Genome-wide functional annotation and structural verification of metabolic ORFeome of Chlamydomonas reinhardtii

BMC Genomics

Volumn 12, Issue SUPPL. 1, 2011, Pages

  Ghamsari, Lila ^a,b   Balaji, Santhanam ^a,b   Shen, Yun ^a,b   Yang, Xinping ^a,b   Balcha, Dawit ^a,b   Fan, Changyu ^a,b   Hao, Tong ^a,b   Yu, Haiyuan ^c   Papin, Jason A ^d   Salehi Ashtiani, Kourosh ^a,b,e,f  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c School of Integrative Plant Sciences   (United States)

^d University of Virginia   (United States)

^e NEW YORK UNIVERSITY ABU DHABI   (United Arab Emirates)

^f NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOINFORMATICS; CELLULAR DISTRIBUTION; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CYTOSOL; GENE CLUSTER; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE SEQUENCE; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC DATABASE; GENETIC TRANSCRIPTION; GENOMICS; GENOTYPE PHENOTYPE CORRELATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; GENETICS; METABOLISM; PLANT GENOME;

ALGAE; CHLAMYDOMONAS REINHARDTII;

ENZYME; VEGETABLE PROTEIN;

CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; CLONING, MOLECULAR; CYTOSOL; DATABASES, GENETIC; ENZYMES; GENOME, PLANT; OPEN READING FRAMES; PLANT PROTEINS;

EID: 79958821230     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-S1-S4     Document Type: Article

References (44)

1. Galperin MY, Koonin EV. From complete genome sequence to 'complete' understanding?. Trends Biotechnol 2010, 28(8):398-406. 10.1016/j.tibtech.2010.05.006, 3065831, 20647113.
2. Oberhardt MA, Palsson B, Papin JA. Applications of genome-scale metabolic reconstructions. Mol Syst Biol 2009, 5:320. 2795471, 19888215.
3. Park JH, Lee SY. Towards systems metabolic engineering of microorganisms for amino acid production. Curr Opin Biotechnol 2008, 19(5):454-460. 10.1016/j.copbio.2008.08.007, 18760356.
4. Schmidt BJ, Lin-Schmidt X, Chamberlin A, Salehi-Ashtiani K, Papin JA. Metabolic systems analysis to advance algal biotechnology. Biotechnol J 2010, 5(7):660-670. 10.1002/biot.201000129, 20665641.
5. Li Y, Han D, Hu G, Sommerfeld M, Hu Q. Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii. Biotechnol Bioeng 2010, 107(2):258-268. 10.1002/bit.22807, 20506159.
6. Boyle NR, Morgan JA. Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii. BMC Syst Biol 2009, 3:4. 2628641, 19128495.
7. Rupprecht J. From systems biology to fuel--Chlamydomonas reinhardtii as a model for a systems biology approach to improve biohydrogen production. J Biotechnol 2009, 142(1):10-20. 10.1016/j.jbiotec.2009.02.008, 19480943.
8. Kruse O, Rupprecht J, Bader KP, Thomas-Hall S, Schenk PM, Finazzi G, Hankamer B. Improved photobiological H2 production in engineered green algal cells. J Biol Chem 2005, 280(40):34170-34177. 10.1074/jbc.M503840200, 16100118.
9. Jans F, Mignolet E, Houyoux PA, Cardol P, Ghysels B, Cuine S, Cournac L, Peltier G, Remacle C, Franck F. A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci U S A 2008, 105(51):20546-20551. 10.1073/pnas.0806896105, 2629347, 19074271.
10. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernández E, Fukuzawa H, González-Ballester D, González-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riaño-Pachón DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martínez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 2007, 318(5848):245-250. 10.1126/science.1143609, 2875087, 17932292.
11. Mao X, Cai T, Olyarchuk JG, Wei L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 2005, 21(19):3787-3793. 10.1093/bioinformatics/bti430, 15817693.
12. Wortman JR, Haas BJ, Hannick LI, Smith RK, Maiti R, Ronning CM, Chan AP, Yu C, Ayele M, Whitelaw CA, White OR, Town CD. Annotation of the Arabidopsis genome. Plant Physiol 2003, 132(2):461-468. 10.1104/pp.103.022251, 166989, 12805579.
13. Hillier LW, Reinke V, Green P, Hirst M, Marra MA, Waterston RH. Massively parallel sequencing of the polyadenylated transcriptome of C. elegans. Genome Res 2009, 19(4):657-666. 10.1101/gr.088112.108, 2665784, 19181841.
14. Salehi-Ashtiani K, Lin C, Hao T, Shen Y, Szeto D, Yang X, Ghamsari L, Lee H, Fan C, Murray RR, Milstein S, Svrzikapa N, Cusick ME, Roth FP, Hill DE, Vidal M. Large-scale RACE approach for proactive experimental definition of C. elegans ORFeome. Genome Res 2009, 19(12):2334-2342. 10.1101/gr.098640.109, 2792173, 19801531.
15. Eberhard S, Jain M, Im CS, Pollock S, Shrager J, Lin Y, Peek AS, Grossman AR. Generation of an oligonucleotide array for analysis of gene expression in Chlamydomonas reinhardtii. Curr Genet 2006, 49(2):106-124. 10.1007/s00294-005-0041-2, 16333659.
16. Nguyen AV, Thomas-Hall SR, Malnoë A, Timmins M, Mussgnug JH, Rupprecht J, Kruse O, Hankamer B, Schenk PM. Transcriptome for photobiological hydrogen production induced by sulfur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot Cell 2008, 7(11):1965-1979. 10.1128/EC.00418-07, 2583537, 18708561.
17. May P, Wienkoop S, Kempa S, Usadel B, Christian N, Rupprecht J, Weiss J, Recuenco-Munoz L, Ebenhöh O, Weckwerth W, Walther D. Metabolomics- and proteomics-assisted genome annotation and analysis of the draft metabolic network of Chlamydomonas reinhardtii. Genetics 2008, 179(1):157-166. 10.1534/genetics.108.088336, 2390595, 18493048.
18. González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR. RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 2010, 22(6):2058-2084. 10.1105/tpc.109.071167, 20587772.
19. Manichaikul A, Ghamsari L, Hom EF, Lin C, Murray RR, Chang RL, Balaji S, Hao T, Shen Y, Chavali AK, Thiele I, Yang X, Fan C, Mello E, Hill DE, Vidal M, Salehi-Ashtiani K, Papin JA. Metabolic network analysis integrated with transcript verification for sequenced genomes. Nat Methods 2009, 6(8):589-592. 10.1038/nmeth.1348, 19597503.
20. Apweiler R, Bairoch A, Wu CH. Protein sequence databases. Chem Biol 2004, 8(1):76-80.
21. Mueller L, Zhang P, Rhee SY. AraCyc: a biochemical pathway database for Arabidopsis. Plant Physiol 2003, 132(2):453-460. 10.1104/pp.102.017236, 166988, 12805578.
22. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. WoLF PSORT: protein localization predictor. Nucleic Acids Res 2007, 35(Web Server issue):W585-587. 1933216, 17517783.
23. Nakai K, Horton P. PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 1999, 24(1):34-36. 10.1016/S0968-0004(98)01336-X, 10087920.
24. Nakai K, Kanehisa M. A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 1992, 14(4):897-911. 10.1016/S0888-7543(05)80111-9, 1478671.
25. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 2002, 18(2):298-305. 10.1093/bioinformatics/18.2.298, 11847077.
26. Casadio R, Martelli PL, Pierleoni A. The prediction of protein subcellular localization from sequence: a shortcut to functional genome annotation. Brief Funct Genomic Proteomic 2008, 7(1):63-73. 10.1093/bfgp/eln003, 18283051.
27. Reinhardt A, Hubbard T. Using neural networks for prediction of the subcellular location of proteins. Nucleic Acids Res 1998, 26(9):2230-2236. 10.1093/nar/26.9.2230, 147531, 9547285.
28. Blum T, Briesemeister S, Kohlbacher O. MultiLoc2: integrating phylogeny and Gene Ontology terms improves subcellular protein localization prediction. BMC Bioinformatics 2009, 10:274. 10.1186/1471-2105-10-274, 2745392, 19723330.
29. Wienkoop S, Weiss J, May P, Kempa S, Irgang S, Recuenco-Munoz L, Pietzke M, Schwemmer T, Rupprecht J, Egelhofer V, Weckwerth W. Targeted proteomics for Chlamydomonas reinhardtii combined with rapid subcellular protein fractionation, metabolomics and metabolic flux analyses. Mol Biosyst 2010, 6(6):1018-1031. 10.1039/b920913a, 20358043.
30. Voss H, Schwager C, Wiemann S, Zimmermann J, Stegemann J, Erfle H, Voie AM, Drzonek H, Ansorge W. Efficient low redundancy large-scale DNA sequencing at EMBL. J Biotechnol 1995, 41(2-3):121-129. 10.1016/0168-1656(95)00007-D, 7654345.
31. Djebali S, Kapranov P, Foissac S, Lagarde J, Reymond A, Ucla C, Wyss C, Drenkow J, Dumais E, Murray RR, Lin C, Szeto D, Denoeud F, Calvo M, Frankish A, Harrow J, Makrythanasis P, Vidal M, Salehi-Ashtiani K, Antonarakis SE, Gingeras TR, Guigó R. Efficient targeted transcript discovery via array-based normalization of RACE libraries. Nat Methods 2008, 5(7):629-635. 10.1038/nmeth.1216, 2713501, 18500348.
32. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5(7):621-628. 10.1038/nmeth.1226, 18516045.
33. Shiraki T, Kondo S, Katayama S, Waki K, Kasukawa T, Kawaji H, Kodzius R, Watahiki A, Nakamura M, Arakawa T, Fukuda S, Sasaki D, Podhajska A, Harbers M, Kawai J, Carninci P, Hayashizaki Y. Cap analysis gene expression for high-throughput analysis of transcriptional starting point and identification of promoter usage. Proc Natl Acad Sci USA 2003, 100(26):15776-15781. 10.1073/pnas.2136655100, 307644, 14663149.
34. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW. Serial analysis of gene expression. Science 1995, 270(5235):484-487. 10.1126/science.270.5235.484, 7570003.
35. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kröger N, Kroth PG, La Roche J, Lindquist E, Lommer M, Martin-Jézéquel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Oudot-Le Secq MP, Napoli C, Obornik M, Parker MS, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, Van de Peer Y, Grigoriev IV. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 2008, 456(7219):239-234. 10.1038/nature07410, 18923393.
36. Palenik B, Grimwood J, Aerts A, Rouzé P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, Zhou K, Otillar R, Merchant SS, Podell S, Gaasterland T, Napoli C, Gendler K, Manuell A, Tai V, Vallon O, Piganeau G, Jancek S, Heijde M, Jabbari K, Bowler C, Lohr M, Robbens S, Werner G, Dubchak I, Pazour GJ, Ren Q, Paulsen I, Delwiche C, Schmutz J, Rokhsar D, Van de Peer Y, Moreau H, Grigoriev IV. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci USA 2007, 104(18):7705-7710. 10.1073/pnas.0611046104, 1863510, 17460045.
37. Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, Chapman J, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E, Lucas S, Grigoriev IV, Schmitt R, Kirk D, Rokhsar DS. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 2010, 329(5988):223-226. 10.1126/science.1188800, 2993248, 20616280.
38. Madan Babu M, Balaji S, Aravind L. General trends in the evolution of prokaryotic transcriptional regulatory networks. Genome Dyn 2007, 3:66-80.
39. Balaji S, Babu MM, Aravind L. Interplay between network structures, regulatory modes and sensing mechanisms of transcription factors in the transcriptional regulatory network of E. coli. J Mol Biol 2007, 372(4):1108-1122. 10.1016/j.jmb.2007.06.084, 2422858, 17706247.
40. Hillier L, Green P. OSP: a computer program for choosing PCR and DNA sequencing primers. PCR Methods Appl 1991, 1(2):124-128.
41. Walhout AJ, Temple GF, Brasch MA, Hartley JL, Lorson MA, van den Heuvel S, Vidal M. GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol 2000, 328:575-592.
42. Reboul J, Vaglio P, Tzellas N, Thierry-Mieg N, Moore T, Jackson C, Shin-i T, Kohara Y, Thierry-Mieg D, Thierry-Mieg J, Lee H, Hitti J, Doucette-Stamm L, Hartley JL, Temple GF, Brasch MA, Vandenhaute J, Lamesch PE, Hill DE, Vidal M. Open-reading-frame sequence tags (OSTs) support the existence of at least 17,300 genes in C. elegans. Nat Genet 2001, 27(3):332-336. 10.1038/85913, 11242119.
43. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113. 10.1186/1471-2105-5-113, 517706, 15318951.
44. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797. 10.1093/nar/gkh340, 390337, 15034147.