Skip to main content
SpringerLink
Log in
Book cover

Plastid Biology pp 559–585Cite as

Hydrogen and Biofuel Production in the Chloroplast

  • Chapter
  • First Online:

  • 1552 Accesses

Part of the book series: Advances in Plant Biology ((AIPB,volume 5))

Abstract

Plastids are the compartments in which oxygenic photosynthesis of higher plants and eukaryotic microalgae converts the energy of sunlight into chemical energy. The latter is used by green cells to generate the whole palette of organic molecules needed to build a cell. Mankind has made use of the green powerhouses from the beginning of its existence on, but in the last decades, products other than food or fire wood have gained importance. Facing the deprivation of fossil fuels and climate changes due to anthropologically caused greenhouse effects, we want to use photosynthetically converted light energy as an energy source to generate renewable energy carriers. Above all, the synthesis of biodiesel made from plant or algal lipids is a promising strategy. As the cultivation of microalgae does not compete with food production, research focuses on understanding and engineering lipid biosynthesis in these unicellular organisms. Additionally, in contrast to higher plants, some green algae are capable of using the process of photosynthesis for the generation of another biofuel: molecular hydrogen. In this chapter, the pathways resulting in the generation of hydrogen and lipids in the plastid are reviewed. Additionally, proven and anticipated targets of biotechnological optimization are highlighted.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

ACCase:

Acetyl-CoA carboxylase

ACP:

Acyl carrier protein

CoA:

Coenzyme A

DAG:

Diacylglycerol

DGAT:

Diacylglycerol acyltransferase

DGDG:

Digalactosyldiacylglycerol

DGTS:

Diacylglycerol-N,N,N-trimethylhomoserine

ER:

Endoplasmic reticulum

FAS:

Fatty acid synthase

FAT:

Fatty acyl-ACP thioesterase

G3P:

Glycerol-3-phosphate

GPAT:

Glycerol-3-phosphate acyltransferase

LACS:

Long chain acyl-CoA synthetase

LPA:

Lysophosphatidic acid

LPAT:

Lysophosphatidic acid acyltransferase

MGDG:

Monogalactosyldiacylglycerol

MLDP:

Major lipid droplet protein

PA:

Phosphatidic acid

PAP:

Phosphatidic acid phosphatase

PDAT:

Phospholipid:diacylglycerol acyltransferase

PtdEtn:

Phosphatidylethanolamine

PtdGro:

Phosphatidylglycerol

PtdIns:

Phosphatidylinositol

SQDG:

Sulfoquinovosyldiacylglycerol

TAG:

Triacylglycerol

References

  1. Adachi T, Takase H, Tomizawa KI (2007) Introduction of a 50 kbp DNA fragment into the plastid genome. Biosci Biotechnol Biochem 71:2266–2273

    PubMed  CAS  Google Scholar 

  2. Antal TK, Krendeleva TE, Laurinavichene TV, Makarova VV, Ghirardi ML, Rubin AB, Tsygankov AA, Seibert M (2003) The dependence of algal H2 production on Photosystem II and O2 consumption activities in sulfur-deprived Chlamydomonas reinhardtii cells. Biochim Biophys Acta 1607:153–160

    PubMed  CAS  Google Scholar 

  3. Antonkine ML et al (2007) Chemical rescue of a site-modified ligand to a [4Fe-4S] cluster in PsaC, a bacterial-like dicluster ferredoxin bound to Photosystem I. Biochim Biophys Acta 1767:712–724

    PubMed  CAS  Google Scholar 

  4. Arnon DI, Losada M, Nozaki M, Tagawa K (1961) Photoproduction of hydrogen, photofixation of nitrogen and a unified concept of photosynthesis. Nature 190:601–606

    PubMed  CAS  Google Scholar 

  5. 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 281:9909–9918

    PubMed  CAS  Google Scholar 

  6. Atteia A, van Lis R, Tielens AG, Martin WF (2013) Anaerobic energy metabolism in unicellular photosynthetic eukaryotes. Biochim Biophys Acta 1827:210–223

    Google Scholar 

  7. Baud S, Santos-Mendoza M, To A, Harscoet E, Lepiniec L, Dubreucq B (2007) WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J 50:825–838

    PubMed  CAS  Google Scholar 

  8. Beer LL, Boyd ES, Peters JW, Posewitz MC (2009) Engineering algae for biohydrogen and biofuel production. Curr Opin Biotechnol 20:264–271

    PubMed  CAS  Google Scholar 

  9. Benemann JR, Berenson JA, Kaplan NO, Kamen MD (1973) Hydrogen evolution by a chloroplast-ferredoxin-hydrogenase system. Proc Natl Acad Sci USA 70:2317–2320

    PubMed  CAS  PubMed Central  Google Scholar 

  10. Bhatla SC, Kaushik V, Yadav MK (2010) Use of oil bodies and oleosins in recombinant protein production and other biotechnological applications. Biotechnol Adv 28:293–300

    PubMed  CAS  Google Scholar 

  11. Blankenship RE et al (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805–809

    PubMed  CAS  Google Scholar 

  12. Boudreau E, Nickelsen J, Lemaire SD, Ossenbuhl F, Rochaix JD (2000) The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability. EMBO J 19:3366–3376

    PubMed  CAS  PubMed Central  Google Scholar 

  13. Bourgis F, Kilaru A, Cao X, Ngando-Ebongue GF, Drira N, Ohlrogge JB, Arondel V (2011) Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proc Natl Acad Sci U S A 108:12527–12532

    PubMed  CAS  PubMed Central  Google Scholar 

  14. Boyle NR et al (2012) Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J Biol Chem 287:15811–15825

    PubMed  CAS  PubMed Central  Google Scholar 

  15. Browse J, McCourt P, Somerville C (1986) A mutant of Arabidopsis deficient in C18–3 and C16–3 leaf lipids. Plant Physiol 81:859–864

    PubMed  CAS  PubMed Central  Google Scholar 

  16. Browse J, Warwick N, Somerville CR, Slack CR (1986) Fluxes through the prokaryotic and eukaryotic pathways of lipid-synthesis in the 16–3 plant Arabidopsis-thaliana. Biochem J 235:25–31

    PubMed  CAS  PubMed Central  Google Scholar 

  17. Bruska MK, Stiebritz MT, Reiher M (2011) Regioselectivity of H cluster oxidation. J Am Chem Soc 133:20588–20603

    PubMed  CAS  PubMed Central  Google Scholar 

  18. Burgal J, Shockey J, Lu CF, Dyer J, Larson T, Graham I, Browse J (2008) Metabolic engineering of hydroxy fatty acid production in plants: RcDGAT2 drives dramatic increases in ricinoleate levels in seed oil. Plant Biotechnol J 6:819–831

    PubMed  CAS  PubMed Central  Google Scholar 

  19. Burgdorf T, Lenz O, Buhrke T, van der Linden E, Jones AK, Albracht SP, Friedrich B (2005) [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J Mol Microbiol Biotechnol 10:181–196

    PubMed  CAS  Google Scholar 

  20. Burgess SJ, Tamburic B, Zemichael F, Hellgardt K, Nixon PJ (2011) Solar-driven hydrogen production in green algae. Adv Appl Microbiol 75:71–110

    PubMed  CAS  Google Scholar 

  21. Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585

    PubMed  CAS  Google Scholar 

  22. 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. ­Photosynthesis Res 84:289–296

    CAS  Google Scholar 

  23. Chi XY, Zhang XW, Guan XY, Ding L, Li YX, Wang MQ, Lin HZ, Qin S (2008) Fatty acid biosynthesis in eukaryotic photosynthetic microalgae: identification of a microsomal delta 12 desaturase in Chlamydomonas reinhardtii. J Microbiol 46:189–201

    PubMed  CAS  Google Scholar 

  24. Chochois V, Dauvillee D, Beyly A, Tolleter D, Cuine S, Timpano H, Ball S, Cournac L, Peltier G (2009) Hydrogen production in Chlamydomonas: photosystem II-dependent and -independent pathways differ in their requirement for starch metabolism. Plant Physiol 151:631–640

    PubMed  CAS  PubMed Central  Google Scholar 

  25. Cinco RM, MacInnis JM, Greenbaum E (1993) The role of carbon dioxide in light-activated hydrogen production by Chlamydomonas reinhardtii. Photosynthesis Res 38:27–33

    CAS  Google Scholar 

  26. Coleman RA, Lee DP (2004) Enzymes of triacylglycerol synthesis and their regulation. Prog Lipid Res 43:134–176

    PubMed  CAS  Google Scholar 

  27. Czabany T, Wagner A, Zweytick D, Lohner K, Leitner E, Ingolic E, Daum G (2008) Structural and biochemical properties of lipid particles from the yeast Saccharomyces cerevisiae. J Biol Chem 283:17065–17074

    PubMed  CAS  Google Scholar 

  28. Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H, Stymne H (2000) Phospholipid: diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci U S A 97:6487–6492

    PubMed  CAS  PubMed Central  Google Scholar 

  29. Dau H, Zaharieva I (2009) Principles, efficiency, and blueprint character of solar-energy conversion in photosynthetic water oxidation. Acc Chem Res 42:1861–1870

    PubMed  CAS  Google Scholar 

  30. Davies JP, Yildiz FH, Grossman A (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15:2150–2159

    PubMed  CAS  PubMed Central  Google Scholar 

  31. Day A, Goldschmidt-Clermont M (2011) The chloroplast transformation toolbox: selectable markers and marker removal. Plant Biotechnol J 9:540–553

    PubMed  CAS  Google Scholar 

  32. Dehesh K, Jones A, Knutzon DS, Voelker TA (1996) Production of high levels of 8:0 and 10:0 fatty acids in transgenic canola by overexpression of Ch FatB2, a thioesterase cDNA from Cuphea hookeriana. Plant J 9:167–172

    PubMed  CAS  Google Scholar 

  33. Delosme R, Olive J, Wollman F-A (1996) Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii. Biochim Biophys Acta (BBA)-Bioenerg 1273:150–158

    Google Scholar 

  34. Delrue F, Setier PA, Sahut C, Cournac L, Roubaud A, Peltier G, Froment AK (2012) An economic, sustainability, and energetic model of biodiesel production from microalgae. Bioresour Technol 111:191–200

    PubMed  CAS  Google Scholar 

  35. Desplats C, Mus F, Cuine S, Billon E, Cournac L, Peltier G (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J Biol Chem 284:4148–4157

    PubMed  CAS  Google Scholar 

  36. Doebbe A, Keck M, La Russa M, Mussgnug JH, Hankamer B, Tekce E, Niehaus K, Kruse O (2010) The interplay of proton, electron, and metabolite supply for photosynthetic H2 production in Chlamydomonas reinhardtii. J Biol Chem 285:30247–30260

    PubMed  CAS  PubMed Central  Google Scholar 

  37. Dunahay TG, Jarvis EE, Dais SS, Roessler PG (1996) Manipulation of microalgal lipid production using genetic engineering. Appl Biochem Biotechnol 57–58:223–231

    Google Scholar 

  38. Durrett TP, Benning C, Ohlrogge J (2008) Plant triacylglycerols as feedstocks for the production of biofuels. Plant J 54:593–607

    PubMed  CAS  Google Scholar 

  39. Falkowski PG (2006) Evolution. Tracing oxygen’s imprint on earth’s metabolic evolution. Science 311:1724–1725

    PubMed  CAS  Google Scholar 

  40. Fan JL, Andre C, Xu CC (2011) A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Lett 585:1985–1991

    PubMed  CAS  Google Scholar 

  41. Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413:117–129

    PubMed  CAS  Google Scholar 

  42. Florin L, Tsokoglou A, Happe T (2001) A novel type of iron hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetic electron transport chain. J Biol Chem 276:6125–6132

    PubMed  CAS  Google Scholar 

  43. Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107:4273–4303

    PubMed  CAS  Google Scholar 

  44. Forestier M, King P, Zhang LP, 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 270:2750–2758

    PubMed  CAS  Google Scholar 

  45. Fouchard S, Hemschemeier A, Caruana A, Pruvost K, Legrand J, Happe T, Peltier G, Cournac L (2005) Autotrophic and mixotrophic hydrogen photoproduction in sulfur-deprived Chlamydomonas cells. Appl Environ Microbiol 71:6199–6205

    PubMed  CAS  PubMed Central  Google Scholar 

  46. Gaffron H (1939) Reduction of carbon dioxide with molecular hydrogen in green algae. ­Nature 143:204–205

    CAS  Google Scholar 

  47. Gaffron H, Rubin J (1942) Fermentative and photochemical production of hydrogen in algae. J Gen Physiol 26:219–240

    PubMed  CAS  PubMed Central  Google Scholar 

  48. Gfeller RP, Gibbs M (1984) Fermentative metabolism of Chlamydomonas reinhardtii: I. Analysis of fermentative products from starch in dark and light. Plant Physiol 75:212–218

    PubMed  CAS  PubMed Central  Google Scholar 

  49. Gfeller RP, Gibbs M (1985) Fermentative metabolism of Chlamydomonas reinhardtii: II. Role of plastoquinone. Plant Physiol 77:509–511

    PubMed  CAS  PubMed Central  Google Scholar 

  50. Ghirardi ML, Togasaki RK, Seibert M (1997) Oxygen sensitivity of algal H2-production. Appl Biochem Biotechnol 63–65:141–151

    PubMed  Google Scholar 

  51. Giannelli L, Scoma A, Torzillo G (2009) Interplay between light intensity, chlorophyll concentration and culture mixing on the hydrogen production in sulfur-deprived Chlamydomonas reinhardtii cultures grown in laboratory photobioreactors. Biotechnol Bioeng 104:76–90

    PubMed  CAS  Google Scholar 

  52. Giroud C, Eichenberger W (1988) Fatty acids of Chlamydomonas reinhardtii-structure, positional distribution and biosynthesis. Biol Chem Hoppe Seyler 369:18–19

    Google Scholar 

  53. Giroud C, Gerber A, Eichenberger W (1988) Lipids of Chlamydomonas reinhardtii-analysis of molecular species and intracellular sites(s) of biosynthesis. Plant Cell Physiol 29:587–595

    CAS  Google Scholar 

  54. Goldet G, Brandmayr C, Stripp ST, Happe T, Cavazza C, Fontecilla-Camps JC, Armstrong FA (2009) Electrochemical kinetic investigations of the reactions of [FeFe]-hydrogenases with carbon monoxide and oxygen: comparing the importance of gas tunnels and active-site electronic/redox effects. J Am Chem Soc 131:14979–14989

    PubMed  CAS  Google Scholar 

  55. Goodson C, Roth R, Wang ZT, Goodenough U (2011) Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost. Eukaryot Cell 10:1592–1606

    PubMed  CAS  PubMed Central  Google Scholar 

  56. Grimme RA, Lubner CE, Bryant DA, Golbeck JH (2008) Photosystem I/molecular wire/metal nanoparticle bioconjugates for the photocatalytic production of H2. J Am Chem Soc 130:6308

    PubMed  CAS  Google Scholar 

  57. Grossman A (2000) Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151:201–224

    PubMed  CAS  Google Scholar 

  58. Grossman AR, Catalanotti C, Yang W, Dubini A, Magneschi L, Subramanian V, Posewitz MC, Seibert M (2011) Multiple facets of anoxic metabolism and hydrogen production in the unicellular green alga Chlamydomonas reinhardtii. New Phytol 190:279–288

    PubMed  CAS  Google Scholar 

  59. Hackstein JH, Akhmanova A, Boxma B, Harhangi HR, Voncken FG (1999) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol 7:441–447

    PubMed  CAS  Google Scholar 

  60. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    PubMed  CAS  PubMed Central  Google Scholar 

  61. Happe T, Kaminski A (2002) Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. Eur J Biochem 269:1022–1032

    PubMed  CAS  Google Scholar 

  62. Happe T, Naber JD (1993) Isolation, characterization and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii. Eur J Biochem 214:475–481

    PubMed  CAS  Google Scholar 

  63. Happe T, Mosler B, Naber JD (1994) Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii. Eur J Biochem 222:769–774

    PubMed  CAS  Google Scholar 

  64. Harwood JL, Guschina IA (2009) The versatility of algae and their lipid metabolism. Biochimie 91:679–684

    PubMed  CAS  Google Scholar 

  65. Hedges SB, Blair JE, Venturi ML, Shoe JL (2004) A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol Biol 4:2

    PubMed  PubMed Central  Google Scholar 

  66. Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807:919–926

    PubMed  CAS  Google Scholar 

  67. Hemschemeier A, Fouchard S, Cournac L, Peltier G, Happe T (2008) Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks. Planta 227:397–407

    PubMed  CAS  Google Scholar 

  68. Hemschemeier A, Jacobs J, Happe T (2008) Biochemical and physiological characterization of the pyruvate formate-lyase Pfl1 of Chlamydomonas reinhardtii, a typically bacterial enzyme in a eukaryotic alga. Eukaryot Cell 7:518–526

    PubMed  CAS  PubMed Central  Google Scholar 

  69. Hofvander P, Carlsson AS, A.S. F (2011) Arabidopsis WRL1 induces a large increase of TAG accumulation in potato microtubers. 5th European symposium on plant lipids: 88

    Google Scholar 

  70. Hong G, Pachter R (2012) Inhibition of biocatalysis in [Fe-Fe] hydrogenase by oxygen: molecular dynamics and density functional theory calculations. ACS Chem Biol 7:1268–1275

    PubMed  CAS  Google Scholar 

  71. Hoshino T, Johnson DJ, Cuello JL (2012) Design of new strategy for green algal photo-hydrogen production: spectral-selective photosystem I activation and photosystem II deactivation. Bioresour Technol 120:233–240

    PubMed  CAS  Google Scholar 

  72. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639

    PubMed  CAS  Google Scholar 

  73. Huang AHC (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Physiol Plant Mol Biol 43:177–200

    CAS  Google Scholar 

  74. Huang AHC (1994) Structure of plant seed oil bodies. Curr Opin Struct Biol 4:493–498

    CAS  Google Scholar 

  75. Ihara M, Nakamoto H, Kamachi T, Okura I, Maeda M (2006) Photoinduced hydrogen production by direct electron transfer from photosystem I cross-linked with cytochrome c 3 to [NiFe]-hydrogenase. Photochem Photobiol 82:1677–1685

    PubMed  CAS  Google Scholar 

  76. Ihara M et al (2006) Light-driven hydrogen production by a hybrid complex of a [NiFe]-hydrogenase and the cyanobacterial photosystem I. Photochem Photobiol 82:676–682

    PubMed  CAS  Google Scholar 

  77. Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett 583:325–329

    PubMed  CAS  Google Scholar 

  78. Jans F et al (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci U S A 105:20546–20551

    PubMed  CAS  PubMed Central  Google Scholar 

  79. Jaworski J, Cahoon EB (2003) Industrial oils from transgenic plants. Curr Opin Plant Biol 6:178–184

    PubMed  CAS  Google Scholar 

  80. Jensen PE, Bassi R, Boekema EJ, Dekker JP, Jansson S, Leister D, Robinson C, Scheller HV (2007) Structure, function and regulation of plant photosystem I. Biochim Biophys Acta Bioenerg 1767:335–352

    CAS  Google Scholar 

  81. Kaczmarzyk D, Fulda M (2010) Fatty acid activation in cyanobacteria mediated by acyl-acyl carrier protein synthetase enables fatty acid recycling. Plant Physiol 152:1598–1610

    PubMed  CAS  PubMed Central  Google Scholar 

  82. Kajikawa M, Yamato KT, Kohzu Y, Shoji S, Matsui K, Tanaka Y, Sakai Y, Fukuzawa H (2006) A front-end desaturase from Chlamydomonas reinhardtii produces pinolenic and coniferonic acids by omega13 desaturation in methylotrophic yeast and tobacco. Plant Cell Physiol 47:64–73

    PubMed  CAS  Google Scholar 

  83. Khozin-Goldberg I, Cohen Z (2011) Unraveling algal lipid metabolism: recent advances in gene identification. Biochimie 93:91–100

    PubMed  CAS  Google Scholar 

  84. Khozin-Goldberg I, Iskandarov U, Cohen Z (2011) LC-PUFA from photosynthetic microalgae: occurrence, biosynthesis, and prospects in biotechnology. Appl Microbiol Biotechnol 91:905–915

    PubMed  CAS  Google Scholar 

  85. Kilian O, Benemann CSE, Niyogi KK, Vick B (2011) High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proc Natl Acad Sci U S A 108:21265–21269

    PubMed  CAS  PubMed Central  Google Scholar 

  86. Knaff DB (2004) Ferredoxin and ferredoxin-dependent enzymes oxygenic photosynthesis: the light reactions. (Ort DR, Yocum CF, Heichel IF (eds)). Springer, Netherlands, pp 333–361

    Google Scholar 

  87. Krasnovsky AA, Van Ni C, Nikandrov VV, Brin GP (1980) Efficiency of hydrogen photoproduction by chloroplast-bacterial hydrogenase systems. Plant Physiol 66:925–930

    PubMed  CAS  PubMed Central  Google Scholar 

  88. Kreuzberg K (1984) Starch fermentation via a formate producing pathway in Chlamydomonas reinhardii, Chlorogonium elongatum and Chlorella fusca. Physiologia Plantarum 61:87–94

    CAS  Google Scholar 

  89. Kruse O, Rupprecht J, Bader KP, Thomas-Hall S, Schenk PM, Finazzi G, Hankamer B (2005) Improved photobiological H2 production in engineered green algal cells. J Biol Chem 280:34170–34177

    PubMed  CAS  Google Scholar 

  90. Lambertz C, Hemschemeier A, Happe T (2010) Anaerobic expression of the ferredoxin-encoding FDX5 gene of Chlamydomonas reinhardtii is regulated by the Crr1 transcription factor. Eukaryot Cell 9:1747–1754

    PubMed  CAS  PubMed Central  Google Scholar 

  91. Lambertz C, Leidel N, Havelius KG, Noth J, Chernev P, Winkler M, Happe T, Haumann M (2011) O2 reactions at the six-iron active site (H-cluster) in [FeFe]-hydrogenase. J Biol Chem 286:40614–40623

    PubMed  CAS  PubMed Central  Google Scholar 

  92. Li Y, Han D, Hu G, Dauvillee D, Sommerfeld M, Ball S, Hu Q (2010) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab Eng 12:387–391

    PubMed  Google Scholar 

  93. Li-Beisson Y SB, Beisson F, Andersson M, Arondel V, Bates P, Baud S, Bird D, DeBono A, Durrett T, Franke R, Graham I, Katayama K, Kelly A, Larson T, Markham J, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid K, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J (2010) Acyl lipid metabolism in the Arabidopsis book. Last R (ed). American Society of Plant Biologists Rockville, MD

    Google Scholar 

  94. Liu B, Benning C (2013) Lipid metabolism in microalgae distinguishes itself. Curr Opin Biotechnol 24:300–309

    Google Scholar 

  95. Lu CF, Napier JA, Clemente TE, Cahoon EB (2011) New frontiers in oilseed biotechnology: meeting the global demand for vegetable oils for food, feed, biofuel, and industrial applications. Curr Opin Biotechnol 22:252–259

    PubMed  CAS  Google Scholar 

  96. Lubner CE, Knörzer P, Silva PJN, Vincent KA, Happe T, Bryant DA, Golbeck JH (2010) Wiring an [Fe-Fe]-hydrogenase with photosystem I for light-induced hydrogen production. Biochemistry 49:10264–10266

    PubMed  CAS  Google Scholar 

  97. Lubner CE, Applegate AM, Knörzer P, Ganago A, Bryant DA, Happe T, Golbeck JH (2011) Solar hydrogen-producing bionanodevice outperforms natural photosynthesis. Proc Natl Acad Sci U S A 108:20988–20991

    PubMed  CAS  PubMed Central  Google Scholar 

  98. Madoka Y, Tomizawa KI, Mizoi J, Nishida I, Nagano Y, Sasaki Y (2002) Chloroplast transformation with modified accD operon increases acetyl-CoA carboxylase and causes extension of leaf longevity and increase in seed yield in tobacco. Plant Cell Physiol 43:1518–1525

    PubMed  CAS  Google Scholar 

  99. Matias PM, Soares CM, Saraiva LM, Coelho R, Morais J, Le Gall J, Carrondo MA (2001) [NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three-dimensional structure determination and refinement at 1.8 A and modelling studies of its interaction with the tetrahaem cytochrome c 3 . J Biol Inorg Chem 6:63–81

    PubMed  CAS  Google Scholar 

  100. McTavish H (1998) Hydrogen evolution by direct electron transfer from photosystem I to hydrogenases. J Biochem 123:644–649

    PubMed  CAS  Google Scholar 

  101. Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–136

    PubMed  CAS  PubMed Central  Google Scholar 

  102. Merchant S, Sawaya MR (2005) The light reactions: a guide to recent acquisitions for the picture gallery. Plant Cell 17:648–663

    PubMed  CAS  PubMed Central  Google Scholar 

  103. Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S, Terauchi AM (2006) Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochim Biophys Acta 1763:578–594

    PubMed  CAS  Google Scholar 

  104. Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J (2012) TAG, You’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol 23:352–363

    PubMed  CAS  Google Scholar 

  105. Michelet L, Lefebvre-Legendre L, Burr SE, Rochaix JD, Goldschmidt-Clermont M (2011) Enhanced chloroplast transgene expression in a nuclear mutant of Chlamydomonas. Plant Biotechnol J 9:565–574

    PubMed  CAS  Google Scholar 

  106. Mignolet E, Lecler R, Ghysels B, Remacle C, Franck F (2012) Function of the chloroplastic NAD(P)H dehydrogenase Nda2 for H2 photoproduction in sulphur-deprived Chlamydomonas reinhardtii. J Biotechnol 162:81–88

    PubMed  CAS  Google Scholar 

  107. Moellering ER, Benning C (2010) RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukaryot Cell 9:97–106

    PubMed  CAS  PubMed Central  Google Scholar 

  108. Mongrand S, Bessoule J-J, Cabantous F, Cassagne C (1998) The C16:3\C18:3 fatty acid balance in photosynthetic tissues from 468 plant species. Phytochemistry 49:1049–1064

    CAS  Google Scholar 

  109. Moore TS, Du Z, Chen Z (2001) Membrane lipid biosynthesis in Chlamydomonas reinhardtii. In vitro biosynthesis of diacylglyceryltrimethylhomoserine. Plant Physiol 125:423–429

    PubMed  CAS  PubMed Central  Google Scholar 

  110. Morweiser M, Kruse O, Hankamer B, Posten C (2010) Developments and perspectives of photobioreactors for biofuel production. Appl Microbiol Biotechnol 87:1291–1301

    PubMed  CAS  Google Scholar 

  111. Mus F, Cournac L, Cardettini V, Caruana A, Peltier G (2005) Inhibitor studies on non-photochemical plastoquinone reduction and H2 photoproduction in Chlamydomonas reinhardtii. Biochim Biophys Acta 1708:322–332

    PubMed  CAS  Google Scholar 

  112. 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 282:25475–25486

    PubMed  CAS  Google Scholar 

  113. Nguyen HM et al (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: With focus on proteins involved in lipid metabolism. Proteomics 11:4266–4273

    PubMed  CAS  Google Scholar 

  114. Oey M, Lohse M, Kreikemeyer B, Bock R (2009) Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J 57:436–445

    PubMed  CAS  Google Scholar 

  115. Ohlrogge J, Pollard M, Bao X, Focke M, Girke T, Ruuska S, Mekhedov S, Benning C (2000) Fatty acid synthesis: from CO2 to functional genomics. Biochem Soc Trans 28:567–574

    PubMed  CAS  Google Scholar 

  116. Pape M, Lambertz C, Happe T, Hemschemeier A (2012) Differential expression of the Chlamydomonas [FeFe]-hydrogenase-encoding HYDA1 gene is regulated by the copper response regulator1. Plant Physiol 159:1700–1712

    PubMed  CAS  PubMed Central  Google Scholar 

  117. Philipps G, Krawietz D, Hemschemeier A, Happe T (2011) A pyruvate formate lyase-deficient Chlamydomonas reinhardtii strain provides evidence for a link between fermentation and hydrogen production in green algae. Plant J 66:330–340

    PubMed  CAS  Google Scholar 

  118. Philipps G, Happe T, Hemschemeier A (2012) Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii. Planta 235:729–745

    PubMed  CAS  Google Scholar 

  119. Radakovits R, Eduafo PM, Posewitz MC (2011) Genetic engineering of fatty acid chain length in Phaeodactylum tricornutum. Metab Eng 13:89–95

    PubMed  CAS  Google Scholar 

  120. Rawsthorne S (2002) Carbon flux and fatty acid synthesis in plants. Prog Lipid Res 41:182–196

    PubMed  CAS  Google Scholar 

  121. Raymond J, Blankenship RE (2004) Biosynthetic pathways, gene replacement and the antiquity of life. Geobiology 2:199–203

    CAS  Google Scholar 

  122. Raymond J, Segre D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:1764–1767

    PubMed  CAS  Google Scholar 

  123. Riekhof WR, Sears BB, Benning C (2005) Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase ­BTA1Cr. Eukaryot Cell 4:242–252

    PubMed  CAS  PubMed Central  Google Scholar 

  124. Roessler PG, Lien S (1984) Purification of hydrogenase from Chlamydomonas reinhardtii. Plant Physiol 75:705–709

    PubMed  CAS  PubMed Central  Google Scholar 

  125. Roessler PG, Ohlrogge JB (1993) Cloning and characterization of the gene that encodes acetyl-coenzyme-A carboxylase in the alga Cyclotella cryptica. J Biol Chem 268:19254–19259

    PubMed  CAS  Google Scholar 

  126. Rühle T, Hemschemeier A, Melis A, Happe T (2008) A novel screening protocol for the isolation of hydrogen producing Chlamydomonas reinhardtii strains. BMC Plant Biol 8:107

    PubMed  PubMed Central  Google Scholar 

  127. Ruuska SA, Girke T, Benning C, Ohlrogge JB (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 14:1191–1206

    PubMed  CAS  PubMed Central  Google Scholar 

  128. Sato N, Fujiwara S, Kawaguchi A, Tsuzuki M (1997) Cloning of a gene for chloroplast omega6 desaturase of a green alga, Chlamydomonas reinhardtii. J Biochem 122:1224–1232

    PubMed  CAS  Google Scholar 

  129. Sawers RG (2005) Formate and its role in hydrogen production in Escherichia coli. Biochem Soc Trans 33:42–46

    PubMed  CAS  Google Scholar 

  130. Scharnewski M, Pongdontri P, Mora G, Hoppert M, Fulda M (2008) Mutants of Saccharomyces cerevisiae deficient in acyl-CoA synthetases secrete fatty acids due to interrupted fatty acid recycling. FEBS J 275:2765–2778

    PubMed  CAS  Google Scholar 

  131. Schroda M (2006) RNA silencing in Chlamydomonas: mechanisms and tools. Curr Genet 49:69–84

    PubMed  CAS  Google Scholar 

  132. Schwarze A, Kopczak MJ, Rogner M, Lenz O (2010) Requirements for construction of a functional hybrid complex of photosystem I and [NiFe]-hydrogenase. Appl Environ Microbiol 76:2641–2651

    PubMed  CAS  PubMed Central  Google Scholar 

  133. Scoma A, Krawietz D, Faraloni C, Giannelli L, Happe T, Torzillo G (2012) Sustained H2 production in a Chlamydomonas reinhardtii D1 protein mutant. J Biotechnol 157: 613–619

    PubMed  CAS  Google Scholar 

  134. Scott SA, Davey MP, Dennis JS, Horst I, Howe CJ, Lea-Smith DJ, Smith AG (2010) Biodiesel from algae: challenges and prospects. Curr Opin Biotechnol 21:277–286

    PubMed  CAS  Google Scholar 

  135. Shanklin J, Cahoon EB (1998) Desaturation and related modifications of fatty acids. Annu Rev Plant Physiol Plant Mol Biol 49:611–641

    PubMed  CAS  Google Scholar 

  136. Sheehan J, Dunahay T, Benemann J, Roessler PG A look back at the US Department of Energy’s aquatic species program—biodiesel from algae, 1998, US Department of Energy’s Office of Fuels Development: Golden, CO: National Renewable Energy Laboratory

    Google Scholar 

  137. Shen B, Allen WB, Zheng PZ, Li CJ, Glassman K, Ranch J, Nubel D, Tarczynski MC (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 153:980–987

    PubMed  CAS  PubMed Central  Google Scholar 

  138. Shima S, Thauer RK (2007) A third type of hydrogenase catalyzing H2 activation. Chem Rec 7:37–46

    PubMed  CAS  Google Scholar 

  139. Shockey JM, Gidda SK, Chapital DC, Kuan JC, Dhanoa PK, Bland JM, Rothstein SJ, ­Mullen RT, Dyer JM (2006) Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum. Plant Cell 18:2294–2313

    PubMed  CAS  PubMed Central  Google Scholar 

  140. Siaut M et al (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7

    PubMed  CAS  PubMed Central  Google Scholar 

  141. Skjånes K, Knutsen G, Källqvist T, Lindblad P (2008) H2 production from marine and freshwater species of green algae during sulfur deprivation and considerations for bioreactor design. Int J Hydrogen Energy 33:511–521

    Google Scholar 

  142. Stiebritz MT, Reiher M (2012) Hydrogenases and oxygen. Chem Sci 3:1739–1751

    CAS  Google Scholar 

  143. Stripp ST, Goldet G, Brandmayr C, Sanganas O, Vincent KA, Haumann M, Armstrong FA, Happe T (2009) How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms. Proc Natl Acad Sci U S A 106:17331–17336

    PubMed  CAS  PubMed Central  Google Scholar 

  144. Stuart TS, Gaffron H (1972) The mechanism of hydrogen photoproduction by several algae. Planta 106:101–112

    PubMed  CAS  Google Scholar 

  145. Suorsa M, Sirpio S, Aro EM (2009) Towards characterization of the chloroplast NAD(P)H dehydrogenase complex. Mol Plant 2:1127–1140

    PubMed  CAS  Google Scholar 

  146. Surzycki R, Cournac L, Peltier G, Rochaix JD (2007) Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas. Proc Natl Acad Sci U S A 104:17548–17553

    PubMed  CAS  PubMed Central  Google Scholar 

  147. Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol Cell Proteomics 9:1514–1532

    PubMed  CAS  PubMed Central  Google Scholar 

  148. Terauchi AM et al (2009) Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J Biol Chem 284:25867–25878

    PubMed  CAS  PubMed Central  Google Scholar 

  149. Thannickal VJ (2009) Oxygen in the evolution of complex life and the price we pay. Am J Respir Cell Mol Biol 40:507–510

    PubMed  CAS  PubMed Central  Google Scholar 

  150. Timmins M, Thomas-Hall SR, Darling A, Zhang E, Hankamer B, Marx UC, Schenk PM (2009) Phylogenetic and molecular analysis of hydrogen-producing green algae. J Exp Bot 60:1691–1702

    PubMed  CAS  PubMed Central  Google Scholar 

  151. Timmins M et al (2009) The metabolome of Chlamydomonas reinhardtii following induction of anaerobic H2 production by sulfur depletion. J Biol Chem 284:35996

    CAS  Google Scholar 

  152. Tolleter D et al (2011) Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23:2619–2630

    PubMed  CAS  PubMed Central  Google Scholar 

  153. Vieler A, Wilhelm C, Goss R, Sub R, Schiller J (2007) The lipid composition of the unicellular green alga Chlamydomonas reinhardtii and the diatom Cyclotella meneghiniana investigated by MALDI-TOF MS and TLC. Chem Phys Lipids 150:143–155

    PubMed  CAS  Google Scholar 

  154. Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272

    PubMed  CAS  Google Scholar 

  155. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501

    PubMed  CAS  Google Scholar 

  156. Vincent KA, Parkin A, Lenz O, Albracht SP, Fontecilla-Camps JC, Cammack R, Friedrich B, Armstrong FA (2005) Electrochemical definitions of O2 sensitivity and oxidative inactivation in hydrogenases. J Am Chem Soc 127: 18179–18189

    PubMed  CAS  Google Scholar 

  157. Vincent KA, Parkin A, Armstrong FA (2007) Investigating and exploiting the electrocatalytic properties of hydrogenases. Chem Rev 107:4366–4413

    PubMed  CAS  Google Scholar 

  158. Voelker T, Worrell A, Anderson L, Bleibaum J, Fan C, Hawkins D, Radke S, Davies H (1992) Fatty acid biosynthesis redirected to medium chains in transgenic oilseed plants. Science 257:72–74

    PubMed  CAS  Google Scholar 

  159. Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot Cell 8:1856–1868

    PubMed  CAS  PubMed Central  Google Scholar 

  160. Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799

    PubMed  CAS  Google Scholar 

  161. Winkler M, Heil B, Heil B, Happe T (2002) Isolation and molecular characterization of the [Fe]-hydrogenase from the unicellular green alga Chlorella fusca. Biochim Biophys Acta 1576:330–334

    PubMed  CAS  Google Scholar 

  162. Winkler M, Kuhlgert S, Hippler M, Happe T (2009) Characterization of the key step for light-driven hydrogen evolution in green algae. J Biol Chem 284:36620–36627

    PubMed  CAS  PubMed Central  Google Scholar 

  163. Winkler M, Hemschemeier A, Jacobs J, Stripp S, Happe T (2010) Multiple ferredoxin isoforms in Chlamydomonas reinhardtii - their role under stress conditions and biotechnological implications. Eur J Cell Biol 89:998–1004

    PubMed  CAS  Google Scholar 

  164. Winkler M, Kawelke S, Happe T (2011) Light driven hydrogen production in protein based semi-artificial systems. Bioresour Technol 102:8493–8500

    PubMed  CAS  Google Scholar 

  165. Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129–139

    PubMed  CAS  PubMed Central  Google Scholar 

  166. Yacoby I, Pochekailov S, Toporik H, Ghirardi ML, King PW, Zhang S (2011) Photosynthetic electron partitioning between [FeFe]-hydrogenase and ferredoxin:NADP+-oxidoreductase (FNR) enzymes in vitro. Proc Natl Acad Sci U S A 108:9396–9401

    PubMed  CAS  PubMed Central  Google Scholar 

  167. Yohn C MM, Behnke C, Brand A (2011) Stress-induced lipid trigger. US Patent

    Google Scholar 

  168. Yoon K, Han D, Li Y, Sommerfeld M, Hu Q (2012) Phospholipid:diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii. Plant Cell 24:3708–3724

    PubMed  CAS  PubMed Central  Google Scholar 

  169. Zauner S, Jochum W, Bigorowski T, Benning C (2012) A cytochrome b 5-containing plastid-located fatty acid desaturase from Chlamydomonas reinhardtii. Eukaryot Cell 11:856–863

    PubMed  CAS  PubMed Central  Google Scholar 

  170. Zhang LP, Happe T, Melis A (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214:552–561

    PubMed  CAS  Google Scholar 

  171. Zhang M, Fan J, Taylor DC, Ohlrogge JB (2009) DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development. Plant Cell 21:3885–3901

    PubMed  CAS  PubMed Central  Google Scholar 

  172. Zheng P et al (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat Genet 40:367–372

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Biologie Environnementale et Biotechnologie, CEA/CNRS/Aix Marseille Université, CEA Cadarache, 13108, Saint-Paul-lez-Durance, France

    Yonghua Li-Beisson & Gilles Peltier

  2. Fakultät für Biologie und Biotechnologie, AG Photobiotechnologie, Ruhr-Universität Bochum, Universitätsstr. 150, 44801, Bochum, Germany

    Philipp Knörzer, Thomas Happe & Anja Hemschemeier

Authors
  1. Yonghua Li-Beisson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gilles Peltier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philipp Knörzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas Happe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anja Hemschemeier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Happe .

Editor information

Editors and Affiliations

  1. Department of Plant Biology, Univeristy of California-Davis, Davis, California, USA

    Steven M. Theg

  2. Physiologie Membranaire et Moléculaire du Chloroplaste, Institut de Biologie Physico-Chimique, Paris, France

    Francis-André Wollman

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Li-Beisson, Y., Peltier, G., Knörzer, P., Happe, T., Hemschemeier, A. (2014). Hydrogen and Biofuel Production in the Chloroplast. In: Theg, S., Wollman, FA. (eds) Plastid Biology. Advances in Plant Biology, vol 5. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1136-3_19

Download citation

Publish with us

Policies and ethics

Search

Navigation