle Scholar
  12. Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, Martin W (2006) Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J Biol Chem 281:9909-9918PubMedCrossRefGoogle Scholar
  13. Auesukaree C, Homma T, Tochio H, Shirakawa M, Kaneko Y, Harashima S (2004) Intracellular phosphate serves as a signal for the regulation of the PHO pathway in Saccharomyces cerevisiae. J Biol Chem 279:17289-17294PubMedCrossRefGoogle Scholar
  14. Baek SH, Chung IM, Yun SJ (2001) Molecular cloning and characterization of a tobacco leaf cDNA encoding a phosphate transporter. Mol Cells 11:1-6PubMedGoogle Scholar
  15. Barabote RD, Tamang DG, Abeywardena SN, Fallah NS, Fu JY, Lio JK, Mirhosseini P, Pezeshk R, Podell S, Salampessy ML, Thever MD, Saier MH Jr (2006) Extra domains in secondary transport carriers and channel proteins. Biochim Biophys Acta 1758:1557-1579PubMedCrossRefGoogle Scholar
  16. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399 and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988-999PubMedCrossRefGoogle Scholar
  17. Bariola PA, Howard CJ, Taylor CB, Verburg MT, Jaglan VD, Green PJ (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J 6:673-685PubMedCrossRefGoogle Scholar
  18. Benemann JR, Berenson JA, Kaplan NO, Kamen MD (1973) Hydrogen evolution by a chloroplast-ferredoxin-hydrogenase system. Proc Natl Acad Sci USA 70:2317-2320PubMedCrossRefGoogle Scholar
  19. Bick JA, Aslund F, Chen Y, Leustek T (1998) Glutaredoxin function for the carboxyl terminal domain of the plant-type 5′-adenylylsulfate (APS) reductase. Proc Natl Acad Sci USA 95:8404-8409PubMedCrossRefGoogle Scholar
  20. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphorus availability. Annu Rev Plant Physiol Plant Mol Biol 24:225-252CrossRefGoogle Scholar
  21. Bieleski RL, Laluchli A (1992) Phosphate uptake, efflux and deficiency in the water fern, Azolla. Plant Cell Environ 15:665-673CrossRefGoogle Scholar
  22. Bogdanova N, Hell R (1997) Cysteine synthesis in plants: protein-protein interactions of serine acetyltransferase from Arabidopsis thaliana. Plant J 11:251-262PubMedCrossRefGoogle Scholar
  23. Bolchi A, Petrucco S, Tenca P, Foroni C, Ottonello S (1999) Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response to variations in sulfur nutritional status: stereospecific down-regulation by L-cysteine. Plant Mol Biol 39:527-537PubMedCrossRefGoogle Scholar
  24. Bork C, Schwenn JD, Hell R (1998) Isolation and characterization of a gene for assimilatory sulfite reductase from Arabidopsis thaliana. Gene 212:147-153PubMedCrossRefGoogle Scholar
  25. Boudsocq M, Droillard MJ, Barbier-Brygoo H, Lauriere C (2007) Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid. Plant Mol Biol 63:491-503PubMedCrossRefGoogle Scholar
  26. Briggs WR, Huala E (1999) Blue-light photoreceptors in higher plants. Annu Rev Cell Dev Biol 15:33-62PubMedCrossRefGoogle Scholar
  27. Bruhl A, Haverkamp T, Gisselmann G, Schwenn JD (1996) A cDNA clone from Arabidopsis thaliana encoding plastidic ferredoxin: sulfite reductase. Biochim Biophys Acta 1295:119-124PubMedCrossRefGoogle Scholar
  28. Buchner P, Stuiver CE, Westerman S, Wirtz M, Hell R, Hawkesford MJ, De Kok LJ (2004) Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiol 136:3396-3408PubMedCrossRefGoogle Scholar
  29. Campbell WH, Kinghorn JR (1990) Functional domains of assimilatory nitrate reductases and nitrite reductases. Trends Biochem Sci 15:315-319PubMedCrossRefGoogle Scholar
  30. 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 138:319-329PubMedCrossRefGoogle Scholar
  31. Charlson RJ, Lovelock JE, Andreae MO, Warren SG (1987) Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326:655-661CrossRefGoogle Scholar
  32. Chen HC, Melis A (2004) Localization and function of SulP, a nuclear-encoded chloroplast sulfate permease in Chlamydomonas reinhardtii. Planta 220:198-210PubMedCrossRefGoogle Scholar
  33. Chen Q, Silflow CD (1996) Isolation and characterization of glutamine synthetase genes in Chlamydomonas reinhardtii. Plant Physiol 112:987-996PubMedCrossRefGoogle Scholar
  34. Chen HC, Yokthongwattana K, Newton AJ, Melis A (2003) SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii. Planta 218:98-106PubMedCrossRefGoogle Scholar
  35. Chen HC, Newton AJ, Melis A (2005) Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H2 evolution in Chlamydomonas reinhardtii. Photosynth Res 84:289-296PubMedCrossRefGoogle Scholar
  36. Chernova MN, Jiang L, Shmukler BE, Schweinfest CW, Blanco P, Freedman SD, Stewart AK, Alper SL (2003) Acute regulation of the SLC26A3 congenital chloride diarrhoea anion exchanger (DRA) expressed in Xenopus oocytes. J Physiol 549:3-19PubMedCrossRefGoogle Scholar
  37. Chiba Y, Ishikawa M, Kijima F, Tyson RH, Kim JH, Yamamoto A, Nambara E, Leustek T, Wallsgrove RM, Naito S (1999) Evidence for autoregulation of cystathionine γ-synthase mRNA stability in Arabidopsis. Science 286:1371-1374PubMedCrossRefGoogle Scholar
  38. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Cl Su (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412-421PubMedCrossRefGoogle Scholar
  39. Christie JM, Swartz TE, Bogomolni RA, Briggs WR (2002) Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J 32:205-219PubMedCrossRefGoogle Scholar
  40. Cole DW, Johnson DW (1977) Atmospheric sulfate additions and cation leaching in a Douglas fir ecosystem. Water Resources Res 13:313-317CrossRefGoogle Scholar
  41. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90-93PubMedCrossRefGoogle Scholar
  42. Croft MT, Warren MJ, Smith AG (2006) Riboswitch regulated gene expression in Chlamydomonas reinhardtii is involved in symbiotic interactions with bacteria. In: 12th International Conference on the Cell and Molecular Biology of Chlamydomonas, Portland, ORGoogle Scholar
  43. Crosson S, Rajagopal S, Moffat K (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42:2-10PubMedCrossRefGoogle Scholar
  44. Curien G, Job D, Douce R, Dumas R (1998) Allosteric activation of Arabidopsis threonine synthase by S-adenosylmethionine. Biochemistry 37:13212-13221PubMedCrossRefGoogle Scholar
  45. David MB, Grigal DF, Ohmann LF, Gertner GZ (1988) Sulfur, carbon, and nitrogen relationships in forest soils across the northern Great Lakes States as affected by atmospheric deposition and vegetation. Can J Forest Res 18:1386-1391CrossRefGoogle Scholar
  46. Davies J, Yildiz F, Grossman AR (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15:2150-2159PubMedGoogle Scholar
  47. Davies JD, Grossman AR (1998) Responses to deficiencies in macronutrients. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S (eds) The Molecular Biology of Chlamydomonas. Kluwer, Dortrecht, pp 613-635Google Scholar
  48. Davies JP, Yildiz F, Grossman AR (1994) Mutants of Chlamydomonas reinhardtii with aberrant responses to sulfur deprivation. Plant Cell 6:53-63PubMedGoogle Scholar
  49. 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 11:1179-1190PubMedGoogle Scholar
  50. de Hostos EL, Togasaki RK, Grossman AR (1988) Purification and biosynthesis of a derepressible periplasmic arylsulfatase from Chlamydomonas reinhardtii. J Cell Biol 106:29-37PubMedCrossRefGoogle Scholar
  51. de Hostos EL, Schilling J, Grossman AR (1989) Structure and expression of the gene encoding the periplasmic arylsulfatase of Chlamydomonas reinhardtii. Mol Gen Genet 218:229-239PubMedCrossRefGoogle Scholar
  52. Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207-213PubMedGoogle Scholar
  53. Dong B, Rengel Z, Delhaize E (1998) Uptake and translocation of phosphate by pho2 mutant and wild-type seedlings of Arabidopsis thaliana. Planta 205:251-256PubMedCrossRefGoogle Scholar
  54. Drew MC, Saker LR, Barber SA, Jenkins W (1984) Changes in the kinetics of phosphate and potassium absorption in nutrient-deficient barley roots measured by a solution-depletion technique. Planta 160:490-499CrossRefGoogle Scholar
  55. Droux M, Ravanel S, Douce R (1995) Methionine biosynthesis in higher plants - purification and characterization of cystathionine β-lyase from spinach chloroplasts. Arch Biochem Biophys 316:585-595PubMedCrossRefGoogle Scholar
  56. Droux M, Ruffet ML, Douce R, Job D (1998) Interactions between serine acetyltranferase and O-acetylserine(thiol) lyase in higher plants. Eur J Biochem 255:235-245PubMedCrossRefGoogle Scholar
  57. Duff SMG, Lefebvre DD, Plaxton WC (1991) Purification, characterization and sub-cellular localization of an acid phosphatase from Brassica nigra suspension cells - Comparison with phosphoenolpyruvate phosphatase. Arch Biochem Biophys 286:226-232PubMedCrossRefGoogle Scholar
  58. Dumont F, Loppes R, Kremers P (1990) New polypeptides and in-vitro translatable mRNAs are produced by phosphate-starved cells of the unicellular alga Chlamydomonas reinhardtii. Planta 182:610-616CrossRefGoogle Scholar
  59. Duncan L, Alper S, Losick R (1996) SpoIIAA governs the release of the cell-type specific transcription factor sigma F from its anti-sigma factor SpoIIAB. J Mol Biol 260:147-164PubMedCrossRefGoogle Scholar
  60. Eberhard S, Jain M, Im CS, Pollock S, Shrager J, Lin Y, Peek AS, Grossman AR (2006) Generation of an oligonucleotide array for analysis of gene expression in Chlamydomonas reinhardtii. Curr Genet 49:106-124PubMedCrossRefGoogle Scholar
  61. Ermilova EV, Zalutskaya ZM, Huang K, Beck CF (2004) Phototropin plays a crucial role in controlling changes in chemotaxis during the initial phase of the sexual life cycle in Chlamydomonas. Planta 219:420-427PubMedCrossRefGoogle Scholar
  62. Everett LA, Green ED (1999) A family of mammalian anion transporters and their involvement in human genetic diseases. Hum Mol Genet 8:1883-1891PubMedCrossRefGoogle Scholar
  63. Everett LA, Glaser B, Beck JC, Idol JR, Buchs A, Heyman M, Adawi F, Hazani E, Nassir E, Baxevanis AD, Sheffield VC, Green ED (1997) Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nat Genet 17:411-422PubMedCrossRefGoogle Scholar
  64. Fernández E, Cardenas J (1989) Genetic and regulatory aspects of nitrate assimilation in algae. Oxford University Press, Oxford, pp 101-124Google Scholar
  65. Fernández E, Galvan A (2007) Inorganic nitrogen assimilation in Chlamydomonas. J Exp Bot 58:2279-2287PubMedCrossRefGoogle Scholar
  66. Fernández E, Franco AR, Córdoba F, Cárdenas J (1986) Regulation of nitrate reductase levels in Chlamydomonas reinhardtii. Cienc Biol (Coimbra) 11:171-174Google Scholar
  67. Fernández E, Schnell R, Ranum LPW, Hussey SC, Silflow CD, Lefebvre PA (1989) Isolation and characterization of the nitrate reductase structural gene of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 86:6449-6453PubMedCrossRefGoogle Scholar
  68. Fernández E, Galvan A, Quesada A (1998) Nitrogen assimilation and its regulation. In: Rochaix JD, Goldschmidt-Clermont M, Merchant SS (eds) Molecular biology of Chlamydomonas: chloroplast and mitochondria, pp 637-659Google Scholar
  69. Ferreira RMB, Teixeira ARN (1992) Sulfur starvation in Lemna leads to degradation of ribulose-bisphosphate carboxylase without plant death. J Biol Chem 267:7253-7257Google Scholar
  70. Filleur S, Daniel-Vedele F (1999) Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta 207:461-469PubMedCrossRefGoogle Scholar
  71. Fischer WN, Kwart M, Hummel S, Frommer WB (1995) Substrate specificity and expression profile of amino-acid transporters (AAPS) in Arabidopsis. J Biol Chem 270:16315-16320PubMedCrossRefGoogle Scholar
  72. Fischer WN, Andre B, Rentsch D, Krollkiewicz S, Tegeder M, Breitkreuz K, Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3:188-195CrossRefGoogle Scholar
  73. Forde BG (2000) Nitrate transporters in plants: structure, function and regulation. Biochem Biophys Res Commun 1465:219-235Google Scholar
  74. Forestier M, King P, Zhang L, Posewitz M, Schwarzer S, Happe T, Ghirardi ML, Seibert M (2003) Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur J Biochem 270:2750-2758PubMedCrossRefGoogle Scholar
  75. Fouchard S, Hemschemeier A, Caruana A, Pruvost J, Legrand J, Happe T, Peltier G, Cournac L (2005) Autotrophic and mixotrophic hydrogen photoproduction in sulfur-deprived chlamydomonas cells. Appl Environ Microbiol 71:6199-6205PubMedCrossRefGoogle Scholar
  76. Foyer CH, Fletcher JM (2001) Plant antioxidants: colour me healthy. Biologist (London) 48:115-120Google Scholar
  77. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21-25CrossRefGoogle Scholar
  78. Franco AR, Cardenas J, Fernandez E (1987) Involvement of reversible inactivation in the regulation of nitrate reductase enzyme levels in Chlamydomonas reinhardtii. Plant Physiol 84:665-669PubMedCrossRefGoogle Scholar
  79. Franco AR, Cardenas J, Fernandez E (1988) Regulation by ammonium of nitrate and nitrite assimilation in Chlamydomonas reinhardtii. Biochem Biophys Res Commun 951:98-103Google Scholar
  80. Fristedt U, van Der Rest M, Poolman B, Konings WN, Persson BL (1999) Studies of cytochrome c oxidase-driven H+-coupled phosphate transport catalyzed by the Saccharomyces cerevisiae Pho84 permease in coreconstituted vesicles. Biochemistry 38:16010-16015PubMedCrossRefGoogle Scholar
  81. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038-2043PubMedCrossRefGoogle Scholar
  82. Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth and gene expression in Arabidopsis. Plant Cell 19:485-494PubMedCrossRefGoogle Scholar
  83. Galván A, Marquez AJ, Vega JM (1984) Purification and molecular properties of ferredoxin-glutamate synthase from Chlamyomonas reinhardtii. Planta 162:180-187CrossRefGoogle Scholar
  84. Galván A, Quesada A, Fernandez E (1996) Nitrate and nitrite are transported by different specific transport systems and by a bispecific transporter in Chlamydomonas reinhardtii. J Biol Chem 271:2088-2092PubMedCrossRefGoogle Scholar
  85. Ghirardi ML, Posewitz MC, Maness PC, Dubini A, Yu J, Seibert M (2007) Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Annu Rev Plant Biol 58:71-91PubMedCrossRefGoogle Scholar
  86. Gilbert GA, Knight JD, Vance CP, Allen DL (1999) Acid phosphatase activity in phosphorous-deficient white lupin roots. Plant Cell Environ 22:801-810CrossRefGoogle Scholar
  87. Gojon A, Dapoigny L, Lejay L, Tillard P, Rufty TW (1998) Effects of genetic modification of nitrate reductase expression on (no3)-N-15 uptake and reduction in Nicotiana plants. Plant Cell Environ 21:43-53CrossRefGoogle Scholar
  88. Goldstein AH, Baertlein DA, Danon A (1989) Phosphate starvation stress as an experimental system for molecular analysis. Plant Mol Biol Rep 7:7-16CrossRefGoogle Scholar
  89. Gomez-Garcia MR, Kornberg A (2004) Formation of an actin-like filament concurrent with the enzymatic synthesis of inorganic polyphosphate. Proc Natl Acad Sci USA 101:15876-15880PubMedCrossRefGoogle Scholar
  90. Gonzalez-Ballester D, Grossman AR (2009) Sulfur: from aquisition to assimilation. In: Stern D, Harris EH, Witman GB (eds) The Chlamydomonas Sourcebook. Academic Press, Amsterdam, pp 159-187Google Scholar
  91. Gonzalez-Ballester D, Camargo A, Fernandez E (2004) Ammonium transporter genes in Chlamydomonas : the nitrate-specific regulatory gene Nit2 is involved in Amt1; 1 expression. Plant Mol Biol 56:863-878PubMedCrossRefGoogle Scholar
  92. Gonzalez-Ballester D, de Montaigu A, Higuera JJ, Galvan A, Fernandez E (2005) Functional genomics of the regulation of the nitrate assimilation pathway in Chlamydomonas. Plant Physiol 137:522-533PubMedCrossRefGoogle Scholar
  93. Gonzalez-Ballester D, Pollock P, Pootakham W, Grossman AR (2008) The central role of a SNRK2 kinase in sulfur deprivation responses. Plant Physiol 147:216-227PubMedCrossRefGoogle Scholar
  94. Goodenough U, Lin H, Lee JH (2007) Sex determination in Chlamydomonas. Semin Cell Dev Biol 18:350-361PubMedCrossRefGoogle Scholar
  95. Gotor C, Cejudo FJ, Barroso C (1997) Tissue-specific expression of AtCys-3A gene encoding the cytosolic isoform of O-acetylserine(thiol)lyase in Arabidopsis. Plant J 11:347-352PubMedCrossRefGoogle Scholar
  96. Green PJ (1994) The ribonucleases of higher plants. Ann Rev Plant Physiol Plant Mol Biol 45:421-445CrossRefGoogle Scholar
  97. Grill E, Loffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthetase). Proc Natl Acad Sci USA 86:6838-6842PubMedCrossRefGoogle Scholar
  98. Grossman A, Takahashi H (2001) Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annu Rev Plant Physiol Plant Mol Biol 52:163-210PubMedCrossRefGoogle Scholar
  99. Grossman AR, Croft M, Gladyshev VN, Merchant SS, Posewitz MC, Prochnik S, Spalding MH (2007) Novel metabolism in Chlamydomonas through the lens of genomics. Curr Opin Plant Biol 10:190-198PubMedCrossRefGoogle Scholar
  100. Guerrero MG, Vega JM, Losada M (1981) The assimilatory nitrate reducing system and its regulation. Annu Rev Plant Physiol 32:169-204CrossRefGoogle Scholar
  101. Guiz C, Hirel B, Shedlofsky G, Gadal P (1979) Occurence and influence of light on the relative proportions of 2 glutamine synthetases in rice leaves. Plant Sci 15:271-277Google Scholar
  102. Gupta AS, Alscher RG, McCune DF (1990) Ozone exposure, glutathione levels and photosynthesis in hybrid poplar. In: H Rennenberg, C Brunold, LJ Dekoli, I Stulen (eds) Sulfur nutrition and sulfur assimilation in higher plants. SPB Academic Publications. the Hague, the Netherlands, pp 195-197Google Scholar
  103. Gutierrez-Marcos J, Roberts M, Campbell E, Wray J (1996) Three members of a novel small gene-family from Arabidopsis thaliana able to complemet functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and “APS reductase” activity. Proc Natl Acad Sci USA 93:13377-13382PubMedCrossRefGoogle Scholar
  104. Habicht KS, Gade M, Thamdrup B, Berg P, Canfield DE (2002) Calibration of sulfate levels in the archaean oceans. Science 298:2372-2374PubMedCrossRefGoogle Scholar
  105. Hallmann A (1999) Enzymes in the extracellular matrix of Volvox : an inducible, calcium-dependent phosphatase with a modular composition. J Biol Chem 274:1691-1697PubMedCrossRefGoogle Scholar
  106. Hanikenne M, Kramer U, Demoulin V, Baurain D (2005) A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschizon merolae. Plant Physiol 137:428-446PubMedCrossRefGoogle Scholar
  107. Hartmann T, Honicke P, Wirtz M, Hell R, Rennenberg H, Kopriva S (2004) Regulation of sulphate assimilation by glutathione in poplars (Populus tremula x P. alba) of wild type and overexpressing gamma-glutamylcysteine synthetase in the cytosol. J Exp Bot 55:837-845PubMedCrossRefGoogle Scholar
  108. Hatzfeld Y, Lee S, Lee M, Leustek T, Saito K (2000) Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248:51-58PubMedCrossRefGoogle Scholar
  109. Hebeler M, Hentrich S, Mayer A, Leibfritz D, Grimme LH (1992) Phosphate regulation and compartmentation in Chlamydomonas reinhardtii studied by in vivo 31P-NMR. In: Murat N (ed) Research in Photosynthesis. Kluwer, the Netherlands, pp 717-720CrossRefGoogle Scholar
  110. Herschbach C, Rennenberg H (1994) Influence of glutathione (GSH) on net uptake of sulfate and sulfate transport in tobacco plants. J Exp Bot 45:1069-1076CrossRefGoogle Scholar
  111. Hesse H, Lipke J, Altmann T, Hofgen R (1999) Molecular cloning and expression analysis of mitochondrial and plastidic isoforms of cysteine synthase [O-acetylserine(thio)lyase] from Arabidopsis thaliana. Amino Acids 16:113-131PubMedCrossRefGoogle Scholar
  112. Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931-1946PubMedCrossRefGoogle Scholar
  113. Ho MS, Carniol K, Losick R (2003) Evidence in support of a docking model for the release of the transcription factor sigma F from the antisigma factor SpoIIAB in Bacillus subtilis. J Biol Chem 278:20898-20905PubMedCrossRefGoogle Scholar
  114. Howarth JR, Fourcroy P, Davidian JC, Smith FW, Hawkesford MJ (2003) Cloning of two contrasting high-affinity sulfate transporters from tomato induced by low sulfate and infection by the vascular pathogen Verticillium dahliae. Planta 218:58-64PubMedCrossRefGoogle Scholar
  115. Huang K, Beck CF (2003) Phototropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 100:6269-6274PubMedCrossRefGoogle Scholar
  116. Im CS, Eberhard S, Huang K, Beck C, Grossman AR (2006) Phototropin involvement in expression of genes encoding chlorophyll and carotenoid biosynthesis enzymes and LHC apoproteins in Chlamydomonas reinhardtii. Plant J 48:1-16PubMedCrossRefGoogle Scholar
  117. 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 103:7911-7916PubMedCrossRefGoogle Scholar
  118. Jensen LT, Ajua-Alemanji M, Culotta VC (2003) The Saccharomyces cerevisiae high affinity phosphate transporter encoded by PHO84 also functions in manganese homeostasis. J Biol Chem 278:42036-42040PubMedCrossRefGoogle Scholar
  119. Jin T, Huppe HC, Turpin DH (1998) In vitro reconstitution of electron transport from glucose-6-phosphate and NADPH to nitrite. Plant Physiol 117:303-309PubMedCrossRefGoogle Scholar
  120. Johnson DW, Turner J, Kelly JM (1982) The effects of acid rain on forest nutrient status. Water Res 18:449-461CrossRefGoogle Scholar
  121. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619-633PubMedCrossRefGoogle Scholar
  122. Jost W, Bak H, Blund K, Terpstra P, Beintema JJ (1991) Amino acid sequence of an extracellular, phosphate-starvation-induced ribonuclease from cultured tomato (Lycopersicon esculentum) cells. Eur J Biochem 198:1-6PubMedCrossRefGoogle Scholar
  123. Juma NG, Tabatabai MA (1988) Comparison of kinetic and thermodynamic parameters of phosphomonoesterases of soils and corn and soybean roots. Soil Biol Biochem 20:533-540CrossRefGoogle Scholar
  124. Jungk A, Asher CJ, Edwards DG, Meyers D (1990) Influence of phosphate status on phosphate uptake kinetics of maize (Zea mays) and soybean (Glycine max). Plant Soil 124:175-182CrossRefGoogle Scholar
  125. Kagawa T, Wada M (2002) Blue light-induced chloroplast relocation. Plant Cell Physiol 43:367-371PubMedCrossRefGoogle Scholar
  126. Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138-2141PubMedCrossRefGoogle Scholar
  127. Kamiya A (1988) Blue light-induced in vivo absorbance changes and in vitro activation of nitrate reductase in nitrate-starved Chlorella mutant. Plant Cell Physiol 29:489-496Google Scholar
  128. Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22-29PubMedCrossRefGoogle Scholar
  129. Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004a) Root-to-shoot transport of sulfate in Arabidopsis - Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136:4198-4204PubMedCrossRefGoogle Scholar
  130. Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004b) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693-2704PubMedCrossRefGoogle Scholar
  131. Kawashima CG, Berkowitz O, Hell R, Noji M, Saito K (2005) Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol 137:220-230PubMedCrossRefGoogle Scholar
  132. Kieber DJ, Jiao J, Kiene RP, Bates TS (1996) Impact of dimethylsulfide photochemistry on methyl sulfur cycling in the equatorial Pacific Ocean. J Geophys Res 101:3715-3722CrossRefGoogle Scholar
  133. Kim H, Hirai MY, Hayashi H, Chino M, Naito S, Fujiwara T (1999) Role of O-acetyl-L-serine in the coordinated regulation of the expression of a soybean seed storage-protein gene by sulfur and nitrogen nutrition. Planta 209:282-289PubMedCrossRefGoogle Scholar
  134. Kinoshita T, Emi T, Tominaga M, Sakamoto K, Shigenaga A, Doi M, Shimazaki K (2003) Blue-light- and phosphorylation-dependent binding of a 14-3-3 protein to phototropins in stomatal guard cells of broad bean. Plant Physiol 133:1453-1463PubMedCrossRefGoogle Scholar
  135. Kirk DL, Kirk MM (1978) Carrier-mediated uptake of arginine and urea by Chlamydomonas reinhardtii. Plant Physiol 61:556-560PubMedCrossRefGoogle Scholar
  136. Klonus D, Höfgen R, Willmitzer L, Riesmeier J (1994) Isolation and characterization of two cDNA clones encoding ATP-sulfurylases from potato by complementation of a yeast mutant. Plant J 6:105-112PubMedCrossRefGoogle Scholar
  137. Ko SB, Shcheynikov N, Choi JY, Luo X, Ishibashi K, Thomas PJ, Kim JY, Kim KH, Lee MG, Naruse S, Muallem S (2002) A molecular mechanism for aberrant CFTR-dependent HCO3 transport in cystic fibrosis. EMBO J 21:5662-5672PubMedCrossRefGoogle Scholar
  138. Kobayashi I, Fujiwara S, Shimogawara K, Kaise T, Usuda H, Tsuzuki M (2003) Insertional mutagenesis in a homologue of a Pi transporter gene confers arsenate resistance on Chlamydomonas. Plant Cell Physiol 44:597-606PubMedCrossRefGoogle Scholar
  139. Koh S, Wiles AM, Sharp JS, Naider FR, Becker JM, Stacey G (2002) An oligopeptide transporter gene family in Arabidopsis. Plant Physiol 128:21-29PubMedCrossRefGoogle Scholar
  140. Komelli A, O’Shea EK (1999) Roles of phophorylation sites in regulatin activity of the transcription factor Pho4. Science 284:977-980CrossRefGoogle Scholar
  141. Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot (Lond) 97:479-495CrossRefGoogle Scholar
  142. Koprivova A, Suter M, den Camp RO, Brunhold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737-746PubMedCrossRefGoogle Scholar
  143. Kraegeloh A, Amendt B, Kunte HJ (2005) Potassium transport in a halophilic member of the bacteria domain: identification and characterization of the K+ uptake systems TrkH and TrkI from Halomonas elongata DSM 2581T. J Bacteriol 187:1036-1043PubMedCrossRefGoogle Scholar
  144. Kredich N (1992) The molecular basis for posititive regulation of cys promoters in Salmonela typhimurium and Escherichia coli. Mol Microbiol 6:2747-2753PubMedCrossRefGoogle Scholar
  145. Kudla J, Hayes R, Gruissem W (1996) Polyadenylation accelerates degradation of chloroplast mRNA. EMBO J 15:7137-7146PubMedGoogle Scholar
  146. Kugita M, Kaneko A, Yamamoto Y, Takeya Y, Matsumoto T, Yoshinaga K (2003) The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into the earliest land plants. Nucleic Acids Res 31:716-721PubMedCrossRefGoogle Scholar
  147. Kunert KJ, Foyer C (1993) Thiol/disulfide exchange in plants. In: de Kik LJ, Stulen I, Rennenberg H, Brunold C, Rauser WE (eds) Sulfur nutrition and sulfur assimilation in higher plants. SPB Academic, the Hague, the Netherlands, pp 139-151Google Scholar
  148. Kustu S, Inwood W (2006) Biological gas channels for NH3 and CO2 : evidence that Rh (Rhesus) proteins are CO2 channels. Transfus Clin Biol 13:103-110PubMedCrossRefGoogle Scholar
  149. Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Physiol 47:569-593Google Scholar
  150. Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO4 uptake in intact canola: the role of phloem-translocated glutathione. Plant Physiol 111:147-157PubMedGoogle Scholar
  151. Lappartient AG, Vidmar JJ, Leustek T, Glass ADM, Touraine B (1999) Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J 18:89-95PubMedCrossRefGoogle Scholar
  152. Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts: the effect of hydrogen peroxide and of paraquat. Biochem J 210:899-903PubMedGoogle Scholar
  153. Lea PJ, Robinson SA, Stewart GR (1990) The enzymology and metabolism of glutamine, glutamate, and asparagine. In: Miflin BJ, Lea PJ (eds) The biochemistry of plants: a comprehensive treatise. Academic Press, New York, pp 121-160Google Scholar
  154. Lee RB (1988) Phosphatase influx and extracellular phosphatase activity in barley roots and rose cells. New Phytol 109:141-148CrossRefGoogle Scholar
  155. Lee S, Leustek T (1998) APS kinase from Arabidopsis thaliana : genomic organization, expression and kinetic analysis of the recombinant enzyme. Biochem Biophys Res Commun 247:171-175PubMedCrossRefGoogle Scholar
  156. Lee S, Leustek T (1999) The effect of cadmium on sulfate assimilation enzymes in Brassica juncea. Plant Sci 141:201-207Google Scholar
  157. Lefebvre DD, Clarkson DT (1984) Characterization of orthophosphate absorption by pea root protoplasts. J Exp Bot 35:1265-1276CrossRefGoogle Scholar
  158. Lefebvre DD, Duff SMG, Fife CA, Julien-Inalsingh C, Plaxton WC (1990) Response to phosphate deprivation in Brassica nigra suspension cells: enhancement of intracellular, cell surface and secreted phosphatase activities compared to increases in Pi-absorption rate. Plant Physiol 93:504-511PubMedCrossRefGoogle Scholar
  159. Leitao JM, Lorenz B, Bachinski N, Wilhelm C, Muller WEG, Schroder HC (1995) Osmotic-stress-induced synthesis and degradation of inorganic polyphosphates in the alga Phaeodactylum tricornutum. Mar Ecol Prog Ser 121:279-288CrossRefGoogle Scholar
  160. Lejay L, Tillard P, Lepetit M, Olive FD, Filleur S, Daniel-Vedele F, Gojon A (1999) Molecualr and functional regulation of two NO3 uptake systems by N- and C-status of Arabidopsis plants. Plant J 18:509-519PubMedCrossRefGoogle Scholar
  161. Lemieux C, Otis C, Turmel M (2000) Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature 403:649-652PubMedCrossRefGoogle Scholar
  162. Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120:637-643PubMedCrossRefGoogle Scholar
  163. Leustek T, Murillo M, Cervantes M (1994) Cloning of a cDNA encoding ATP sulfurylase from Arabidopsis thaliana by functional expression in Saccharomyces cerevisiae. Plant Physiol 105:897-902PubMedCrossRefGoogle Scholar
  164. Li D, Zhu H, Liu K, Liu X, Leggewie G, Udvardi M, Wang D (2002) Purple acid phosphatases of Arabidopsis thaliana - Comparative analysis and differential regulation by phosphate deprivation. J Biol Chem 277:27772-27781PubMedCrossRefGoogle Scholar
  165. Lien T, Knutsen G (1973) Phosphate as a control factor in cell division of Chlamydomonas reinhardti, studies in synchronous culture. Exptl Cell Res 78:79-88PubMedCrossRefGoogle Scholar
  166. Lin H, Goodenough UW (2007) Gametogenesis in the Chlamydomonas reinhardtii minus mating type is controlled by two genes, MID and MTD1. Genetics 176:913-925PubMedCrossRefGoogle Scholar
  167. Lipsick JS (1996) One billion year of Myb. Oncogene 13:223-235PubMedGoogle Scholar
  168. Lisitsky I, Kotler A, Schuster G (1997) The mechanism of preferential degradation of polyadenylated RNA in the chloroplast - The exoribonuclease 100RNP/polynucleotide phosphorylase displays high binding affinity for poly(A) sequence. J Biol Chem 272:17648-17653PubMedCrossRefGoogle Scholar
  169. Liu KH, Tsay YF (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22:1005-1013PubMedCrossRefGoogle Scholar
  170. Logan HM, Cathala N, Grignon C, Davidian JC (1996) Cloning of a cDNA encoded by a member of the Arabidopsis thaliana ATP sulfuylase multigene family: Expression studies in yeast and in relation to plant sulfur nutrition. J Biol Chem 271:12227-12233PubMedCrossRefGoogle Scholar
  171. Lomans BP, van der Drift C, Pol A, Op den Camp HJ (2002) Microbial cycling of volatile organic sulfur compounds. Cell Mol Life Sci 59:575-588PubMedCrossRefGoogle Scholar
  172. Loppes R (1976a) Genes involved in the regulation of the neutral phosphatase in Chlamydomonas reinhardi. Mol Gen Genet 148:315-321PubMedCrossRefGoogle Scholar
  173. Loppes R (1976b) Release of enzymes by normal and wall-free cells of Chlamydomonas. J Bacteriol 128:114-116PubMedGoogle Scholar
  174. Loppes R, Deltour R (1981) A pleiotropic mutant of Chlamydomonas reinhardi showing cell wall abnormalities and altered phosphatase activities. Plant Sci Lett 21:193-197CrossRefGoogle Scholar
  175. Loppes R, Matagne RF (1973) Acid phosphatase mutants in Chlamydomonas : isolation and characterization by biochemical, electrophoretic and genetic analysis. Genetics 75:593-604PubMedGoogle Scholar
  176. Loppes R, Braipson J, Matagne RF, Sassen A, Ledoux L (1977) Regulation of the neutral phosphatase in Chlamydomonas reinhardi : an immunogenetic study of wild-type and mutant strains. Biochem Genet 15:1147-1157PubMedCrossRefGoogle Scholar
  177. Lovelock JE (1972) Gaia as seen through the atmosphere. Atmos Environ 6:579-580CrossRefGoogle Scholar
  178. Lunn JE, Droux M, Martin J, Douce R (1990) Localization of ATP sulfurylase and O-acetyl(thiol)lyase in spinach leaves. Plant Physiol 94:1345-1352PubMedCrossRefGoogle Scholar
  179. MacDonald NW, Burton AJ, Jurgensen MF, McLaughlin JW, Mroz GD (1991) Variation in forest soil properties along a Great Lakes air pollution gradient. Soil Sci Soc Am J 55:1709-1715CrossRefGoogle Scholar
  180. Mahler RJ, Maples RL (1986) Responses of wheat to sulfur fertilization. Commun Soil Sci Plant Anal 17:975-988CrossRefGoogle Scholar
  181. Mahler RJ, Maples RL (1987) Effect of sulfur additions on soil and the nutrition of wheat. Commun Soil Sci Plant Anal 18:653-673CrossRefGoogle Scholar
  182. Mann AF, Fentem PA, Stewart GR (1979) Identification of 2 forms of glutamine synthetase in barley (Hordeum vulgares). Biochem Biophys Res Commun 88:515-521PubMedCrossRefGoogle Scholar
  183. Mariscal V, Moulin P, Orsel M, Miller AJ, Fernandez E, Galvan A (2006) Differential regulation of the Chlamydomonas Nar1 gene family by carbon and nitrogen. Protist 157:421-433PubMedCrossRefGoogle Scholar
  184. Marquez AG, Galvan F, Vega JM (1984) Purification and characterization of the NADH-glutamate synthase from Chlamydomonas reinhardtii. Plant Sci 34:305-314Google Scholar
  185. Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol 47:127-158Google Scholar
  186. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, LondonGoogle Scholar
  187. Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235-3251PubMedCrossRefGoogle Scholar
  188. Matagne RF, Loppes R (1975) Isolation and study of mutants lacking a derepressible phosphatase in Chlamydomonas reinhardi. Genetics 80:239-250PubMedGoogle Scholar
  189. Matagne RF, Loppes R, Deltour R (1976) Phosphatases of Chlamydomonas reinhardi : Biochemical and cytochemical approach with specific mutants. J Bacteriol 126:937-950PubMedGoogle Scholar
  190. Matsumura T, Sakakibara H, Nakano R, Kimata Y, Sugiyama T, Hase T (1997) A nitrate-inducible ferredoxin in maize roots - genomic organization and differential expression of two non-photosynthetic ferredoxin isoproteins. Plant Physiol 114:653-660PubMedCrossRefGoogle Scholar
  191. May MJ, Leaver CJ (1994) Arabidopsis thaliana Ψ-glutamylcysteine synthase is structurally unrelated to mammalian, yeast and Escherichia coli homologs. Proc Natl Acad Sci USA 91:10059-10063PubMedCrossRefGoogle Scholar
  192. McInerney P, Mizutani T, Shiba T (2006) Inorganic polyphosphate interacts with ribosomes and promotes translation fidelity in vitro and in vivo. Mol Microbiol 60:438-447PubMedCrossRefGoogle Scholar
  193. McPharlin IR, Bieleski RL (1987) Phosphate uptake by Spirodela and Lemna during early phosphorus deficiency. Aust J Plant Physiol 14:561-572Google Scholar
  194. Meister A (1994) Glutathione-ascorbic acid antioxidant system in animals. J Biol Chem 269:9397-9400PubMedGoogle Scholar
  195. Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711-760PubMedCrossRefGoogle Scholar
  196. Melis A (2007) Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 226:1075-1086PubMedCrossRefGoogle Scholar
  197. Melis A, Chen HC (2005) Chloroplast sulfate transport in green algae-genes, proteins and effects. Photosynth Res 86:299-307PubMedCrossRefGoogle Scholar
  198. Merchan F, van den Ende H, Fernandez E, Beck CF (2001) Low-expression genes induced by nitrogen starvation and subsequent sexual differentiation in Chlamydomonas reinhardtii, isolated by the differential display technique. Planta 213:309-317PubMedCrossRefGoogle Scholar
  199. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245-250PubMedCrossRefGoogle Scholar
  200. Miller AJ, Smith SJ (1996) Nitrate transport and compartmentation in cereal roots. J Exp Bot 47:843-854CrossRefGoogle Scholar
  201. Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58:2297-2306PubMedCrossRefGoogle Scholar
  202. Minoda A, Sato N, Nozaki H, Okada K, Takahashi H, Sonoike K, Tsuzuki M (2002) Role of sulfoquinovosyl diacylglycerol for the maintenance of photosystem II in Chlamydomonas reinhardtii. Eur J Biochem 269:2353-2358PubMedCrossRefGoogle Scholar
  203. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun D-J, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102:7760-7765PubMedCrossRefGoogle Scholar
  204. Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447:1126-1129PubMedCrossRefGoogle Scholar
  205. Moseley JL, Grossman AR (2009) Phosphorus limitation from the physiological to the genomic. In: EH Harris, D Stern, GB Witman (eds) The Chlamydomonas Sourcebook. Academic Press, Amsterdam, pp 189-215Google Scholar
  206. Moseley JL, Chang CW, Grossman AR (2006) Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot Cell 5:26-44PubMedCrossRefGoogle Scholar
  207. Moseley J, Gonzalez-Ballester D, Pootakham W, Bailey S, Grossman AR (2009) Genetic interactions between regulators of Chlamydomonas phosphorus and sulfur deprivation responses. Genetics 181:889-905PubMedCrossRefGoogle Scholar
  208. Muchhal US, Raghothama KG (1999) Transcriptional regulation of plant phosphate transporters. Proc Natl Acad Sci USA 96:5868-5872PubMedCrossRefGoogle Scholar
  209. Murillo M, Leustek T (1995) Adenosine-5′-triphosphate sulfurylase fom Arabidopsis thaliana and Escherichia coli are functionally equivalent but structurally and kinetically divergent: nucleotide sequence of two adenosine-5′-triphosphate sulfurylase cDNAs fom Arabidopsis thaliana and analysis of a recombinant enzyme. Arch Biochem Biophys 323:195-204PubMedCrossRefGoogle Scholar
  210. Mus F, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii : anoxic gene expression, hydrogenase induction and metabolic pathways. J Biol Chem 282:25475-25486PubMedCrossRefGoogle Scholar
  211. Muttucumaru N, Halford NG, Elmore JS, Dodson AT, Parry M, Shewry PR, Mottram DS (2006) Formation of high levels of acrylamide during the processing of flour derived from sulfate-deprived wheat. J Agric Food Chem 54:8951-8955PubMedCrossRefGoogle Scholar
  212. Naito S, Yokota-Hirai M, Chino M, Komeda Y (1994) Expression of soybean (Glycine max L. Merr.) seed storage protein gene in transgenic Arabidopsis thaliana and its response to nutritional stress and to abscisic acid mutations. Plant Physiol 104:497-503PubMedGoogle Scholar
  213. Najafi SM, Harris DA, Yudkin MD (1996) The SpoIIAA protein of Bacillus subtilis has GTP-binding properties. J Bacteriol 178:6632-6634PubMedGoogle Scholar
  214. Nakazato H, Okamoto T, Ishikawa M, Okuyama H (1997) Purification and characterization of phosphate inducibly synthesized in Spirodela oligorrhiza grown under phosphate deficient conditions. Plant Physiol 35:437-446Google Scholar
  215. Nanatani K, Fujiki T, Kanou K, Takeda-Shitaka M, Umeyama H, Ye L, Wang X, Nakajima T, Uchida T, Maloney PC, Abe K (2007) Topology of AspT, the aspartate: alanine antiporter of Tetragenococcus halophilus, determined by site-directed fluorescence labeling. J Bacteriol 189:7089-7097PubMedCrossRefGoogle Scholar
  216. Navarro MT, Prieto R, Fernandez E, Galvan A (1996) Constitutive expression of nitrate reductase changes the regulation of nitrate and nitrite transporters in Chlamydomonas reinhardtii. Plant J 9:819-827CrossRefGoogle Scholar
  217. Nishimura Y, Kikis EA, Zimmer SL, Komine Y, Stern DB (2004) Antisense transcript and RNA processing alterations suppress instability of polyadenylated mRNA in Chlamydomonas chloroplasts. Plant Cell 16:2849-2869PubMedCrossRefGoogle Scholar
  218. Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138-1148PubMedCrossRefGoogle Scholar
  219. Noctor G, Arisi AC, Jouanin L, Kunert KJ, Rennenberg H, Foyer C (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transgenic plants. J Exp Bot 49:623-647Google Scholar
  220. Noji M, Saito K (2002) Molecular and biochemical analysis of serine acetyltransferase and cysteine synthase towards sulfur metabolic engineering in plants. Amino Acids 22:231-243PubMedCrossRefGoogle Scholar
  221. Noji M, Inoue K, Kimura N, Gouda A, Saito K (1998) Isoform-dependent differences in feedback regulation and subcellular localization of serine acetyltransferase involved in cysteine biosynthesis from Arabidopsis thaliana. J Biol Chem 273:32739-32745PubMedCrossRefGoogle Scholar
  222. Noji M, Takagi Y, Kimura N, Inoue K, Saito M, Horikoshi M, Saito F, Takahashi H, Saito K (2001) Serine acetyltransferase involved in cysteine biosynthesis from spinach: molecular cloning, characterization and expression analysis of cDNA encoding a plastidic isoform. Plant Cell Physiol 42:627-634PubMedCrossRefGoogle Scholar
  223. Nürnberger T, Abel S, Jost W, Glund K (1990) Induction of an extracellular ribonuclease in cultured tomato cells upon phosphate starvation. Plant Physiol 92:970-976PubMedCrossRefGoogle Scholar
  224. O’Connell KF, Baker RE (1992) Possible cross-regulation of phosphate and sulfate metabolism in Saccharomyces cerevisiae. Genetics 132:63-73PubMedGoogle Scholar
  225. Ogawa N, DeRisi J, Brown PO (2000) New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Mol Biol Cell 11:4309-4321PubMedGoogle Scholar
  226. Ohta N, Matsuzaki M, Misumi O, Miyagishima SY, Nozaki H, Tanaka K, Shin IT, Kohara Y, Kuroiwa T (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10:67-77PubMedCrossRefGoogle Scholar
  227. Ohyama K, Fukuzawa H, Kohchi T, Sano T, Sano S, Shirai H, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1988) Structure and organization of Marchantia polymorpha chloroplast genome. I. Cloning and gene identification. J Mol Biol 203:281-298PubMedCrossRefGoogle Scholar
  228. Okumoto S, Koch W, Tegeder M, Fischer WN, Biehl A, Leister D, Stierhof YD, Frommer WB (2004) Root phloem-specific expression of the plasma membrane amino acid proton co-transporter AAP3. J Exp Bot 55:2155-2168PubMedCrossRefGoogle Scholar
  229. Ozcan S, Dover J, Rosenwald AG, Wolf S, Johnston M (1996) Two glucose transporters in Saccharomyces cerevisiae are glucose sensors that generate a signal for induction of gene expression. Proc Natl Acad Sci USA 93:12428-12432PubMedCrossRefGoogle Scholar
  230. Ozcan S, Dover J, Johnston M (1998) Glucose sensing and signaling by two glucose receptors in the yeast Saccharomyces cerevisiae. EMBO J 17:2566-2573PubMedCrossRefGoogle Scholar
  231. Pabo CO, Sauer RT (1992) Transcription factors: structural families and principles of DNA recognition. Annu Rev Biochem 61:1053-1095PubMedCrossRefGoogle Scholar
  232. Pasquale SM, Goodenough UW (1987) Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J Cell Biol 105:2279-2292PubMedCrossRefGoogle Scholar
  233. Patni NJ, Dhawale SW, Aaronson S (1977) Extracellular phosphatases of Chlamydomonas reinhardi and their regulation. J Bacteriol 130:205-211PubMedGoogle Scholar
  234. Peltier G, Schmidt GW (1991) Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 88:4791-4795PubMedCrossRefGoogle Scholar
  235. Petrucco S, Bolchi A, Foroni C, Percudani R, Rossi GL, Ottonello S (1996) A maize gene encoding as NADPH binding enzyme highly homologous to isoflavone reductase is activated in response to sulfur starvation. Plant Cell Environ 8:69-80Google Scholar
  236. Peuke AD, Jeschke WD, Hartung W (1998) Foliar application of nitrate or ammonium as sole nitrogen supply in Ricinus communis. II. The flows of cations, chloride and abscisic acid. New Phytol 140:625-636CrossRefGoogle Scholar
  237. Piedras P, Pineda M, Muñoz J, Cardenas J (1992) Purification and characterization of an L-amino-acid oxidase from Chlamydomonas reinhardtii. Planta 188:13-18CrossRefGoogle Scholar
  238. Pineda M, Cardenas J (1996) Transport and assimilation of purines in Chlamydomonas reinhardtii. Scientia Marina 60:195-201Google Scholar
  239. Plumley FG, Schmidt GW (1989) Nitrogen-dependent regulation of photosynthetic gene expression. Proc Natl Acad Sci USA 86:2678-2682PubMedCrossRefGoogle Scholar
  240. Poirier Y, Thoma S, Somerville C, Schiefelbein J (1991) A mutant in Arabidopsis deficient in xylem loading of phosphate. Plant Physiol 97:1087-1093PubMedCrossRefGoogle Scholar
  241. Pollock SV, Pootakham W, Shibagaki N, Moseley JL, Grossman AR (2005) Insights into the acclimation of Chlamydomonas reinhardtii to sulfur deprivation. Photosynth Res 86:475-489PubMedCrossRefGoogle Scholar
  242. Pootakham W, Grossman AR (2009) The sulfate transporters of Chlamydononas reinhardtii and their regulation. In PreparationGoogle Scholar
  243. Prieto R, Dubus A, Galvan A, Fernandez E (1996) Isolation and characterization of two new negative regulatory mutants for nitrate assimilation in Chlamydomonas reinhardtii obtained by insertional mutagenesis. Mol Gen Genet 251:461-471PubMedGoogle Scholar
  244. Prior A, Uhrig JF, Heins L, Wiesmann A, Lilliq CH, Stolz C, Soll J, Schwenn JD (1999) Structural and kinetic properties of adenylylsulfate reductase from Catheranthus roseus cell cultures. Biochem Biophys Res Commun 1430:25-38Google Scholar
  245. Quesada A, Fernández E (1994) Expression of nitrate assimilation related genes in Chlamydomonas reinhardtii. Plant Mol Biol 24:185-194PubMedCrossRefGoogle Scholar
  246. Quesada A, Galván A, Schnell R, Lefebvre PA, Fernández E (1993) Five nitrate assimilation-related loci are clustered in Chlamydomonas reinhardtii. Mol Gen Genet 240:387-394PubMedGoogle Scholar
  247. Quesada A, Galván A, Fernández E (1994) Identification of nitrate transporter genes in Chlamydomonas reinhardtii. Plant J 5:407-419PubMedCrossRefGoogle Scholar
  248. Quesada A, Krapp A, Trueman LJ, Daniel-Vedele F, Fernández E, Forde BG, Caboche M (1997) PCR-identification of a Nicotiana plumbaginigolia cDNA homologous to the high-affintiy nitrate transporters of the crnA family. Plant Mol Biol 34:265-274PubMedCrossRefGoogle Scholar
  249. Quesada A, Gomez I, Fernández E (1998) Clustering of the nitrite reductase gene and a light-regulated gene with nitrate assimilation loci in Chlamydomonas reinhardtii. Planta 206:259-265PubMedCrossRefGoogle Scholar
  250. Quiñones MA, Aparicio PJ (1990) Flavin type action spectrum of nitrate utilization by Monoraphidium braunii. Photobiochem Photobiophys 51:689-692Google Scholar
  251. Quiñones MA, Galván A, Fernández E, Aparicio PJ (1999) Blue-light requirement for the biosynthesis of an NO2 transport system in the Chlamydomonas reinhardtii nitrate transport mutant S10. Plant Cell Environ 22:1169-1175CrossRefGoogle Scholar
  252. Quisel J, Wykoff D, Grossman AR (1996) Biochemical characterization of the extracellular phosphatases produced by phosphorus-deprived Chlamydomonas reinhardtii. Plant Physiol 111:839-848PubMedCrossRefGoogle Scholar
  253. Raghothama KG (2000a) Phosphate transport and signaling. Curr Opin Plant Biol 3:182-187PubMedGoogle Scholar
  254. Raghothama KG (2000b) Phosphorus acquisition; plant in the driver’s seat. Trends Plant Sci 5:412-413PubMedCrossRefGoogle Scholar
  255. Rauser WE (1987) Changes in glutathione content of maize seedlings exposed to cadmium. Plant Sci 51:171-175CrossRefGoogle Scholar
  256. Ravanel S, Droux M, Douce R (1995a) Methionine biosynthesis in higher plants. Purification and characterization of cystathionine γ-synthase from spinach chloroplasts. Arch Biochem Biophys 316:572-584PubMedCrossRefGoogle Scholar
  257. Ravanel S, Ruffet ML, Douce R (1995b) Cloning of an Arabidopsis thaliana cDNA encoding cystathionine β-lyase by functional complementation in Escherichia coli. Plant Mol Biol 29:875-882PubMedCrossRefGoogle Scholar
  258. Ravanel S, Job D, Douce R (1996) Purification and properties of cystathionine β-lyase from Arabidopsis thaliana overexpressed in Escherichia coli. Biochem J 320:383-392PubMedGoogle Scholar
  259. Ravanel S, Gakiere B, Job D, Douce R (1998a) Cystathionine γ-synthase from Arabidopsis thaliana : purification and biochemical characterization of the recombinant enzyme overexpressed in Escherichia coli. Biochem J 331:639-648PubMedGoogle Scholar
  260. Ravanel S, Gakiere B, Job D, Douce R (1998b) The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci USA 95:7805-7812PubMedCrossRefGoogle Scholar
  261. Ravina CG, Barroso C, Vega JM, Gotor C (1999) Cysteine biosynthesis in Chlamydomonas reinhardtii - molecular cloning and regulation of O-acetylserine(thiol)lyase. Eur J Biochem 264:848-853PubMedCrossRefGoogle Scholar
  262. Ravina CG, Chang CI, Tsakraklides GP, McDermott JP, Vega JM, Leustek T, Gotor C, Davies J (2002) Transcriptional and post-transcriptional control of cysteine biosynthesis in Chlamydomonas reinhardtii. Plant Physiol 130:2076-2084PubMedCrossRefGoogle Scholar
  263. Rawlins MR, Leaver CJ, May MJ (1995) Characterization of an Arabidopsis thaliana cDNA encoding glutathione synthetase. FEBS Lett 376:81-86PubMedCrossRefGoogle Scholar
  264. Redinbaugh MG, Campbell WH (1998) Nitrate regulation of the oxidative pentose phosphate pathway in maize (Zea mays L.) root platids: induction of 6-phosphogluconate dehydorgenase activity, protein and transcript levels. Plant Sci 134:129-140CrossRefGoogle Scholar
  265. Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103:19206-19211PubMedCrossRefGoogle Scholar
  266. Rennenberg H (1982) Glutathione metabolism and possible biological role in higher plants. Phytochem 21:2771-2781CrossRefGoogle Scholar
  267. Rentsch D, Boorer KJ, Frommer WB (1998) Structure and function of plasma membrane amino acid, oligopeptides and sucrose transporters from higher plants. J Memb Biol 162:177-190CrossRefGoogle Scholar
  268. Rexach J, Montero B, Fernandez E, Galvan A (1999) Differential regulation of the high affinity nitrite transport systems III and IV in Chlamydomonas reinhardtii. Plant Cell Environ 12:1441-1453Google Scholar
  269. Rexach J, Fernandez E, Galvan A (2000) The Chlamydomonas reinhardtii Nar1 gene encodes a chloroplast membrane protein involved in nitrite transport. Plant Cell Environ 12:1441-1453Google Scholar
  270. Riekhof WR, Ruckle ME, Lydic TA, Sears BB, Benning C (2003) The sulfolipids 2′-O-acyl-sulfoquinovosyldiacylglycerol and sulfoquinovosyldiacylglycerol are absent from a Chlamydomonas reinhardtii mutant deleted in SQD1. Plant Physiol 133:864-874PubMedCrossRefGoogle Scholar
  271. Ritchie SW, Redinbaugh MG, Shiraishi N, Vrba JM, Campbell WH (1994) Identification of a maize root transcript expressed in the primary response to nitrate: characterization of a cDNA with homology to ferredoxin-NADP oxidoreductase. Plant Mol Biol 26:679-690PubMedCrossRefGoogle Scholar
  272. Rodriguez C, Sanz P, Gancedo C (2003) New mutations of Saccharomyces cerevisiae that partially relieve both glucose and galactose repression activate the protein kinase Snf1. FEMS Yeast Res 3:77-84PubMedCrossRefGoogle Scholar
  273. Romer S, Dharlingue A, Camara B, Schantz R, Kuntz M (1992) Cysteine synthase from Capsicum annuum chromoplants: characterization and cDNA cloning of an up-regulated enzyme during fruit development. J Biol Chem 267:17966-17970PubMedGoogle Scholar
  274. Rost B, Schneider R, Sander C (1997) Protein fold recognition by prediction-based threading. J Mol Biol 270:471-480PubMedCrossRefGoogle Scholar
  275. Rotte C, Leustek T (2000) Differential subcellular localization and expression of ATP sulfurylase and 5′-adenylylsulfate reductase during ontogenesis of Arabidopsis leaves indicates that cytosolic and plastid forms of ATP sulfurylase may have specialized functions. Plant Physiol 124:715-724PubMedCrossRefGoogle Scholar
  276. Rouached H, Berthomieu P, El Kassis E, Cathala N, Catherinot V, Labesse G, Davidian JC, Fourcroy P (2005) Structural and functional analysis of the C-terminal STAS (sulfate transporter and anti-sigma antagonist) domain of the Arabidopsis thaliana sulfate transporter SULTR1.2. J Biol Chem 280:15976-15983PubMedCrossRefGoogle Scholar
  277. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phospate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122-2133PubMedCrossRefGoogle Scholar
  278. Ruffet M-L, Lebrun M, Droux M, Douce R (1995) Subcellular localization of serine acetyltransferase from Pisum sativum and characterization of an Arabidopsis thaliana putative cytosolic isoform. Eur J Biochem 227:500-509PubMedCrossRefGoogle Scholar
  279. Ruiz FA, Marchesini N, Seufferheld M, Govindjee, Docampo R (2001) The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J Biol Chem 276:46196-46203Google Scholar
  280. Sachay JE, Wallace RL, Johns MA (1991) Phosphate stress response in hydroponically grown maize. Plant Soil 132:85-90CrossRefGoogle Scholar
  281. Saito K (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr Opin Plant Biol 3:188-195PubMedGoogle Scholar
  282. Saito K, Miura N, Yamazaki M, Hirano H, Murakoshi I (1992) Molecular cloning and bacterial expression of cDNA encoding a plant cysteine synthase. Proc Natl Acad Sci USA 89:8078-8082PubMedCrossRefGoogle Scholar
  283. Saito K, Tatsuguchi K, Takagi Y, Murakoshi I (1994) Isolation and charcterization of cDNA that encodes a putative mitochondrion-localizing isoform of cysteine synthase [O-acetylserine(thiol)lyase] from Spinacia oleracea. J Biol Chem 269:28187-28192PubMedGoogle Scholar
  284. Saito K, Yokoyama H, Noji M, Murakoshi I (1995) Molecular cloning and characterization of a plant serine acetyltransferase playing a regulatory role in cysteine biosynthesis from watermelon. J Biol Chem 270:16321-16326PubMedCrossRefGoogle Scholar
  285. Saito K, Inoue K, Fukushima R, Noji M (1997) Genomic structure and expression analyses of serine acetyltransferase gene in Citrullus vulgaris (watermelon). Gene 189:57-63PubMedCrossRefGoogle Scholar
  286. Sato N, Sonoike K, Tsuzuki M, Kawaguchi A (1995a) Impaired Photosystem II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyl diacylglycerol. Eur J Biochem 234:16-23PubMedCrossRefGoogle Scholar
  287. Sato N, Tsuzuki M, Matsuda Y, Ehara T, Osafune T, Kawaguchi A (1995b) Isolation and characterization of mutants affected in lipid metabolism of Chlamydomonas reinhardtii. Eur J Biochem 230:987-993PubMedCrossRefGoogle Scholar
  288. Savard F, Richard C, Guertin M (1996) The Chlamydomonas reinhardtii LI818 gene represents a distant relative of the cabI\II genes that is regulated during the cell cycle and in response to illumination. Plant Mol Biol 32:461-473PubMedCrossRefGoogle Scholar
  289. Scheible WR, Lauerer M, Schulze ED, Caboche M, Stitt M (1997) Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J 11:671-691CrossRefGoogle Scholar
  290. Scheller HV, Huang B, Hatch E, Goldsbrough PB (1987) Phytochelatin synthesis and glutathione levels in response to heavy metals in tomato cells. Plant Physiol 85:1031-1035PubMedCrossRefGoogle Scholar
  291. Schjorring JK, Jensen P (1984) Phosphorus nutrition of barley, buckwheat and rape seedlings. II. Influx and efflux of phosphorus by intact roots of different P status. Physiol Plantarum 61:584-590CrossRefGoogle Scholar
  292. Schnell RA, Lefebvre PA (1993) Isolation of the Chlamydomonas regulatory gene NIT2 by transposon tagging. Genetics 134:737-747PubMedGoogle Scholar
  293. Schreiner O, Lien T, Knutsen G (1975) The capacity for arylsulfatase synthesis in synchronous and synchronized cultures of Chlamydomonas reinhardtii. Biochim Biophys Acta 384:180-193PubMedCrossRefGoogle Scholar
  294. Schultze M, Quiclet-Sire B, Kondorosi E, Virelizer H, Glushka JN, Endre G, Gero SD, Kondorosi A (1992) Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc Natl Acad Sci USA 89:192-196PubMedCrossRefGoogle Scholar
  295. Schürmann P, Brunold C (1980) Formation of cysteine from adenosine 5′-phosphosulfate (APS) in extracts from spinach chloroplasts. Z. Pflanzenphysiol 100:257-268Google Scholar
  296. Sechley KA, Yamaya T, Oaks A (1992) Compartmentation of nitrogen assimilation in higher plants. Int Rev Cytol 134:85-163CrossRefGoogle Scholar
  297. Setya A, Murillo M, Leustek T (1996) Sulfate reduction in higher plants: molecular evidence for a novel 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 93:13383-13388PubMedCrossRefGoogle Scholar
  298. Shibagaki N, Grossman AR (2004) Probing the function of STAS domains of the Arabidopsis sulfate transporters. J Biol Chem 279:30791-30799PubMedCrossRefGoogle Scholar
  299. Shibagaki N, Grossman AR (2006) The role of the STAS domain in the function and biogenesis of a sulfate transporter as probed by random mutagenesis. J Biol Chem 281:22964-22973PubMedCrossRefGoogle Scholar
  300. Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475-486PubMedCrossRefGoogle Scholar
  301. Shimogawara K, Usuda H (1995) Uptake of inorganic phosphate by suspension-cultured tobacco cells: kinetics and regulation of Pi starvation. Plant Cell Physiol 36:341-351Google Scholar
  302. Shimogawara K, Wykoff DD, Usuda H, Grossman AR (1999) Chlamydomonas reinhardtii mutants abnormal in their responses to phosphorus deprivation. Plant Physiol 120:1-10CrossRefGoogle Scholar
  303. Siderius M, Musgrave A, van den Ende H, Koerten H, Cambier P, van der Meer P (1996) Chlamydomonas eugametos (Chlorophyta) stores phosphate in polyphosphate bodies together with calcium. J Phycol 32:402-409CrossRefGoogle Scholar
  304. Slomovic S, Portnoy V, Liveanu V, Schuster G (2006) RNA polyadenylation in prokaryotes and organelles; different tails tell different tales. Crit Rev Plant Sci 25:65-77CrossRefGoogle Scholar
  305. Smith FW, Rae AL, Hawkesford MJ (2000) Molecular mechanisms of phosphate and sulphate transort in plants. Biochem Biophys Res Commun 1465:236-245Google Scholar
  306. Smith FW, Hawkesford MJ, Ealing PM, Clarkson DT, Vanden Berg PJ, Belcher AR, Warrilow AG (1997) Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. Plant J 12:875-884PubMedCrossRefGoogle Scholar
  307. Smith H (1995) Physiological and ecological function within the phytochrome family. Annu Rev Plant Physiol Plant Mol Biol 46:289-315CrossRefGoogle Scholar
  308. Somerville CR, Ogren WL (1980) Inhibition of photosynthesis in Arabidopsis mutants leaf glutamate synthase activity. Nature 286:257-259CrossRefGoogle Scholar
  309. Soupene E, Inwood W, Kustu S (2004) Lack of the Rhesus protein Rh1 impairs growth of the green alga Chlamydomonas reinhardtii at high CO2. Proc Natl Acad Sci USA 101:7787-7792PubMedCrossRefGoogle Scholar
  310. Stacey G, Koh S, Granger C, Becker JM (2002) Peptide transport in plants. Trends Plant Sci 7:257-263PubMedCrossRefGoogle Scholar
  311. Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2:178-186PubMedCrossRefGoogle Scholar
  312. Stitt M, Krapp A (1999) the interaction betwen elevated carbon dioxide and nitrogen nutrition: the physiological and molecualr background. Plant Cell Environ 22:583-621CrossRefGoogle Scholar
  313. Suetsugu N, Wada M (2007) Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. J Biol Chem 388:927-935Google Scholar
  314. Superti-Furga A, Rossi A, Steinmann B, Gitzelmann R (1996) A chondrodysplasia family produced by mutations in the diastrophic dysplasia sulfate transporter gene: genotype/phenotype correlations. Am J Med Genet 63:144-147PubMedCrossRefGoogle Scholar
  315. Suzuki A, Rothstein SJ (1997) Structure and regulation of ferredoxin-dependent glutamate synthase from Arabidopsis thaliana: cloning of cDNA, expression in different tissues of wild-type and gltS mutant strains and light induction. Eur J Biochem 243:708-718PubMedCrossRefGoogle Scholar
  316. Tadano T, Ozawa K, Sakai H, Osaki M, Matsui H (1993) Secretion of acid phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme secreted by lupin roots. Plant Soil 155-156:95-98CrossRefGoogle Scholar
  317. Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, de Almeida Engler J, Engler G, Van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:11102-11107PubMedCrossRefGoogle Scholar
  318. Takahashi H, Watanabe-Takahashi A, Smith F, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171-182PubMedCrossRefGoogle Scholar
  319. Takahashi H, Braby CE, Grossman AR (2001) Sulfur economy and cell wall biosynthesis during sulfur limitation of Chlamydomonas reinhardtii. Plant Physiol 127:665-673PubMedCrossRefGoogle Scholar
  320. Taylor CB, Green PJ (1991) Genes with homology to fungal and S-gene RNases are expressed in Arabidopsis thaliana. Plant Physiol 96:980-984PubMedCrossRefGoogle Scholar
  321. Taylor CB, Bariola PA, del Cardayré SB, Raines RT, Green PJ (1993) RNS2: a senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation. Proc Natl Acad Sci USA 90:5118-5122PubMedCrossRefGoogle Scholar
  322. Trull MC, Guiltinan MJ, Lynch JP, Deikman J (1997) The response of wild-type and ABA mutant of Arabidopsis thaliana to phosphorous starvation. Plant Cell Environ 20:85-92CrossRefGoogle Scholar
  323. Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK (2007) Nitrate transporters and peptide transporters. FEBS Lett 581:2290-2300PubMedCrossRefGoogle Scholar
  324. Tucker K, Fadool DA (2002) Neurotrophin modulation of voltage-gated potassium channels in rat through TrkB receptors is time and sensory experience dependent. J Physiol 542:413-429PubMedCrossRefGoogle Scholar
  325. Turmel M, Otis C, Lemieux C (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 96:10248-10253PubMedCrossRefGoogle Scholar
  326. Turmel M, Otis C, Lemieux C (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 3:22PubMedCrossRefGoogle Scholar
  327. Turmel M, Otis C, Lemieux C (2006) The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Mol Biol Evol 23:1324-1338PubMedCrossRefGoogle Scholar
  328. Usami S, Abe S, Weston MD, Shinkawa H, Van Camp G, Kimberling WJ (1999) Non-syndromic hearing loss associated with enlarged vestibular aqueduct is caused by PDS mutations. Hum Genet 104:188-192PubMedCrossRefGoogle Scholar
  329. Vallon O, Bulte L, Kuras R, Olive J, Wollman FA (1993) Extensive accumulation of an extracellular L-amino-acid oxidase during gametogenesis of Chlamydomonas reindhartii. Eur J Biochem 215:351-360PubMedCrossRefGoogle Scholar
  330. van der Leij M, Smith SJ, Miller AJ (1998) Remobilization of vacuolar stored nitrate in barley root cells. Planta 205:64-72CrossRefGoogle Scholar
  331. Varin L, Marsolais F, Richard M, Rouleau M (1997) Biochemistry and molecular biology of plant sulfotransferases. FASEB J 11:517-525PubMedGoogle Scholar
  332. Veljanovski V, Vanderbeld B, Knowles VL, Snedden WA, Plaxton WC (2006) Biochemical and molecular characterization of AtPAP26, a vacuolar purple acid phosphatase up-regulated in phosphate-deprived Arabidopsis suspension cells and seedlings. Plant Physiol 142:1282-1293PubMedCrossRefGoogle Scholar
  333. Vidmar JJ, Schjoerring JK, Touraine B, Glass ADM (1999) Regulation of the hvst1 gene encoding a high-affinity sulfate transporter from Hordeum vulgare. Plant Mol Biol 40:883-892PubMedCrossRefGoogle Scholar
  334. Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, Ito S, Tsudzuki J, Nakashima K, Tsudzuki T, Suzuki Y, Hamada A, Ohta T, Inamura A, Yoshinaga K, Sugiura M (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 94:5967-5972PubMedCrossRefGoogle Scholar
  335. Walch-Liu P, Neumann D, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51:227-237PubMedCrossRefGoogle Scholar
  336. Wallsgrove RM, Lea PJ, Miflin BJ (1983) Intracellular localization of aspartate kinase and the enzymes of threonine and methionine biosynthesis in green leaves. Plant Physiol 71:780-784PubMedCrossRefGoogle Scholar
  337. Wang YH, Garvin DF, Kochian LV (2002) Rapid induction of regulatory and transporter genes in response to phosphorus, potassium and iron deficiencies in tomato roots: evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiol 130:1361-1370PubMedCrossRefGoogle Scholar
  338. Warman PR, Sampson HG (1994) Effect of sulfur additions on the yield and elemental composition of canola and spring wheat. J Plant Nutr 17:1817-1825CrossRefGoogle Scholar
  339. Weiss M, Bental M, Pick U (1991) Hydrolysis of polyphosphates and permeability changes in response to osmotic shocks in cells of the halotolerant alga Dunaliella. Plant Physiol 97:1241-1248PubMedCrossRefGoogle Scholar
  340. Werner TP, Amrhein N, Freimoser FM (2007) Inorganic polyphosphate occurs in the cell wall of Chlamydomonas reinhardtii and accumulates during cytokinesis. BMC Plant Biol 7:51PubMedCrossRefGoogle Scholar
  341. Wetzel RG (1983) Limnology (2nd edn). Saunders College Publishing, Philadelphia, PAGoogle Scholar
  342. Wykoff D, Davies J, Grossman A (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129-139PubMedCrossRefGoogle Scholar
  343. Wykoff D, Grossman A, Weeks DP, Usuda H, Shimogawara K (1999) Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci USA 96:15336-15341PubMedCrossRefGoogle Scholar
  344. Yao Q, Li XL, Feng G, Christie P (2001) Mobilization of sparingly soluble inorganic phosphates by external mycelium of an arbuscular mycorrhizal fungus. Plant Soil 230:279-285CrossRefGoogle Scholar
  345. Yehudai-Resheff S, Zimmer SL, Komine Y, Stern DB (2007) Integration of chloroplast nucleic acid metabolism into the phosphate deprivation response in Chlamydomonas reinhardtii. Plant Cell 19:1023-1038PubMedCrossRefGoogle Scholar
  346. Yildiz FH, Davies JP, Grossman AR (1994) Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol 104:981-987PubMedGoogle Scholar
  347. Yildiz FH, Davies JP, Grossman AR (1996) Sulfur availability and the SAC1 gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii. Plant Physiol 112:669-675PubMedCrossRefGoogle Scholar
  348. Yoneda Y, Hieda M, Nagoshi E, Miyamoto Y (1999) Nucleocytoplasmic protein transport and recycling of Ran. Cell Struct Funct 24:425-433PubMedCrossRefGoogle Scholar
  349. Yonekura-Sakakibara K, Onda Y, Ashikari T, Tanaka Y, Kusumi T, Hase T (2000) Analysis of reductant supply systems for ferredoxin-dependent sulfite reductase in photosynthetic and nonphotosynthetic organs of maize. Plant Physiol 122:887-894PubMedCrossRefGoogle Scholar
  350. Yoshimoto N, Takahashi H, Smith WS, Yamaya T, Saito K (2002) Two distinct high affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29:465-473PubMedCrossRefGoogle Scholar
  351. Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H (2007) Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 145:378-388PubMedCrossRefGoogle Scholar
  352. Youssefian S, Nakamura M, Sano H (1993) Tobacco plants transformed with the O-acetylserine(thiol)lyase gene of wheat are resistant to toxic levels of hydrogen sulphide gas. Plant J 4:759-769PubMedCrossRefGoogle Scholar
  353. Zhang D, Lefebvre PA (1997) FAR1, a negative regulatory locus required for the repression if the nitrate reductase gene in Chlamydomonas reinhardtii. Genetics 146:121-133PubMedGoogle Scholar
  354. Zhang L, Melis A (2002) Probing green algal hydrogen production. Philos Trans R Soc Lond B Biol Sci 357:1499-1507; discussion 1507-1411Google Scholar
  355. Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529-6534PubMedCrossRefGoogle Scholar
  356. 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 3:1331-1348PubMedCrossRefGoogle Scholar
  357. Zhao T, Li G, Mi S, Li S, Hannon GJ, Wang XJ, Qi Y (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21:1190-1203PubMedCrossRefGoogle Scholar
  358. Zhou D, Okamoto M, Vidmar JJ, Glass ADM (1999) Regulation of a putative high-affinity nitrate transporter (nrt2;1At) in roots of Arabidopsis thaliana. Plant J 17:563-568CrossRefGoogle Scholar
  359. Zhou JJ, Fernandez E, Galvan A, Miller AJ (2000) A high affinity nitrate transport system from Chlamydomonas requires two gene products. FEBS Lett 466:225-227PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Arthur R. Grossman
    • 1
  • David Gonzalez-Ballester
    • 1
  • Nakako Shibagaki
    • 1
  • Wirulda Pootakham
    • 1
    • 2
  • Jeffrey Moseley
    • 1
  1. 1.Department of Plant BiologyThe Carnegie InstitutionStanfordUSA
  2. 2.Department of Biological SciencesStanford UniversityStanfordUSA

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