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Photo and Nutritional Regulation of Euglena Organelle Development

  • Steven D. SchwartzbachEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 979)

Abstract

Euglena can use light and CO2, photosynthesis, as well as a large variety of organic molecules as the sole source of carbon and energy for growth. Light induces the enzymes, in this case an entire organelle, the chloroplast, that is required to use CO2 as the sole source of carbon and energy for growth. Ethanol, but not malate, inhibits the photoinduction of chloroplast enzymes and induces the synthesis of the glyoxylate cycle enzymes that comprise the unique metabolic pathway leading to two carbon, ethanol and acetate, assimilation. In resting, carbon starved cells, light mobilizes the degradation of the storage carbohydrate paramylum and transiently induces the mitochondrial proteins required for the aerobic metabolism of paramylum to provide the carbon and energy required for chloroplast development. Other mitochondrial proteins are degraded upon light exposure providing the amino acids required for the synthesis of light induced proteins. Changes in protein levels are due to increased and decreased rates of synthesis rather than changes in degradation rates. Changes in protein synthesis rates occur in the absence of a concomitant increase in the levels of mRNAs encoding these proteins indicative of photo and metabolic control at the translational rather than the transcriptional level. The fraction of mRNA encoding a light induced protein such as the light harvesting chlorophyll a/b binding protein of photosystem II, (LHCPII) associated with polysomes in the dark is similar to the fraction associated with polysomes in the light indicative of photoregulation at the level of translational elongation. Ethanol, a carbon source whose assimilation requires carbon source specific enzymes, the glyoxylate cycle enzymes, represses the synthesis of chloroplast enzymes uniquely required to use light and CO2 as the sole source of carbon and energy for growth. The catabolite sensitivity of chloroplast development provides a mechanism to prioritize carbon source utilization. Euglena uses all of its resources to develop the metabolic capacity to utilize carbon sources such as ethanol which are rarely in the environment and delays until the rare carbon source is no longer available forming the chloroplast which is required to utilize the ubiquitous carbon source, light and CO2.

Keywords

Chloroplast Catabolite repression Enzyme induction Euglena Glyoxylate cycle Mitochondria Organelle development Photoregulation Translational control 

Abbreviations

2-D gel

Two dimensional gel electrophoresis

ALA

δ-Aminolevulinic acid

DCMU

(3-(3,4-Dichlorophenyl)-1,1-dime-thylurea)

LHCPI

Light harvesting chlorophyll a/b binding protein of photosystem I

LHCPII

Light harvesting chlorophyll a/b binding protein of photosystem II

PBG

Porphobilinogen

pLHCPII

Precursor to LHCPII

RUBISCO

Ribulose bisphosphate carboxylase-oxygenase

References

  1. App AA, Jagendorf AT (1963) Repression of chloroplast development in Euglena gracilis. J Protozool 10:340–343CrossRefGoogle Scholar
  2. Barnett WE, Schwartzbach SD, Farrelly JG, Schiff JA, Hecker LI (1976) Comments on the translational and transcriptional origin of Euglena chloroplastic aminoacyl-tRNA synthetases. Arch Microbiol 109(3):201–203PubMedCrossRefGoogle Scholar
  3. Beale SI, Foley T (1982) Induction of delta-aminolevulinic-acid synthase activity and inhibition of heme-synthesis in Euglena-gracilis by N-methyl mesoporphyrin-Ix. Plant Physiol 69(6):1331–1333PubMedPubMedCentralCrossRefGoogle Scholar
  4. Beale SI, Foley T, Dzelzkalns V (1981) Delta-aminolevulinic-acid synthase from Euglena-gracilis. Proc Natl Acad Sci U S A 78(3):1666–1669PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bingham S, Schiff JA (1979a) Events surrounding the early development of Euglena chloroplasts. 15. Origin of plastid thylakoid polypeptides in wild-type and mutant cells. Biochim Biophys Acta 547(3):512–530PubMedCrossRefGoogle Scholar
  6. Bingham S, Schiff JA (1979b) Events surrounding the early development of Euglena chloroplasts. 16. Plastid thylakoid polypeptides during greening. Biochim Biophys Acta 547(3):531–543PubMedCrossRefGoogle Scholar
  7. Bouet C, Schantz R, Dubertret G, Pineau B, Ledoigt G (1986) Translational regulation of protein synthesis during light-induced chloroplast development in Euglena. Planta 167(4):511–520PubMedCrossRefGoogle Scholar
  8. Bovarnick JG, Chang SW, Schiff JA, Schwartzbach SD (1974a) Events surrounding the early development of Euglena chloroplasts: experiments with streptomycin in non-dividing cells. J Gen Microbiol 83(0):51–62PubMedCrossRefGoogle Scholar
  9. Bovarnick JG, Schiff JA, Freedman Z, Egan JM (1974b) Events surrounding early development of Euglena chloroplasts-cellular origins of chloroplast enzymes in Euglena. 4. Cellular origins of chloroplast enzymes in Euglena. J Gen Microbiol 83:63–71PubMedCrossRefGoogle Scholar
  10. Brandt P, Winter J (1987) The influence of permanent light and of intermittent light on the reconstitution of the light-harvesting system in regreening Euglena-gracilis. Protoplasma 136(1):56–62CrossRefGoogle Scholar
  11. Breitenberger CA, Graves MC, Spremulli LL (1979) Evidence for the nuclear location of the gene for chloroplast elongation factor G. Arch Biochem Biophys 194(1):265–270PubMedCrossRefGoogle Scholar
  12. Brunold C, Schiff JA (1976) Studies of sulfate utilization of algae: 15. Enzymes of assimilatory sulfate reduction in euglena and their cellular localization. Plant Physiol 57(3):430–436PubMedPubMedCentralCrossRefGoogle Scholar
  13. Buetow DE (1967) Acetate repression of chlorophyll synthesis in Euglena gracilis. Nature 213(5081):1127–1128PubMedCrossRefGoogle Scholar
  14. Cannons A, Merrett MJ (1983) The regulation of synthesis of mitochondrial enzymes in regreening and division-synchronized Euglena cultures. Planta 159(2):125–129PubMedCrossRefGoogle Scholar
  15. Cannons AC, Merrett MJ (1984) Regulation of synthesis of citrate synthase in regreening Euglena gracilis. Eur J Biochem 142(3):597–602PubMedCrossRefGoogle Scholar
  16. Cannons A, Merrett MJ (1985) Citrate-synthase mRNA in relation to enzyme synthesis in division-synchronized Euglena cultures. Planta 164(4):529–533PubMedCrossRefGoogle Scholar
  17. Chelm BK, Hallick RB (1976) Changes in expression of chloroplast genome of Euglena-gracilis during chloroplast development. Biochemistry 15(3):593–599PubMedCrossRefGoogle Scholar
  18. Chelm BK, Hoben PJ, Hallick RB (1977a) Cellular content of chloroplast DNA and chloroplast ribosomal-RNA genes in Euglena-gracilis during chloroplast development. Biochemistry 16(4):782–786PubMedCrossRefGoogle Scholar
  19. Chelm BK, Hoben PJ, Hallick RB (1977b) Expression of chloroplast ribosomal-RNA genes of Euglena-gracilis during chloroplast development. Biochemistry 16(4):776–781PubMedCrossRefGoogle Scholar
  20. Chelm BK, Gray PW, Hallick RB (1978) Mapping of transcribed regions of Euglena-gracilis chloroplast DNA. Biochemistry 17(20):4239–4244PubMedCrossRefGoogle Scholar
  21. Chelm BK, Hallick RB, Gray PW (1979) Transcription program of the chloroplast genome of Euglena-gracilis during chloroplast development. Proc Natl Acad Sci U S A 76(5):2258–2262PubMedPubMedCentralCrossRefGoogle Scholar
  22. Codd GA, Merrett MJ (1970) Enzymes of the glycollate pathway in relation to greening in Euglena gracilis. Planta 95(2):127–132PubMedCrossRefGoogle Scholar
  23. Codd GA, Merrett MJ (1971) The regulation of glycolate metabolism in division synchronized cultures of Euglena. Plant Physiol 47(5):640–643PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cohen D, Schiff JA (1976) Events surrounding the early development of Euglena chloroplasts. Photoregulation of the transcription of chloroplastic and cytoplasmic ribosomal RNAs. Arch Biochem Biophys 177(1):201–216PubMedCrossRefGoogle Scholar
  25. Collins N, Merrett MJ (1975a) Localization of glycollate-pathway enzymes in Euglena. Biochem J 148(2):321–328PubMedPubMedCentralCrossRefGoogle Scholar
  26. Collins N, Merrett MJ (1975b) Microbody-marker enzymes during transition from phototrophic to organotrophic growth in Euglena. Plant Physiol 55(6):1018–1022PubMedPubMedCentralCrossRefGoogle Scholar
  27. Cook JR, Carver M (1966) Partial Photo-repression of glyoxylate by-pass in Euglena. Plant Cell Physiol 7(3):377–383Google Scholar
  28. Corriveau JL, Beale SI (1986) Influence of Gabaculine on growth, chlorophyll synthesis, and delta-aminolevulinic-acid synthase activity in Euglena-gracilis. Plant Sci 45(1):9–17CrossRefGoogle Scholar
  29. Cunningham FX, Schiff JA (1986a) Chlorophyll-protein complexes from Euglena gracilis and mutants deficient in chlorophyll b: I. Pigment composition. Plant Physiol 80(1):223–230PubMedPubMedCentralCrossRefGoogle Scholar
  30. Cunningham FX, Schiff JA (1986b) Chlorophyll-protein complexes from Euglena gracilis and mutants deficient in chlorophyll b: II. Polypeptide composition. Plant Physiol 80(1):231–238PubMedPubMedCentralCrossRefGoogle Scholar
  31. Cushman JC, Price CA (1986) Synthesis and turnover of proteins in proplastids and chloroplasts of Euglena gracilis. Plant Physiol 82(4):972–977PubMedPubMedCentralCrossRefGoogle Scholar
  32. Diamond J, Schiff JA, Kelner A (1975) Photoreactivating enzyme from euglena and the control of its intracellular level. Arch Biochem Biophys 167(2):603–614PubMedCrossRefGoogle Scholar
  33. Dockerty A, Merrett MJ (1979) Isolation and enzymic characterization of euglena proplastids. Plant Physiol 63(3):468–473PubMedPubMedCentralCrossRefGoogle Scholar
  34. Dos Santos FV, Rocchetta I, Conforti V, Bench S, Feldman R, Levin MJ (2007) Gene expression patterns in Euglena gracilis: insights into the cellular response to environmental stress. Gene 389(2):136–145CrossRefGoogle Scholar
  35. Dubertret G (1981) Functional and structural organization of chlorophyll in the developing photosynthetic membranes of Euglena-gracilis-Z .II. Characteristics of the late formation of active photosystem-II reaction centers during first stages of greening. Plant Physiol 67(1):47–53PubMedPubMedCentralCrossRefGoogle Scholar
  36. Dwyer MR, Smillie RM (1970) A light-induced beta-1,3-glucan breakdown associated with differentiation of chloroplasts in Euglena-Gracilis. Biochim Biophys Acta 216(2):392–401PubMedCrossRefGoogle Scholar
  37. Dwyer MR, Smillie RM (1971) Beta-1,3-glucan - a source of carbon and energy for chloroplast development in Euglena-gracilis. Aust J Biol Sci 24(1):15–22PubMedCrossRefGoogle Scholar
  38. Dwyer MR, Smydzuk J, Smillie RM (1970) Synthesis and breakdown of beta-1,3-glucan in Euglena-gracilis during growth and carbon depletion. Aust J Biol Sci 23(5):1005–1013CrossRefGoogle Scholar
  39. Eberly SL, Spremulli GH, Spremulli LL (1986) Light induction of the Euglena chloroplast protein synthesis elongation factors: relative effectiveness of different wavelength ranges. Arch Biochem Biophys 245(2):338–347PubMedCrossRefGoogle Scholar
  40. Egan JM, Carell EF (1972) Studies on chloroplast development and replication in Euglena: III. A study of the site of synthesis of alkaline deoxyribonuclease induced during chloroplast development in Euglena gracilis. Plant Physiol 50(3):391–395PubMedPubMedCentralCrossRefGoogle Scholar
  41. Egan JM, Schiff JA (1974) re-examination of action spectrum for chlorophyll synthesis in Euglena-gracilis. Plant Sci Lett 3(2):101–105CrossRefGoogle Scholar
  42. Egan JM, Dorsky D, Schiff JA (1975) Events surrounding the early development of Euglena chloroplasts: VI. Action spectra for the formation of chlorophyll, lag elimination in chlorophyll synthesis, and appearance of TPN-dependent triose phosphate dehydrogenase and alkaline DNase activities. Plant Physiol 56(2):318–323PubMedPubMedCentralCrossRefGoogle Scholar
  43. Enomoto T, Sulli C, Schwartzbach SD (1997) A soluble chloroplast protease processes the Euglena polyprotein precursor to the light harvesting chlorophyll a/b binding protein of photosystem II. Plant Cell Physiol 38:743–746CrossRefGoogle Scholar
  44. Evans WR (1971) The effect of cycloheximide on membrane transport in Euglena. A comparative study with nigericin. J Biol Chem 246(20):6144–6151PubMedGoogle Scholar
  45. Evers A, Ernst-Fonberg ML (1974) Differential responses of two carboxylases from Euglena to state of chloroplast development. FEBS Lett 46(1):233–235PubMedCrossRefGoogle Scholar
  46. Fayyaz-Chaudhary M, Merrett MJ (1984) Glycollate-pathway enzymes in mitochondria from phototrophic, organotrophic and mixotrophic cells of Euglena. Planta 162(6):518–523PubMedCrossRefGoogle Scholar
  47. Fayyaz-Chaudhary MF, Cannons AC, Merrett MJ (1984) Photoregulation of nadph-glutamate dehydrogenase in regreening cultures of Euglena-gracilis. Plant Sci Lett 34(1–2):89–94CrossRefGoogle Scholar
  48. Fayyaz-Chaudhary M, Javed Q, Merrett MJ (1985) Effect of growth-conditions on nadph-specific glutamate-dehydrogenase activity of Euglena-gracilis. New Phytol 101(3):367–376CrossRefGoogle Scholar
  49. Foley T, Beale SI (1982) Delta-aminolevulinic-acid formation from gamma,delta-dioxovaleric acid in extracts of Euglena-gracilis. Plant Physiol 70(5):1495–1502PubMedPubMedCentralCrossRefGoogle Scholar
  50. Foley T, Dzelzkalns V, Beale SI (1982) Delta-aminolevulinic-acid synthase of Euglena-gracilis - regulation of activity. Plant Physiol 70(1):219–226PubMedPubMedCentralCrossRefGoogle Scholar
  51. Fong F, Schiff JA (1977) Mitochondrial respiration and chloroplast development in Euglena-gracilis var bacillaris. Plant Physiol 59(6):92–92Google Scholar
  52. Fox L, Erion J, Tarnowski J, Spremulli L, Brot N, Weissbach H (1980) Euglena gracilis chloroplast EF-Ts. Evidence that it is a nuclear-coded gene product. J Biol Chem 255(13):6018–6019PubMedGoogle Scholar
  53. Freyssinet G (1976) Influence of culture conditions on the length of the lag period of chlorophyll synthesis in preilluminated dark-grown Euglena. Plant Physiol 57(5):831–835PubMedPubMedCentralCrossRefGoogle Scholar
  54. Freyssinet G (1977) Protein synthesizing system of euglena - synthesis of ribosomal-proteins invivo and their characterization. Physiol Veg 15(3):519–550Google Scholar
  55. Freyssinet G (1978) Determination of the site of synthesis of some Euglena cytoplasmic and chloroplast ribosomal proteins. Exp Cell Res 115(1):207–219PubMedCrossRefGoogle Scholar
  56. Freyssinet G, Schwob C (1976) Relation between paramylum content and the length of the lag period of chlorophyll synthesis during greening of dark-grown Euglena gracilis. Plant Physiol 57(5):824–830PubMedPubMedCentralCrossRefGoogle Scholar
  57. Freyssinet G, Verdier G, Trabuchet G, Heizmann P, Nigon V (1972) Influence of nutritional conditions on light response in etiolated Euglena cells. Physiol Veg 10(3):421–442Google Scholar
  58. Freyssinet G, Harris GC, Nasatir M, Schiff JA (1979) Events surrounding the early development of Euglena chloroplasts: 14. Biosynthesis of cytochrome c-552 in wild type and mutant cells. Plant Physiol 63(5):908–915PubMedPubMedCentralCrossRefGoogle Scholar
  59. Freyssinet G, Eichholz RL, Buetow DE (1984a) Kinetics of accumulation of ribulose-1,5-bisphosphate carboxylase during greening in Euglena gracilis: photoregulation. Plant Physiol 75(3):850–857PubMedPubMedCentralCrossRefGoogle Scholar
  60. Freyssinet G, Freyssinet M, Buetow DE (1984b) Kinetics of accumulation of ribulose-1,5-bisphosphate carboxylase during greening in Euglena gracilis: nutritional regulation. Plant Physiol 75(3):858–861PubMedPubMedCentralCrossRefGoogle Scholar
  61. Garlaschi FM, Garlaschi AM, Lombardi A, Forti G (1974) Effect of ethanol on metabolism of Euglena-gracilis. Plant Sci Lett 2(1):29–39CrossRefGoogle Scholar
  62. Geimer S, Belicova A, Legen J, Slavikova S, Herrmann RG, Krajcovic J (2009) Transcriptome analysis of the Euglena gracilis plastid chromosome. Curr Genet 55(4):425–438PubMedCrossRefGoogle Scholar
  63. Gilbert CW, Buetow DE (1982) Two-dimensional gel analysis of polypeptide appearance in forming thylakoid membranes. Biochem Biophys Res Commun 107(2):649–655PubMedCrossRefGoogle Scholar
  64. Gingrich JC, Hallick RB (1985) The Euglena gracilis chloroplast ribulose-1,5-bisphosphate carboxylase gene. I. Complete DNA sequence and analysis of the nine intervening sequences. J Biol Chem 260(30):16156–16161PubMedGoogle Scholar
  65. Goins DJ, Reynolds RJ, Schiff JA, Barnett WE (1973) A cytoplasmic regulatory mutant of Euglena: constitutivity for the light-inducible chloroplast transfer RNAs. Proc Natl Acad Sci U S A 70(6):1749–1752PubMedPubMedCentralCrossRefGoogle Scholar
  66. Gold JC, Spremulli LL (1985) Euglena gracilis chloroplast initiation factor 2. Identification and initial characterization. J Biol Chem 260(28):14897–14900PubMedGoogle Scholar
  67. Gomez-Silva B, Schiff JA (1985) Synthetic abilities of Euglena chloroplasts in darkness. Biochim Biophys Acta 808(3):448–454PubMedCrossRefGoogle Scholar
  68. Gomez-Silva B, Timko MP, Schiff JA (1985) Chlorophyll biosynthesis from glutamate or 5-aminolevulinate in intact Euglena chloroplasts. Planta 165(1):12–22PubMedCrossRefGoogle Scholar
  69. Gurevitz M, Kratz H, Ohad I (1977) Polypeptides of chloroplastic and cytoplastic origin required for development of photosystem-2 activity, and chlorophyll-protein complexes, in Euglena-gracilis Z chloroplast membranes. Biochim Biophys Acta 461(3):475–488PubMedCrossRefGoogle Scholar
  70. Hallick RB, Greenberg BM, Gruissem W, Hollingsowrth MJ, Karabin GD, Narita JO, Nickoloff JA, Passavant CW, Stiegler GL (1983) Organization and expression of the chloroplast genome of Euglena gracilis. Structue and function of plant genomes. Plenum, New YorkGoogle Scholar
  71. Hallick RB, Hollingsworth MJ, Nickoloff JA (1984) Transfer RNA genes of Euglena gracilis chloroplast DNA: a review. Plant Mol Biol 3(3):169–175PubMedCrossRefGoogle Scholar
  72. Harris RC, Kirk JT (1969) Control of chloroplast formation in Euglena gracilis. Antagonism between carbon and nitrogen sources. Biochem J 113(1):195–205PubMedPubMedCentralCrossRefGoogle Scholar
  73. Hecker LI, Egan J, Reynolds RJ, Nix CE, Schiff JA, Barnett WE (1974) The sites of transcription and translation for Euglena chloroplastic aminoacyl-tRNA synthetases. Proc Natl Acad Sci U S A 71(5):1910–1914PubMedPubMedCentralCrossRefGoogle Scholar
  74. Heizmann P, Trabuchet G, Verdier G, Freyssinet G, Nigon V (1972) Influence of illumination on polysome formation in dark-grown Euglena gracilis cultures. Biochim Biophys Acta 277(1):149–160PubMedCrossRefGoogle Scholar
  75. Heizmann PH, Salvador GF, Nigon V (1976) Occurrence of plastidial rRNAs and plastidial structures in bleached mutants of Euglena gracilis. Exp Cell Res 99(2):253–260PubMedCrossRefGoogle Scholar
  76. Heizmann P, Doly J, Hussein Y, Nicolas P, Nigon V, Bernardi G (1981) The chloroplast genome of bleached mutants of Euglena gracilis. Biochim Biophys Acta 653(3):412–415PubMedCrossRefGoogle Scholar
  77. Heizmann P, Hussein Y, Nicolas P, Nigon V (1982) Modifications of chloroplast DNA during streptomycin induced mutagenesis in Euglena gracilis. Curr Genet 5(1):9–15PubMedCrossRefGoogle Scholar
  78. Hollingsworth MJ, Johanningmeier U, Karabin GD, Stiegler GL, Hallick RB (1984) Detection of multiple, unspliced precursor mRNA transcripts for the Mr 32,000 thylakoid membrane protein from Euglena gracilis chloroplasts. Nucleic Acids Res 12(4):2001–2017PubMedPubMedCentralCrossRefGoogle Scholar
  79. Holowinsky AW, Schiff JA (1970) Events surrounding the early development of Euglena chloroplasts. I. Induction by preillumination. Plant Physiol 45(3):339–347PubMedPubMedCentralCrossRefGoogle Scholar
  80. Horrum MA, Schwartzbach SD (1980a) Absence of photo and nutritional regulation of 2 glycolate pathway enzymes in Euglena. Plant Sci Lett 20(2):133–139CrossRefGoogle Scholar
  81. Horrum MA, Schwartzbach SD (1980b) Nutritional regulation of organelle biogenesis in Euglena - repression of chlorophyll and Nadp-glyceraldehyde-3-phosphate dehydrogenase synthesis. Plant Physiol 65(2):382–386PubMedPubMedCentralCrossRefGoogle Scholar
  82. Horrum MA, Schwartzbach SD (1980c) Nutritional regulation of organelle biogenesis in Euglena: photo- and metabolite induction of mitochondria. Planta 149(4):376–383PubMedCrossRefGoogle Scholar
  83. Horrum MA, Schwartzbach SD (1981) Nutritional regulation of organelle biogenesis in Euglena - induction of microbodies. Plant Physiol 68(2):430–434PubMedPubMedCentralCrossRefGoogle Scholar
  84. Horrum MA, Schwartzbach SD (1982) Induction of fumarase in resting Euglena. Biochim Biophys Acta 714(3):407–414PubMedCrossRefGoogle Scholar
  85. Houlne G, Schantz R (1987) Molecular analysis of the transcripts encoding the light-harvesting chlorophyll a/b protein in Euglena gracilis: unusual size of the mRNA. Curr Genet 12(8):611–616PubMedCrossRefGoogle Scholar
  86. Houlne G, Schantz R (1988) Characterization of cDNA sequences for LHCI apoproteins in Euglena gracilis: the mRNA encodes a large precursor containing several consecutive divergent polypeptides. Mol Gen Genet 213(2–3):479–486PubMedCrossRefGoogle Scholar
  87. Hovenkamp-Obbema R, Stegwee D (1974) Effect of chloramphenicol on development of proplastids in Euglena-gracilis .1. Synthesis of ribulosediphosphate carboxylase, Nadp-linked glyceraldehyde-3-phosphate dehydrogenase and aminolevulinate dehydratase. Z Pflanzenphysiol 73(5):430–438CrossRefGoogle Scholar
  88. Hovenkamp-Obbema R, Moorman A, Stegwee D (1974) Aminolevulinate dehydratase in greening cells of Euglena-gracilis. Z Pflanzenphysiol 72(4):277–286CrossRefGoogle Scholar
  89. Hussein Y, Heizmann P, Nicolas P, Nigon V (1982) Quantitative estimations of chloroplast DNA in bleached mutants of Euglena gracilis. Curr Genet 6(2):111–117PubMedCrossRefGoogle Scholar
  90. James L, Schwartzbach SD (1982) Differential regulation of phosphoglycolate and phosphoglycerate phosphatases in Euglena. Plant Sci Lett 27(2):223–232CrossRefGoogle Scholar
  91. Javed Q, Merrett MJ (1987) Mobilization of Nadph-glutamate dehydrogenase messenger-RNA in regreening cultures of Euglena-gracilis. Plant Sci 49(1):31–36CrossRefGoogle Scholar
  92. Johanningmeier U, Hallick RB (1987) The psbA gene of DCMU-resistant Euglena gracilis has an amino acid substitution at serine codon 265. Curr Genet 12(6):465–470PubMedCrossRefGoogle Scholar
  93. Karlan AW, Russell GK (1976) Aldolase levels in wild-type and mutant Euglena-gracilis. J Protozool 23(1):176–179CrossRefGoogle Scholar
  94. Karn RC, Hudock GA (1973) Photorepressible isoenzyme of malic enzyme in Euglena-gracilis strain-Z. J Protozool 20(2):316–320PubMedCrossRefGoogle Scholar
  95. Keller M, Chan RL, Tessier LH, Weil JH, Imbault P (1991) Post-transcriptional regulation by light of the biosynthesis of Euglena ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit. Plant Mol Biol 17(1):73–82PubMedCrossRefGoogle Scholar
  96. Kemper ES (1982) Stimulation and inhibition of the metabolism and growth of Euglena gracilis. In: Buetow DE (ed) The biology of Euglena, Physiology, vol 3. Academic Press, New York, pp 197–252Google Scholar
  97. Kishore R, Schwartzbach SD (1992a) Photo and nutritional regulation of the light-harvesting chlorophyll a/b-binding protein of photosystem II mRNA levels in Euglena. Plant Physiol 98(3):808–812PubMedPubMedCentralCrossRefGoogle Scholar
  98. Kishore R, Schwartzbach SD (1992b) Translational control of the synthesis of the Euglena light harvesting chlorophyll a/b binding protein of photosystem II. Plant Sci 85:79–89CrossRefGoogle Scholar
  99. Kishore R, Muchhal U, Schwartzbach SD (1993) The presequence of Euglena LHCPII, a cytoplasmically synthesized chloroplast protein, contains a functional endoplasmic reticulum targeting domain. Proc Natl Acad Sci U S A 90:11845–11849PubMedPubMedCentralCrossRefGoogle Scholar
  100. Klein S, Schiff JA, Holowinsky AW (1972) Events surrounding the early development of Euglena chloroplasts. II. Normal development of fine structure and the consequences of preillumination. Dev Biol 28(1):253–273PubMedCrossRefGoogle Scholar
  101. Koziol AG, Durnford DG (2008) Euglena light-harvesting complexes are encoded by multifarious polyprotein mRNAs that evolve in concert. Mol Biol Evol 25(1):92–100PubMedCrossRefGoogle Scholar
  102. Kraus BL, Spremulli LL (1986) Chloroplast initiation factor 3 from Euglena gracilis. Identification and initial characterization. J Biol Chem 261(11):4781–4784PubMedGoogle Scholar
  103. Kraus BL, Spremulli LL (1988) Evidence for the nuclear location of the genes for chloroplast IF-2 and IF-3 in Euglena. Plant Physiol 88(4):993–995PubMedPubMedCentralCrossRefGoogle Scholar
  104. Krauspe R, Scheer A, Schaper S, Bohley P (1986) Proteolysis in Euglena gracilis: II. Soluble and particle-bound acidic proteinase activities of the cysteine and aspartic types during growth and chloroplast development. Planta 167(4):482–490PubMedCrossRefGoogle Scholar
  105. Krauspe R, Lerbs S, Parthier B, Wollgiehn R (1987) Light induction of translatable messenger-RNAs for chloroplastic leucyl-transfer-RNA and valyl-transfer-RNA synthetases of Euglena-gracilis. J Plant Physiol 130(4–5):327–342CrossRefGoogle Scholar
  106. Laval-Martin D, Farineau J, Pineau B, Calvayrac R (1981) Evolution of enzymes involved in carbon metabolism (phosphoenolpyruvate and ribulose-bisphosphate carboxylases, phosphoenolpyruvate carboxykinase) during the light-induced greening of Euglena gracilis strains Z and ZR. Planta 151(2):157–167PubMedCrossRefGoogle Scholar
  107. Lin Q, Ma L, Burkhart W, Spremulli LL (1994) Isolation and characterization of cDNA clones for chloroplast translational initiation factor-3 from Euglena gracilis. J Biol Chem 269(13):9436–9444PubMedGoogle Scholar
  108. Lord JM, Merrett MJ (1971) The intracellular localization of glycollate oxidoreductase in Euglena gracilis. Biochem J 124(2):275–281PubMedPubMedCentralCrossRefGoogle Scholar
  109. Madhusudhan R, Ishikawa T, Sawa Y, Shigeoka S, Shibata H (2003) Post-transcriptional regulation of ascorbate peroxidase during light adaptation of Euglena gracilis. Plant Sci 165(1):233–238CrossRefGoogle Scholar
  110. Mayer SM, Beale SI (1990) Light regulation of delta-aminolevulinic acid biosynthetic enzymes and tRNA in Euglena gracilis. Plant Physiol 94(3):1365–1375PubMedPubMedCentralCrossRefGoogle Scholar
  111. Mayer SM, Beale SI (1991) delta-aminolevulinic acid biosynthesis from glutamatein Euglena gracilis: photocontrol of enzyme levels in a chlorophyll-free mutant. Plant Physiol 97(3):1094–1102PubMedPubMedCentralCrossRefGoogle Scholar
  112. Mayer SM, Beale SI, Weinstein JD (1987) Enzymatic conversion of glutamate to delta-aminolevulinic acid in soluble extracts of Euglena gracilis. J Biol Chem 262(26):12541–12549PubMedGoogle Scholar
  113. McCarthy SA, Schwartzbach SD (1984) Absence of photoregulation of abundant messenger-RNA levels in Euglena. Plant Sci Lett 35(1):61–66CrossRefGoogle Scholar
  114. McCarthy SA, James L, Schwartzbach SD (1982) Photo and nutritional regulation of chloroplast valy-transfer RNA-synthetase in Euglena. Arch Microbiol 133(2):149–154CrossRefGoogle Scholar
  115. Miller ME, Jurgenson JE, Reardon EM, Price CA (1983) Plastid translation in organello and in vitro during light-induced development in Euglena. J Biol Chem 258(23):14478–14484PubMedGoogle Scholar
  116. Miyatake K, Ito T, Kitaoka S (1984) Subcellular location and some properties of phosphoenolpyruvate carboxykinase (Pepck) in Euglena-gracilis. Agric Biol Chem Tokyo 48(8):2139–2141Google Scholar
  117. Monroy AF, Schwartzbach SD (1983) Photocontrol of the polypeptide composition of Euglena: analysis by two-dimensional gel electrophoresis. Planta 158(3):249–258PubMedCrossRefGoogle Scholar
  118. Monroy AF, Schwartzbach SD (1984) Catabolite repression of chloroplast development in Euglena. Proc Natl Acad Sci U S A 81(9):2786–2790PubMedPubMedCentralCrossRefGoogle Scholar
  119. Monroy AF, Schwartzbach SD (1985) Influence of photosynthesis and chlorophyll synthesis on polypeptide accumulation in greening Euglena. Plant Physiol 77(4):811–816PubMedPubMedCentralCrossRefGoogle Scholar
  120. Monroy AF, Gomez-Silva B, Schwartzbach SD, Schiff JA (1986) Photocontrol of chloroplast and mitochondrial polypeptide levels in Euglena. Plant Physiol 80:618–622PubMedPubMedCentralCrossRefGoogle Scholar
  121. Monroy AF, Mccarthy SA, Schwartzbach SD (1987) Evidence for translational regulation of chloroplast and mitochondrial biogenesis in Euglena. Plant Sci 51(1):61–76CrossRefGoogle Scholar
  122. Montandon PE, Stutz E (1983) Nucleotide sequence of a Euglena gracilis chloroplast genome region coding for the elongation factor Tu; evidence for a spliced mRNA. Nucleic Acids Res 11(17):5877–5892PubMedPubMedCentralCrossRefGoogle Scholar
  123. Muchhal US, Schwartzbach SD (1992) Characterization of a Euglena gene encoding a polyprotein precursor to the light-harvesting chlorophyll a/b-binding protein of photosystem II. Plant Mol Biol 18(2):287–299PubMedCrossRefGoogle Scholar
  124. Nakazawa M, Minami T, Teramura K, Kumamoto S, Hanato S, Takenaka S, Ueda M, Inui H, Nakano Y, Miyatake K (2005) Molecular characterization of a bifunctional glyoxylate cycle enzyme, malate synthase/isocitrate lyase, in Euglena gracilis. Comp Biochem Physiol 141(4):445–452CrossRefGoogle Scholar
  125. Nakazawa M, Nishimura M, Inoue K, Ueda M, Inui H, Nakano Y, Miyatake K (2011) Characterization of a bifunctional glyoxylate cycle enzyme, malate synthase/isocitrate lyase, of Euglena gracilis. J Eukaryot Microbiol 58(2):128–133PubMedCrossRefGoogle Scholar
  126. Neumann D, Parthier B (1973) Effects of nalidixic acid, chloramphenicol, cycloheximide, and anisomycin on structure and development of plastids and mitochondria in greening Euglena gracilis. Exp Cell Res 81(2):255–268PubMedCrossRefGoogle Scholar
  127. Nover L (1976) Density labeling of chloroplast-specific leucyl-transfer-RNA synthetase in greening cells of Euglena-gracilis. Plant Sci Lett 7(6):403–407CrossRefGoogle Scholar
  128. Ogren WL (1984) Photorespiration - pathways, regulation, and modification. Annu Rev Plant Phys 35:415–442CrossRefGoogle Scholar
  129. Ono K, Miyatake K, Inui H, Kitaoka S, Nakano Y (1994) Induction of glyoxylate cycle-key enzymes, malate synthase, and isocitrate lyase in ethanol-grown Euglena gracilis. Biosci Biotech Bioch 58(3):582–583CrossRefGoogle Scholar
  130. Ono K, Kawanaka Y, Izumi Y, Inui H, Miyatake K, Kitaoka S, Nakano Y (1995) Mitochondrial alcohol dehydrogenase from ethanol-grown Euglena gracilis. J Biochem 117(6):1178–1182PubMedCrossRefGoogle Scholar
  131. Ono K, Kondo M, Osafune T, Miyatake K, Inui H, Kitaoka S, Nishimura M, Nakano Y (2003) Presence of glyoxylate cycle enzymes in the mitochondria of Euglena gracilis. J Eukaryot Microbiol 50(2):92–96PubMedCrossRefGoogle Scholar
  132. Ortiz W, Stutz E (1980) Synthesis of polypeptides of the chlorophyll-protein complexes in isolated-chloroplasts of Euglena-gracilis. FEBS Lett 116(2):298–302CrossRefGoogle Scholar
  133. Osafune T, Schiff JA (1983) W10BSmL, a mutant of Euglena gracilis var. bacillaris lacking plastids. Exp Cell Res 148(2):530–535PubMedCrossRefGoogle Scholar
  134. Osafune T, Klein S, Schiff JA (1980) Events surrounding the early development of Euglena chloroplasts. Structure of the developing proplastid in the first hours of illumination from serial sections of wild-type cells. J Ultrastruct Res 73(1):77–90PubMedCrossRefGoogle Scholar
  135. Osafune T, Schiff JA, Hase E (1991a) Stage-dependent localization of LHCP II apoprotein in the Golgi of synchronized cells of Euglena gracilis by immunogold electron microscopy. Exp Cell Res 193(2):320–330PubMedCrossRefGoogle Scholar
  136. Osafune T, Sumida S, Schiff JA, Hase E (1991b) Immunolocalization of LHCPII apoprotein in the Golgi during light-induced chloroplast development in non-dividing Euglena cells. J Electron Microsc 40:41–47Google Scholar
  137. Parker JE, Javed Q, Merrett MJ (1985) Glutamate dehydrogenase (NADP-dependent) mRNA in relation to enzyme synthesis in Euglena gracilis. Evidence for post-transcriptional control. Eur J Biochem 153(3):573–578PubMedCrossRefGoogle Scholar
  138. Parthier B, Krauspe R (1974) Chloroplast and cytoplasmic transfer RNA of Euglena-gracilis – transfer RNA-Leu of blue-green-algae as a substitute for chloroplast transfer RNA-leu. Biochem Physiol Pfl 165(1–2):1–17CrossRefGoogle Scholar
  139. Parthier B, Krauspe R, Samtleben S (1972) Light-stimulated synthesis of aminoacyl-tRNA synthetases in greening Euglena gracilis. Biochim Biophys Acta 277(2):335–341PubMedCrossRefGoogle Scholar
  140. Passavant CW, Stiegler GL, Hallick RB (1983) Location of the single gene for elongation factor Tu on the Euglena gracilis chloroplast chromosome. J Biol Chem 258(2):693–695PubMedGoogle Scholar
  141. Peak MJ, Peak JG, Ting IP (1972) Light-induced reduction in specific activity of malate enzyme in Euglena-gracilis-Z. Biochem Biophys Res Commun 48(5):1074–1078PubMedCrossRefGoogle Scholar
  142. Pineau B (1982) Biosynthesis of ribulose-1.5-bisphosphate carboxylase in greening cells of Euglena gracilis: the accumulation of ribulose-1.5-bisphosphate carboxylase and of its subunits. Planta 156(2):117–128PubMedCrossRefGoogle Scholar
  143. Pineau B, Dubertret G, Schantz R (1985) Functional and structural organization of chlorophyll in the developing photosynthetic membranes of Euglena-gracilis Z V-separation and characterization of pigment-protein complexes of the differentiated thylakoids. Photosynth Res 6(2):159–174PubMedCrossRefGoogle Scholar
  144. Ponsgen-Schmidt E, Schneider T, Hammer U, Betz A (1988) Comparison of phosphoenolpyruvate-carboxykinase from autotrophically and heterotrophically grown Euglena and its role during dark anaerobiosis. Plant Physiol 86(2):457–462PubMedPubMedCentralCrossRefGoogle Scholar
  145. Rabinowitz H, Reisfeld A, Sagher D, Edelman M (1975) Ribulose diphosphate carboxylase from autotrophic Euglena gracilis. Plant Physiol 56(3):345–350PubMedPubMedCentralCrossRefGoogle Scholar
  146. Ravel-Chapuis P, Nigon V (1981) Analysis of the production of delta-aminolevulinic-acid and chlorophyll in Euglena-gracilis Z. Plant Sci Lett 21(4):333–343CrossRefGoogle Scholar
  147. Rawson JRY, Boerma C (1976a) Influence of growth-conditions upon number of chloroplast DNA-molecules in Euglena-gracilis. Proc Natl Acad Sci U S A 73(7):2401–2404PubMedPubMedCentralCrossRefGoogle Scholar
  148. Rawson JRY, Boerma CL (1976b) Measurement of fraction of chloroplast DNA transcribed during chloroplast development in Euglena-gracilis. Biochemistry 15(3):588–592PubMedCrossRefGoogle Scholar
  149. Rawson JRY, Boerma CL (1979) Hybridization of EcoRI chloroplast DNA fragments of Euglena to pulse labeled RNA from different stages of chloroplast development. Biochem Biophys Res Commun 89(2):743–749PubMedCrossRefGoogle Scholar
  150. Rawson JRY, Boerma CL, Andrews WH, Wilkerson CG (1981) Complexity and abundance of ribonucleic-acid transcribed from restriction endonuclease fragments of Euglena chloroplast deoxyribonucleic-acid during chloroplast development. Biochemistry 20(9):2639–2644PubMedCrossRefGoogle Scholar
  151. Reger BJ, Fairfield SA, Epler JL, Barnett WE (1970) Identification and origin of some chloroplast aminoacyl-tRNA synthetases and tRNAs. Proc Natl Acad Sci U S A 67(3):1207–1213PubMedPubMedCentralCrossRefGoogle Scholar
  152. Richard F, Nigon V (1973) Synthesis of delta-aminolevulinic acid and chlorophyll during illumination of etiolated Euglena gracilis. Biochim Biophys Acta 313(1):130–149PubMedCrossRefGoogle Scholar
  153. Rikin A, Schwartzbach SD (1988) Extremely large and slowly processed precursors to the Euglena light harvesting chlorophyll a/b binding proteins of photosystem II. Proc Natl Acad Sci U S A 85:5117–5121PubMedPubMedCentralCrossRefGoogle Scholar
  154. Rikin A, Schwartzbach S (1989a) Translational regulation of the synthesis of Euglena fumarase by light and ethanol. Plant Physiol 90:63–69PubMedPubMedCentralCrossRefGoogle Scholar
  155. Rikin A, Schwartzbach SD (1989b) Regulation by light and ethanol of the synthesis of the light harvesting chlorophyll a/b binding protein of photosystem II in Euglena. Planta 178:76–83PubMedCrossRefGoogle Scholar
  156. Rosenberg A, Pecker M (1964) Lipid alterations in Euglena gracilis cells during light-induced greening. Biochemistry 3:254–258PubMedCrossRefGoogle Scholar
  157. Russell GK, Draffan AG, Schmidt GW, Lyman H (1978) Light-induced enzyme formation in a chlorophyll-less mutant of Euglena-gracilis. Plant Physiol 62(5):678–682PubMedPubMedCentralCrossRefGoogle Scholar
  158. Saidha T, Stern AI, Lee DH, Schiff JA (1985) Localization of a sulphate-activating system within Euglena mitochondria. Biochem J 232(2):357–365PubMedPubMedCentralCrossRefGoogle Scholar
  159. Salvador GF (1978) Delta-aminolevulinic-acid synthesis from gamma-delta-dioxovaleric acid by acellular preparations of Euglena-gracilis. Plant Sci Lett 13(4):351–355CrossRefGoogle Scholar
  160. Salvador GF, Beney G, Nigon V (1976) Control of delta-aminolevulinic-acid synthesis during greening of dark-grown Euglena-gracilis. Plant Sci Lett 6(3):197–202CrossRefGoogle Scholar
  161. Schantz R, Schantz ML, Duranton H (1975) Changes in amino-acid and peptide composition of Euglena-gracilis cells during chloroplast development. Plant Sci Lett 5(5):313–324CrossRefGoogle Scholar
  162. Schiff JA (1963) Oxygen exchange by Euglena cells undergoing chloroplast development. Carnegie Inst Wash Yearbook 62:375–378Google Scholar
  163. Schiff JA, Zeldin MH, Rubman J (1967) Chlorophyll formation and photosynthetic competence in euglena during light-induced chloroplast development in the presence of 3, (3,4-dichlorophenyl) 1,1-dimethyl urea (DCMU). Plant Physiol 42(12):1716–1725PubMedPubMedCentralCrossRefGoogle Scholar
  164. Schiff JA, Lyman H, Russel GK (1971) Isolation of mutants from Euglena gracilis. Methods Enzymol 23:143–162CrossRefGoogle Scholar
  165. Schiff JA, Lyman H, Russel GK (1980) Isolation of mutants from Euglena gracilis: an addendum. Methods Enzymol 69:23–29CrossRefGoogle Scholar
  166. Schiff JA, Schwartzbach SD, Osafune T, Hase E (1991a) Photocontrol and processing of Lhcp-II apoprotein in Euglena - possible role of Golgi and other cytoplasmic sites. J Photoch Photobio B Biol 11(2):219–236CrossRefGoogle Scholar
  167. Schiff JA, Schwartzbach SD, Osafune T, Hase E (1991b) Photocontrol and processing of LHCPII apoprotein in Euglena: possible role of Golgi and other cytoplasmic sites. J Photchem Photobiol B Biol 11:219–236CrossRefGoogle Scholar
  168. Schimpf C, Govindarajan AG, Parthier BP (1982) Influence of preillumination (potentiation) and carbon substrates on plastid aminoacyl-tRNA synthetases in greening Euglena cells. Biochem Physiol Pfl 177(9):777–788CrossRefGoogle Scholar
  169. Schmidt GW, Lyman H (1974) Photocontrol of chloroplast enzyme synthesis in mutant and wild type Euglena gracilis. In Proceedings of the third international congress. Photosynthesis. Elsevier, Amsterdam, New YorkGoogle Scholar
  170. Schuber F, Aleksijevic A, Blee E (1981) Comparative role of polyamines in division and plastid differentiation of Euglena-gracilis. Biochim Biophys Acta 675(2):178–187PubMedCrossRefGoogle Scholar
  171. Schwartzbach SD, Frreyssinet G, Schiff JA (1974) The chloroplast and cytoplasmic ribosomes of Euglena .1 stability of chloroplast ribosomes prepared by an improved procedure. Plant Physiol 53:533–542PubMedPubMedCentralCrossRefGoogle Scholar
  172. Schwartzbach SD, Schiff JA, Goldstein NH (1975) Events surrounding the early development of euglena chloroplasts: v. Control of paramylum degradation. Plant Physiol 56(2):313–317PubMedPubMedCentralCrossRefGoogle Scholar
  173. Schwartzbach SD, Hecker LI, Barnett WE (1976a) Transcriptional origin of Euglena chloroplast tRNAs. Proc Natl Acad Sci U S A 73:1984–1988PubMedPubMedCentralCrossRefGoogle Scholar
  174. Schwartzbach SD, Schiff JA, Klein S (1976b) Biosynthetic events required for lag elimination in chlorophyll synthesis in Euglena. Planta 131(1):1–9PubMedCrossRefGoogle Scholar
  175. Schwelitz FD, Cisneros PL, Jagielo JA (1978a) Effect of glucose on biochemical and ultrastructural characteristics of developing Euglena chloroplasts. J Protozool 25(3):398–403PubMedCrossRefGoogle Scholar
  176. Schwelitz FD, Cisneros PL, Jagielo JA (1978b) Effect of glucose on developing Euglena plastids. J Cell Biol 79(2):A313–A313Google Scholar
  177. Schwelitz FD, Cisneros PL, Jagielo JA, Comer JL, Butterfied KA (1978c) Relationship of fixed carbon and nitrogen-sources to greening process in Euglena-gracilis strain Z. J Protozool 25(2):257–261CrossRefGoogle Scholar
  178. Shashidhara LS, Smith AG (1991) Expression and subcellular location of the tetrapyrrole synthesis enzyme porphobilinogen deaminase in light-grown Euglena gracilis and three nonchlorophyllous cell lines. Proc Natl Acad Sci U S A 88(1):63–67PubMedPubMedCentralCrossRefGoogle Scholar
  179. Small GD, Sturgen RS (1976) Purification and properties of a light-inducible nuclease from Euglena gracilis. Nucleic Acids Res 3(5):1277–1293PubMedPubMedCentralCrossRefGoogle Scholar
  180. Spano AJ, Schiff JA (1987) Purification, properties, and cellular localization of Euglena ferredoxin-NADP reductase. Biochim Biophys Acta 894(3):484–498PubMedCrossRefGoogle Scholar
  181. Spano AJ, Ghaus H, Schiff JA (1987) Chlorophyll-protein complexes and other thylakoid components at the low intensity threshold in Euglena chloroplast development. Plant Cell Physiol 28(6):1101–1108Google Scholar
  182. Spremulli LL (1982) Chloroplast elongation factor Tu: evidence that it is the product of a chloroplast gene in Euglena. Arch Biochem Biophys 214(2):734–741PubMedCrossRefGoogle Scholar
  183. Srinivas U, Lyman H (1980) Photomorphogenic regulation of chloroplast replication in Euglena - enhanced loss of chloroplast DNA in red-light. Plant Physiol 66(2):295–301PubMedPubMedCentralCrossRefGoogle Scholar
  184. Stern AI, Epstein HT, Schiff JA (1964a) Studies of chloroplast development in Euglena. VI Light intensity as a controlling factor in development. Plant Physiol 39(2):226–231PubMedPubMedCentralCrossRefGoogle Scholar
  185. Stern AI, Schiff JA, Epstein HT (1964b) Studies of chloroplast development in Euglena. V. pigment biosynthesis, photosynthetic oxygen evolution and carbon dioxide fixation during chloroplast development. Plant Physiol 39(2):220–226PubMedPubMedCentralCrossRefGoogle Scholar
  186. Stevenson JK, Hallick RB (1994) The psaA operon pre-mRNA of the Euglena gracilis chloroplast is processed into photosystem I and II mRNAs that accumulate differentially depending on the conditions of cell growth. Plant J 5(2):247–260PubMedCrossRefGoogle Scholar
  187. Sulli C, Schwartzbach SD (1995) The polyprotein precursor to the Euglena light harvesting chlorophyll a/b-binding protein is transported to the Golgi apparatus prior to chloroplast import and polyprotein processing. J Biol Chem 270:13084–13090PubMedCrossRefGoogle Scholar
  188. Sumida S, Ehara T, Osafune T, Hase E (1987) Ammonia-induced and light-induced degradation of paramylum in Euglena-gracilis. Plant Cell Physiol 28(8):1587–1592Google Scholar
  189. Timko MP, Schiff JA (1983) Membrane-bound coupling factor atpase activity during light-induced chloroplast development in Euglena-gracilis. Physiol Plantarum 58(1):41–46CrossRefGoogle Scholar
  190. Verdier G (1975) Synthesis and translation site of light-induced mRNAs in etiolated Euglena gracilis. Biochim Biophys Acta 407(1):91–98PubMedCrossRefGoogle Scholar
  191. Verdier G (1979a) Poly(adenylic acid)-containing RNA of Euglena gracilis during chloroplast development. 2. Transcriptional origin of the different RNA. Eur J Biochem 93(3):581–586PubMedCrossRefGoogle Scholar
  192. Verdier G (1979b) Poly(adenylic acid)-containing RNA of Euglena gracilis during chloroplast development. I. Analysis of their complexity by hybridization to complementary DNA. Eur J Biochem 93(3):573–580PubMedCrossRefGoogle Scholar
  193. Verdier G, Trabuchet G, Heizmann P, Nigon V (1973) Effect of illumination on RNA synthesis and poly(adenylic acid) sequences in cultures of etiolated Euglena gracilis. Biochim Biophys Acta 312(3):528–539PubMedCrossRefGoogle Scholar
  194. Vesteg M, Vacula R, Burey S, Loffelhardt W, Drahovska H, Martin W, Krajcovic J (2009) Expression of nucleus-encoded genes for chloroplast proteins in the flagellate Euglena gracilis. J Eukaryot Microbiol 56(2):159–166PubMedCrossRefGoogle Scholar
  195. Weinstein JD, Beale SI (1983) Separate physiological roles and subcellular compartments for two tetrapyrrole biosynthetic pathways in Euglena gracilis. J Biol Chem 258(11):6799–6807PubMedGoogle Scholar
  196. Weiss C, Houlne G, Schantz ML, Schantz R (1988) Photoregulation of the synthesis of chloroplast membrane-proteins in Euglena-gracilis. J Plant Physiol 133(5):521–528CrossRefGoogle Scholar
  197. Weiss C, Houlne G, Schantz R (1992) Photocontrol of thylakoid protein synthesis in Euglena: differential post-transcriptional regulation depending on nutritional conditions. Planta 188(4):468–477PubMedCrossRefGoogle Scholar
  198. Woodward J, Merrett MJ (1975) Induction potential for glyoxylate cycle enzymes during the cell cycle of Euglena gracilis. Eur J Biochem 55(3):555–559PubMedCrossRefGoogle Scholar
  199. Yi LSH, Gilbert CW, Buetow DE (1985) Temporal appearance of chlorophyll-protein complexes and the N,N1-dicyclohexylcarbodiimide-binding coupling factoro-subunit-III in forming thylakoid membranes of Euglena-gracilis. J Plant Physiol 118(1):7–21PubMedCrossRefGoogle Scholar
  200. Yokota A, Kitaoka S (1979) Metabolism of glycolate in Euglena gracilis. 3. Occurrence of glycolate dehydrogenase in mitochondria and microsomes in streptomycin-bleached mutant of Euglena, Gracilis Z. Agric Biol Chem Tokyo 43(4):855–857Google Scholar
  201. Yokota A, Kitaoka S (1981) Metabolism of glycolate in Euglena-gracilis. 5. Occurrence and subcellular-distribution of enzymes involved in the glycolate pathway and their physiological-function in a bleached mutant of Euglena-gracilis Z. Agric Biol Chem Tokyo 45(1):15–22Google Scholar
  202. Yokota A, Nakano Y, Kitaoka S (1978) Different effects of some growing conditions on glycolate dehydrogenase in mitochondria and microbodies in Euglena gracilis. Agric Biol Chem 42:115–120Google Scholar
  203. Yokota A, Haga S, Kitaoka S (1985a) Purification and some properties of glyoxylate reductase (NADP+) and its functional location in mitochondria in Euglena gracilis z. Biochem J 227(1):211–216PubMedPubMedCentralCrossRefGoogle Scholar
  204. Yokota A, Suehiro S, Kitaoka S (1985b) Purification and some properties of mitochondrial glutamate:glyoxylate aminotransferase and mechanism of its involvement in glycolate pathway in Euglena gracilis z. Arch Biochem Biophys 242(2):507–514PubMedCrossRefGoogle Scholar
  205. Zeldin MH, Skea W, Matteson D (1973) Organelle formation in the presence of a protease inhibitor. Biochem Biophys Res Commun 52(2):544–549PubMedCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of MemphisMemphisUSA

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