Genome, Functional Gene Annotation, and Nuclear Transformation of the Heterokont Oleaginous Alga CCMP1779

English version České info

Unicellular marine algae have promise for providing sustainable and scalable biofuel feedstocks, although no single species has emerged as a preferred organism. Moreover, adequate molecular and genetic resources prerequisite for the rational engineering of marine algal feedstocks are lacking for most candidate species. Heterokonts of the genus Nannochloropsis naturally have high cellular oil content and are already in use for industrial production of high-value lipid products. First success in applying reverse genetics by targeted gene replacement makes Nannochloropsis oceanica an attractive model to investigate the cell and molecular biology and biochemistry of this fascinating organism group. Here we present the assembly of the 28.7 Mb genome of N. oceanica CCMP1779. RNA sequencing data from nitrogen-replete and nitrogen-depleted growth conditions support a total of 11,973 genes, of which in addition to automatic annotation some were manually inspected to predict the biochemical repertoire for this organism. Among others, more than 100 genes putatively related to lipid metabolism, 114 predicted transcription factors, and 109 transcriptional regulators were annotated. Comparison of the N. oceanica CCMP1779 gene repertoire with the recently published N. gaditana genome identified 2,649 genes likely specific to N. oceanica CCMP1779. Many of these N. oceanica–specific genes have putative orthologs in other species or are supported by transcriptional evidence. However, because similarity-based annotations are limited, functions of most of these species-specific genes remain unknown. Aside from the genome sequence and its analysis, protocols for the transformation of N. oceanica CCMP1779 are provided. The availability of genomic and transcriptomic data for Nannochloropsis oceanica CCMP1779, along with efficient transformation protocols, provides a blueprint for future detailed gene functional analysis and genetic engineering of Nannochloropsis species by a growing academic community focused on this genus.

Vyšlo v časopise: Genome, Functional Gene Annotation, and Nuclear Transformation of the Heterokont Oleaginous Alga CCMP1779. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1003064
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003064

Souhrn

Zdroje

1. DismukesGC, CarrieriD, BennetteN, AnanyevGM, PosewitzMC (2008) Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr Opin Biotechnol 19: 235–240.

2. WijffelsRH, BarbosaMJ (2010) An outlook on microalgal biofuels. Science 329: 796–799.

3. WeyerKM, BushDR, DarzinsA, WillsonBD (2010) Theoretical maximum algal oil production. Bioenergy Res 3: 204–213.

4. BowlerC, AllenAE, BadgerJH, GrimwoodJ, JabbariK, et al. (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456: 239–244.

5. SiautM, HeijdeM, MangognaM, MontsantA, CoeselS, et al. (2007) Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum. Gene 406: 23–35.

6. CockJM, SterckL, RouzeP, ScornetD, AllenAE, et al. (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465: 617–621.

7. DerelleE, FerrazC, RombautsS, RouzeP, WordenAZ, et al. (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103: 11647–11652.

8. KilianO, BenemannCS, NiyogiKK, VickB (2011) High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proc Natl Acad Sci USA

9. Van Den Hook C, Mann DG, Jahns HM (1995) Algae: an introduction to phycology. New York, NY: Cambridge University Press.

10. Reyes-PrietoA, WeberAP, BhattacharyaD (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41: 147–168.

11. SchneiderJC, RoesslerP (1994) Radiolabeling studies of lipids and fatty acids in Nannochloropsis (Eustigmatophyceae), an oleagenious marine alga. J Phycol 30: 594–598.

12. TononT, HarveyD, LarsonTR, GrahamIA (2002) Long chain polyunsaturated fatty acid production and partitioning to triacylglycerols in four microalgae. Phytochemistry 61: 15–24.

13. SukenikA, CarmeliY (1990) Lipid synthesis and fatty acid composition in Nannochloropsis sp. (Eustigmatophyceae) grown in a light-dark cycle. J Phycol 26: 463–469.

14. DanielewiczMA, AndersonLA, FranzAK (2011) Triacylglycerol profiling of marine microalgae by mass spectrometry. J Lipid Res 52: 2101–2108.

15. HuHH, GaoKS (2003) Optimization of growth and fatty acid composition of a unicellular marine picoplankton, Nannochloropsis sp., with enriched carbon sources. Biotechnol Lett 25: 421–425.

16. RodolfiL, Chini ZittelliG, BassiNÝ, PadovaniG, BiondiN, et al. (2009) Microalgae for oil: Strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102: 100–112.

17. XuF, CaiZL, CongW, FanOY (2004) Growth and fatty acid composition of Nannochloropsis sp grown mixotrophically in fed-batch culture. Biotechnol Lett 26: 1319–1322.

18. SrinivasR, OchsC (2012) Effect of uv-a irradiance on lipid accumulation in Nannochloropsis oculata. Photochem Photobiol 88: 684–689.

19. SimionatoD, SforzaE, Corteggiani CarpinelliE, BertuccoA, GiacomettiGM, et al. (2011) Acclimation of Nannochloropsis gaditana to different illumination regimes: effects on lipids accumulation. Bioresour Technol 102: 6026–6032.

20. PanK, QinJJ, LiS, DaiWK, ZhuBH, et al. (2011) Nuclear monoploidy and asexual propagation of Nannochloropsis oceanica (Eustigmatophyceae) as revealed by its genome sequence. J Phycol 47: 1425–1432.

21. RadakovitsR, JinkersonRE, FuerstenbergSI, TaeH, SettlageRE, et al. (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 3: 686.

22. SaitouN, NeiM (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.

23. AndersenRA, BrettRW, PotterD, SextonJP (1998) Phylogeny of the Eustigmatophyceae based upon 18S rDNA, with emphasis on Nannochloropsis. Protist 149: 14.

24. Harris EH (2009) The Chlamydomonas Source Book. Oxford, Burlington, San Diego.

25. VielerA, BrubakerSB, VickB, BenningC (2012) A lipid droplet protein of Nannochloropsis with functions partially analogous to plant oleosins. Plant Physiol 158: 1562–1569.

26. LiSS, TsaiHJ (2009) Transgenic microalgae as a non-antibiotic bactericide producer to defend against bacterial pathogen infection in the fish digestive tract. Fish Shellfish Immunol 26: 316–325.

27. BertholdP, SchmittR, MagesW (2002) An engineered Streptomyces hygroscopicus aph 7″ gene mediates dominant resistance against hygromycin B in Chlamydomonas reinhardtii. Protist 153: 401–412.

28. CantarelBL, KorfI, RobbSM, ParraG, RossE, et al. (2008) MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18: 188–196.

29. EilbeckK, MooreB, HoltC, YandellM (2009) Quantitative measures for the management and comparison of annotated genomes. BMC Bioinformatics 10: 67.

30. ParraG, BradnamK, KorfI (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23: 1061–1067.

31. CockJM, SterckL, RouzeP, ScornetD, AllenAE, et al. (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465: 617–621.

32. ConesaA, GötzS, Garcia-GomezJM, TerolJ, TalonM, et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676.

33. MyhreS, TveitH, MollestadT, LaegreidA (2006) Additional gene ontology structure for improved biological reasoning. Bioinformatics 22: 2020–2027.

34. ZdobnovEM, ApweilerR (2001) InterProScan–an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847–848.

35. MillerR, WuG, DeshpandeRR, VielerA, GaertnerK, et al. (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen-deprivation predict diversion of metabolism. Plant Physiol 154: 1737–1752.

36. BennetzenJL, SanMiguelP, ChenM, TikhonovA, FranckiM, et al. (1998) Grass genomes. Proc Natl Acad Sci USA 95: 1975–1978.

37. SanMiguelP, TikhonovA, JinYK, MotchoulskaiaN, ZakharovD, et al. (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765–768.

38. GardnerPP, DaubJ, TateJ, MooreBL, OsuchIH, et al. (2011) Rfam: Wikipedia, clans and the “decimal” release. Nucleic Acids Res 39: D141–145.

39. NawrockiEP, KolbeDL, EddySR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25: 1335–1337.

40. ChenN (2004) Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics Chapter 4: Unit 4 10.

41. AdaiA, JohnsonC, MlotshwaS, Archer-EvansS, ManochaV, et al. (2005) Computational prediction of miRNAs in Arabidopsis thaliana. Genome Res 15: 78–91.

42. GreenBR, PicherskyE, KloppstechK (1991) Chlorophyll a/b-binding proteins: an extended family. Trends Biochem Sci 16: 181–186.

43. GrossmanA, ManodoriA, SnyderD (1990) Light-harvesting proteins of diatoms: their relationship to the chlorophyll a/b binding proteins of higher plants and their mode of transport into plastids. Mol Gen Genet 224: 91–100.

44. NymarkM, ValleKC, BrembuT, HanckeK, WingeP, et al. (2009) An integrated analysis of molecular acclimation to high light in the marine diatom Phaeodactylum tricornutum. PLoS ONE 4: e7743 doi:10.1371/journal.pone.0007743

45. PeersG, TruongTB, OstendorfE, BuschA, ElradD, et al. (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462: 518–521.

46. AlboresiA, GerottoC, GiacomettiGM, BassiR, MorosinottoT (2010) Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proc Natl Acad Sci USA 107: 11128–11133.

47. ZhuSH, GreenBR (2010) Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochim Biophys Acta 1797: 1449–1457.

48. LiXP, BjorkmanO, ShihC, GrossmanAR, RosenquistM, et al. (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391–395.

49. BrownJS (1987) Functional organization of chlorophyll a and carotenoids in the alga, Nannochloropsis salina. Plant Physiol 83: 434–437.

50. SukenikA, LivneA, AptKE, GrossmanAR (2000) Characterization of a gene encoding the light-harvesting violaxanthin-chlorophyll protein of Nannochloropsis sp (Eustigmatophyceae). J Phycol 36: 563–570.

51. LiuZ, YanH, WangK, KuangT, ZhangJ, et al. (2004) Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428: 287–292.

52. Demmig-AdamsB, GilmoreAM, AdamsWW3rd (1996) Carotenoids 3: in vivo function of carotenoids in higher plants. FASEB J 10: 403–412.

53. NiyogiKK, GrossmanAR, BjorkmanO (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121–1134.

54. GentileMP, BlanchHW (2001) Physiology and xanthophyll cycle activity of Nannochloropsis gaditana. Biotechnol Bioeng 75: 1–12.

55. FieldCB, BehrenfeldMJ, RandersonJT, FalkowskiP (1998) Primary production of the biosphere: Integrating terrestrial and oceanic components. Science 281: 237–240.

56. WangY, DuanmuD, SpaldingM (2011) Carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii : inorganic carbon transport and CO2 recapture. Photosynth Res 109: 115–122.

57. MoroneyJV, YnalvezRA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Euk Cell 6: 1251–1259.

58. ImCS, GrossmanAR (2002) Identification and regulation of high light-induced genes in Chlamydomonas reinhardtii. Plant J 30: 301–313.

59. BurowMD, ChenZY, MoutonTM, MoroneyJV (1996) Isolation of cDNA clones of genes induced upon transfer of Chlamydomonas reinhardtii cells to low CO2. Plant Mol Biol 31: 443–448.

60. MiuraK, YamanoT, YoshiokaS, KohinataT, InoueY, et al. (2004) Expression profiling-based identification of CO2-responsive genes regulated by CCM1 controlling a carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 135: 1595–1607.

61. SpaldingMH, JeffreyM (1989) Membrane-associated polypeptides induced in Chlamydomonas by limiting CO2 concentrations. Plant Physiol 89: 133–137.

62. ReinfelderJR, KraepielAML, MorelFMM (2000) Unicellular C4 photosynthesis in a marine diatom. Nature 407: 996–999.

63. ReinfelderJR, MilliganAJ, MorelFoMM (2004) The role of the c4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol 135: 2106–2111.

64. ArmbrustEV, BergesJA, BowlerC, GreenBR, MartinezD, et al. (2004) The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306: 79–86.

65. JanouskovecJ, HorakA, ObornikM, LukesJ, KeelingPJ (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci U S A 107: 10949–10954.

66. SforzaE, CiprianiR, MorosinottoT, BertuccoA, GiacomettiGM (2012) Excess CO2 supply inhibits mixotrophic growth of Chlorella protothecoides and Nannochloropsis salina. Bioresour Technol 104: 523–529.

67. XuF, CongW, CaiZ-L, OuyangF (2004) Effects of organic carbon sources on cell growth and eicosapentaenoic acid content of Nannochloropsis sp. J Appl Phycol 16: 499–503.

68. GallowayRE (1990) Selective conditions and isolation of mutants in salt-tolerant, lipid-producing microalgae. J Phycol 26: 752–760.

69. GhirardiML, DubiniA, YuJ, ManessPC (2009) Photobiological hydrogen-producing systems. Chem Soc Rev 38: 52–61.

70. GhirardiML, PosewitzMC, ManessPC, DubiniA, YuJ, et al. (2007) Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Ann Rev Plant Biol 58: 71–91.

71. PosewitzMC, KingPW, SmolinskiSL, SmithRD, GinleyAR, et al. (2005) Identification of genes required for hydrogenase activity in Chlamydomonas reinhardtii. Biochem Soc Trans 33: 102–104.

72. HodgsonPA, HendersonRJ, SargentJR, LeftleyJW (1991) Patterns of variation in the lipid class and fatty-acid composition of Nannochloropsis oculata (Eustigmatophyceae) during batch culture. 1. The growth-cycle. J Appl Phycol 3: 169–181.

73. MarrakchiH, ZhangYM, RockCO (2002) Mechanistic diversity and regulation of Type II fatty acid synthesis. Biochem Soc Trans 30: 1050–1055.

74. SchweizerE, HofmannJ (2004) Microbial type I fatty acid synthases (FAS): Major players in a network of cellular FAS systems. Microbiol Mol Biol Rev 68: 501–517.

75. MetzJG, RoesslerP, FacciottiD, LeveringC, DittrichF, et al. (2001) Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes. Science 293: 290–293.

76. GoldbergI, BlochK (1972) Fatty acid synthetases in Euglena gracilis. J Biol Chem 247: 7349–7357.

77. HauvermaleA, KunerJ, RosenzweigB, GuerraD, DiltzS, et al. (2006) Fatty acid production in Schizochytrium sp.: Involvement of a polyunsaturated fatty acid synthase and a type I fatty acid synthase. Lipids 41: 739–747.

78. BenningC (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Ann Rev Cell Dev Biol 25: 71–91.

79. GuschinaIA, HarwoodJL (2006) Lipids and lipid metabolism in eukaryotic algae. Prog Lipid Res 45: 160–186.

80. HarwoodJL, GuschinaIA (2009) The versatility of algae and their lipid metabolism. Biochimie 91: 679–684.

81. RajakumariS, DaumG (2010) Janus-faced enzymes yeast Tgl3p and Tgl5p catalyze lipase and acyltransferase reactions. Mol Biol Cell 21: 501–510.

82. EastmondPJ (2006) SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell 18: 665–675.

83. AthenstaedtK, DaumG (2005) Tgl4p and Tgl5p, two triacylglycerol lipases of the yeast Saccharomyces cerevisiae are localized to lipid particles. J Biol Chem 280: 37301–37309.

84. KunauWH, DommesV, SchulzH (1995) β-Oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: A century of continued progress. Prog Lip Res 34: 267–342.

85. WandersRJA, WaterhamHR (2006) Biochemistry of mammalian peroxisomes revisited. Ann Rev Biochem 75: 295–332.

86. GoepfertS, PoirierY (2007) β-Oxidation in fatty acid degradation and beyond. Curr Opin Plant Biol 10: 245–251.

87. ShenYQ, LangBF, BurgerG (2009) Diversity and dispersal of a ubiquitous protein family: acyl-CoA dehydrogenases. Nucleic Acids Res 37: 5619–5631.

88. MichelG, TononT, ScornetD, CockJM, KloaregB (2010) The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol 188: 82–97.

89. MichelG, TononT, ScornetD, CockJM, KloaregB (2010) Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytol 188: 67–81.

90. LamHM, CoschiganoKT, OliveiraIC, Melo-OliveiraR, CoruzziGM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Ann Rev Plant Physiol Plant Mol Biol 47: 569–593.

91. KroukG, CrawfordNM, CoruzziGM, TsayYF (2010) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Bioly 13: 265–272.

92. JanderG, JoshiV (2009) Aspartate-derived amino acid biosynthesis in Arabidopsis thaliana. The Arabidopsis Book e0121.

93. BinderS (2010) Branched-chain amino acid metabolism in Arabidopsis thaliana. The Arabidopsis Book e0137.

94. TzinV, GaliliG (2010) The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. The Arabidopsis Book e0132.

95. MurakamiR, HashimotoH (2009) Unusual nuclear division in Nannochloropsis oculata (Eustigmatophyceae, Heterokonta) which may ensure faithful transmission of secondary plastids. Protist 160: 41–49.

96. TakahashiH, KoprivaS, GiordanoM, SaitoK, HellR (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Ann Rev Plant Biol 62: 157–184.

97. ThomasD, Surdin-KerjanY (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 61: 503–532.

98. KoprivaS, FritzemeierK, WiedemannG, ReskiR (2007) The putative moss 3′ phosphoadenosine 5′ phosphosulfate reductase is a novel form of adenosine 5′ phosphosulfate reductase without an iron sulfur cluster. J Biol Chem 282: 22930–22938.

99. PatronN, DurnfordD, KoprivaS (2008) Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evolutionary Biology 8: 39.

100. AgrawalS, StriepenB (2010) More membranes, more proteins: Complex protein import mechanisms into secondary plastids. Protist 161: 672–687.

101. SchnellDJ, BlobelG, KeegstraK, KesslerF, KoK, et al. (1997) A consensus nomenclature for the protein-import components of the chloroplast envelope. Trends Cell Biol 7: 303–304.

102. LiHM, ChiuCC (2010) Protein transport into chloroplasts. Ann Rev Plant Biol 61: 157–180.

103. Shipman-RostonRL, RuppelNJ, DamocC, PhinneyBS, InoueK (2010) The significance of protein maturation by plastidic type I signal peptidase 1 for thylakoid development in Arabidopsis chloroplasts. Plant Physiol 152: 1297–1308.

104. ShiLX, ThegSM (2010) A stromal heat shock protein 70 system functions in protein import into chloroplasts in the moss Physcomitrella patens. Plant Cell 22: 205–220.

105. McFaddenGI, van DoorenGG (2004) Evolution: red algal genome affirms a common origin of all plastids. Curr Biol 14: R514–R516.

106. GschloesslB, GuermeurY, CockJM (2008) HECTAR: A method to predict subcellular targeting in heterokonts. BMC Bioinformatics 9: 393.

107. MiyagishimaSY, KabeyaY (2010) Chloroplast division: squeezing the photosynthetic captive. Curr Opin Microbiol 13: 738–746.

108. OsteryoungKW, NunnariJ (2003) The division of endosymbiotic organelles. Science 302: 1698–1704.

109. EmanuelssonO, NielsenH, BrunakS, vonHG (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005–1016.

110. EmanuelssonO, NielsenH, vonHG (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978–984.

111. PetersenTN, BrunakS, vonHG, NielsenH (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786.

112. NishikawaT, KajitaniH, SatoM, MogiY, MoriyannaY, et al. (2010) Isolation of chloroplast FtsZ and AtpC, and analysis of protein targeting into the complex chloroplast of the haptophyte Pavlova pinguis. Cytologia 75: 203–210.

113. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.

114. van DoorenGG, ReiffSB, TomovaC, MeissnerM, HumbelBM, et al. (2009) A novel dynamin-related protein has been recruited for apicoplast fission in Toxoplasma gondii. Curr Biol 19: 267–276.

115. KiefelBR, GilsonPR, BeechPL (2006) Cell biology of mitochondrial dynamics. Int Rev Cytol 254: 151–213.

116. MiyagishimaSY, NozakiH, NishidaK, MatsuzakiM, KuroiwaT (2004) Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J Mol Evol 58: 291–303.

117. LutkenhausJ (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Ann Rev Biochem 76: 539–562.

118. CollettiKS, TattersallEA, PykeKA, FroelichJE, StokesKD, et al. (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10: 507–516.

119. VithaS, FroehlichJE, KoksharovaO, PykeKA, vanEH, et al. (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15: 1918–1933.

120. YoshidaY, KuroiwaH, MisumiO, YoshidaM, OhnumaM, et al. (2010) Chloroplasts divide by contraction of a bundle of nanofilaments consisting of polyglucan. Science 329: 949–953.

121. YoshidaY, KuroiwaH, HirookaS, FujiwaraT, OhnumaM, et al. (2009) The bacterial ZapA-like protein ZED is required for mitochondrial division. Curr Biol 19: 1491–1497.

122. MatsuzakiM, MisumiO, ShinIT, MaruyamaS, TakaharaM, et al. (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653–657.

123. ErringtonJ, DanielRA, ScheffersDJ (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67: 52–65 table.

124. KoksharovaOA, WolkCP (2002) A novel gene that bears a DnaJ motif influences cyanobacterial cell division. J Bacteriol 184: 5524–5528.

125. MarboutyM, SaguezC, Cassier-ChauvatC, ChauvatF (2009) Characterization of the FtsZ-interacting septal proteins SepF and Ftn6 in the spherical-celled cyanobacterium Synechocystis strain PCC 6803. J Bacteriol 191: 6178–6185.

126. MiyagishimaSY (2011) Mechanism of plastid division: from a bacterium to an organelle. Plant Physiol 155: 1533–1544.

127. CoeselS, MangognaM, IshikawaT, HeijdeM, RogatoA, et al. (2009) Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity. EMBO Rep 10: 655–661.

128. IshikawaM, TakahashiF, NozakiH, NagasatoC, MotomuraT, et al. (2009) Distribution and phylogeny of the blue light receptors aureochromes in eukaryotes. Planta 230: 543–552.

129. TakahashiF, YamagataD, IshikawaM, FukamatsuY, OguraY, et al. (2007) AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc Natl Acad Sci USA 104: 19625–19630.

130. DasP, LeiW, AzizSS, ObbardJP (2011) Enhanced algae growth in both phototrophic and mixotrophic culture under blue light. Bioresour Technol 102: 3883–3887.

131. MatsuoT, IshiuraM (2011) Chlamydomonas reinhardtii as a new model system for studying the molecular basis of the circadian clock. FEBS Lett 585: 1495–1502.

132. NikaidoSS, JohnsonCH (2000) Daily and circadian variation in survival from ultraviolet radiation in Chlamydomonas reinhardtii. Photochem Photobiol 71: 758–765.

133. FabregasJ, MasedaA, DominguezA, FerreiraM, OteroA (2002) Changes in the cell composition of the marine microalga,Nannochloropsis gaditana, during a light:dark cycle. Biotechnol Lett 24: 1699–1703.

134. ZhangEE, KaySA (2010) Clocks not winding down: unravelling circadian networks. Nat Rev Mol Cell Biol 11: 764–776.

135. MonteE, Al-SadyB, LeivarP, QuailPH (2007) Out of the dark: how the PIFs are unmasking a dual temporal mechanism of phytochrome signalling. J Exp Bot 58: 3125–3133.

136. StrayerC, OyamaT, SchultzTF, RamanR, SomersDE, et al. (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289: 768–771.

137. SerranoG, Herrera-PalauR, RomeroJM, SerranoA, CouplandG, et al. (2009) Chlamydomonas CONSTANS and the evolution of plant photoperiodic signaling. Curr Biol 19: 359–368.

138. Perez-RuedaE, Collado-VidesJ (2000) The repertoire of DNA-binding transcriptional regulators in Escherichia coli K-12. Nucleic Acids Res 28: 1838–1847.

139. CherryJM, AdlerC, BallC, ChervitzSA, DwightSS, et al. (1998) SGD: Saccharomyces Genome Database. Nucleic Acids Res 26: 73–79.

140. Reece-HoyesJS, DeplanckeB, ShinglesJ, GroveCA, HopeIA, et al. (2005) A compendium of Caenorhabditis elegans regulatory transcription factors: a resource for mapping transcription regulatory networks. Genome Biol 6: R110.

141. AdryanB, TeichmannSA (2006) FlyTF: a systematic review of site-specific transcription factors in the fruit fly Drosophila melanogaster. Bioinformatics 22: 1532–1533.

142. RiechmannJL, HeardJ, MartinG, ReuberL, JiangC, et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105–2110.

143. RiechmannJL, RatcliffeOJ (2000) A genomic perspective on plant transcription factors. Curr Opin Plant Biol 3: 423–434.

144. GrayPA, FuH, LuoP, ZhaoQ, YuJ, et al. (2004) Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 306: 2255–2257.

145. VaquerizasJM, KummerfeldSK, TeichmannSA, LuscombeNM (2009) A census of human transcription factors: function, expression and evolution. Nat Rev Genet 10: 252–263.

146. Riano-PachonDM, RuzicicS, DreyerI, Mueller-RoeberB (2007) PlnTFDB: an integrative plant transcription factor database. BMC Bioinformatics 8: 42.

147. ZhangH, JinJ, TangL, ZhaoY, GuX, et al. (2011) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39: D1114–1117.

148. JinH, MartinC (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41: 577–585.

149. YanhuiC, XiaoyuanY, KunH, MeihuaL, JigangL, et al. (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60: 107–124.

150. BraunEL, GrotewoldE (1999) Newly discovered plant c-myb-like genes rewrite the evolution of the plant myb gene family. Plant Physiol 121: 21–24.

151. KranzH, ScholzK, WeisshaarB (2000) c-MYB oncogene-like genes encoding three MYB repeats occur in all major plant lineages. Plant J 21: 231–235.

152. Riano-PachonDM, CorreaLG, Trejos-EspinosaR, Mueller-RoeberB (2008) Green transcription factors: a Chlamydomonas overview. Genetics 179: 31–39.

153. StrackeR, WerberM, WeisshaarB (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4: 447–456.

154. BouhoucheN, SyvanenM, KadoCI (2000) The origin of prokaryotic C2H2 zinc finger regulators. Trends Microbiol 8: 77–81.

155. SchroederA, MuellerO, StockerS, SalowskyR, LeiberM, et al. (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7: 3.

156. ZerbinoDR, BirneyE (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.

157. WuTD, WatanabeCK (2005) GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21: 1859–1875.

158. SommerDD, DelcherAL, SalzbergSL, PopM (2007) Minimus: a fast, lightweight genome assembler. BMC Bioinformatics 8: 64.

159. AltschulSF, MaddenTL, SchäfferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.

160. KemenE, GardinerA, Schultz-LarsenT, KemenAC, BalmuthAL, et al. (2011) Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol 9: e1001094 doi:10.1371/journal.pbio.1001094.

161. LevesqueCA, BrouwerH, CanoL, HamiltonJP, HoltC, et al. (2010) Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11: R73.

162. TylerBM, TripathyS, ZhangX, DehalP, JiangRH, et al. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261–1266.

163. TrapnellC, WilliamsBA, PerteaG, MortazaviA, KwanG, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511–515.

164. KorfI (2004) Gene finding in novel genomes. BMC Bioinformatics 5: 59.

165. StankeM, WaackS (2003) Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19Suppl 2: ii215–225.

166. FinnRD, MistryJ, TateJ, CoggillP, HegerA, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211–222.

167. QuevillonE, SilventoinenV, PillaiS, HarteN, MulderN, et al. (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33: W116–120.

168. LiL, StoeckertCJJr, RoosDS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189.

169. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.

170. BaoZ, EddySR (2002) Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res 12: 1269–1276.

171. WickerT, SabotF, Hua-VanA, BennetzenJL, CapyP, et al. (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8: 973–982.

172. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.

173. FolchJ, LeesM, Sloane StanleyGH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497–509.

174. CastruitaM, CaseroD, KarpowiczSJ, KropatJ, VielerA, et al. (2011) Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 23: 1273–1292.

175. CornishAJ, GartnerK, YangH, PetersJW, HeggEL (2011) Mechanism of proton transfer in [FeFe]-hydrogenase from Clostridium pasteurianum. J Biol Chem 286: 38341–38347.

176. CavalierDM, LerouxelO, NeumetzlerL, YamauchiK, ReineckeA, et al. (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20: 1519–1537.

177. FawleyKP, FawleyMW (2007) Observations on the diversity and ecology of freshwater Nannochloropsis (Eustigmatophyceae), with descriptions of new taxa. Protist 158: 325–336.