Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes

BMC Evolutionary Biology

Volumn 8, Issue 1, 2008, Pages

  Maruyama, Shinichiro ^a   Misawa, Kazuharu ^a,c   Iseki, Mineo ^b   Watanabe, Masakatsu ^b   Nozaki, Hisayoshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOGLUCONATE DEHYDROGENASE; COMPLEMENTARY DNA;

ALGAL GENETICS; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; CYANOBACTERIUM; ENDOSYMBIOSIS; EUGLENA; EUKARYOTE; GENE SEQUENCE; GND GENE; HORIZONTAL GENE TRANSFER; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASTID; RED ALGA; STATISTICAL ANALYSIS; BACTERIAL GENOME; BAYES THEOREM; ENZYMOLOGY; GENE LIBRARY; GENETICS; GENOME; GREEN ALGA; MOLECULAR EVOLUTION; PLANT; POLYMERASE CHAIN REACTION; STATISTICAL MODEL;

ALGAE; CYANOBACTERIA; DIPLONEMA; EUGLENIDA; EUKARYOTA; EXCAVATA; FUNGI/METAZOA GROUP; GLAUCOCYSTOPHYCEAE; HETEROLOBOSEA; PROTISTA; RHODOPHYTA; STRAMENOPILES;

ALGAE, GREEN; ALGAE, RED; BAYES THEOREM; CYANOBACTERIA; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GENE LIBRARY; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; GENOME, PLANT; LIKELIHOOD FUNCTIONS; PHOSPHOGLUCONATE DEHYDROGENASE; PHYLOGENY; PLANTS; PLASTIDS; POLYMERASE CHAIN REACTION;

EID: 44949146132     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-8-151     Document Type: Article

References (55)

1. Principles of Protein and Lipid Targeting in Secondary Symbiogenesis: Euglenoid, Dinoflagellate, and Sporozoan Plastid Origins and the Eukaryote Family Tree. T Cavalier-Smith, J Eukaryot Microbiol 1999 46 347 366 10.1111/j.1550-7408.1999.tb04614.x 18092388
2. The Origin and Establishment of the Plastid in Algae and Plants. A Reyes-Prieto AP Weber D Bhattacharya, Annu Rev Genet 2007 41 147 168 10.1146/annurev.genet.41.110306.130134 17600460
3. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. SM Adl AG Simpson MA Farmer RA Andersen OR Anderson JR Barta SS Bowser G Brugerolle RA Fensome S Fredericq TY James S Karpov P Kugrens J Krug CE Lane LA Lewis J Lodge DH Lynn DG Mann RM McCourt L Mendoza O Moestrup SE Mozley-Standridge TA Nerad CA Shearer AV Smirnov FW Spiegel MF Taylor, J Eukaryot Microbiol 2005 52 399 451 10.1111/j.1550-7408.2005.00053.x 16248873
4. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. W Martin T Rujan E Richly A Hansen S Cornelsen T Lins D Leister B Stoebe M Hasegawa D Penny, Proc Natl Acad Sci USA 2002 99 12246 12251 12218172 10.1073/pnas.182432999
5. Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. A Reyes-Prieto JD Hackett MB Soares MF Bonaldo D Bhattacharya, Curr Biol 2006 16 2320 2325 10.1016/j.cub.2006.09.063 17141613
6. Mass identification of chloroplast proteins of endosymbiont origin by phylogenetic profiling based on organism-optimized homologous protein groups. N Sato M Ishikawa M Fujiwara K Sonoike, Genome inform 2005 16 56 68 16901089
7. Do plastid-related characters support the chromalveolate hypothesis? A Bodyl, J Phycol 2005 41 712 719 10.1111/j.1529-8817.2005.00091.x
8. Did trypanosomatid parasites have photosynthetic ancestors? BS Leander, Trends Microbiol 2004 12 251 258 10.1016/j.tim.2004.04.001 15165602
9. The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. MB Rogers PR Gilson V Su GI McFadden PJ Keeling, Mol Biol Evol 2007 24 54 62 10.1093/molbev/msl129 16990439
10. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. EV Armbrust JA Berges C Bowler BR Green D Martinez NH Putnam S Zhou AE Allen KE Apt M Bechner MA Brzezinski BK Chaal A Chiovitti AK Davis MS Demarest JC Detter T Glavina D Goodstein MZ Hadi U Hellsten M Hildebrand BD Jenkins J Jurka VV Kapitonov N Kröger WW Lau TW Lane FW Larimer JC Lippmeier S Lucas M Medina A Montsant M Obornik MS Parker B Palenik GJ Pazour PM Richardson TA Rynearson MA Saito DC Schwartz K Thamatrakoln K Valentin A Vardi FP Wilkerson DS Rokhsar, Science 2004 306 79 86 10.1126/science.1101156 15459382
11. The highly reduced genome of an enslaved algal nucleus. S Douglas S Zauner M Fraunholz M Beaton S Penny LT Deng X Wu M Reith T Cavalier-Smith UG Maier, Nature 2001 410 1091 1096 10.1038/35074092 11323671
12. Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature's smallest nucleus. PR Gilson V Su CH Slamovits ME Reith PJ Keeling GI McFadden, Proc Natl Acad Sci USA 2006 103 9566 9571 16760254 10.1073/pnas.0600707103
13. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. BM Tyler S Tripathy X Zhang P Dehal RH Jiang A Aerts FD Arredondo L Baxter D Bensasson JL Beynon J Chapman CM Damasceno AE Dorrance D Dou AW Dickerman IL Dubchak M Garbelotto M Gijzen SG Gordon F Govers NJ Grunwald W Huang KL Ivors RW Jones S Kamoun K Krampis KH Lamour MK Lee WH McDonald M Medina HJ Meijer EK Nordberg DJ Maclean MD Ospina-Giraldo PF Morris V Phuntumart NH Putnam S Rash JK Rose Y Sakihama AA Salamov A Savidor CF Scheuring BM Smith BW Sobral A Terry TA Torto-Alalibo J Win Z Xu H Zhang IV Grigoriev DS Rokhsar JL Boore, Science 2006 313 1261 1266 10.1126/science.1128796 16946064
14. Unique phylogenetic relationships of glucokinase and glucosephosphate isomerase of the amitochondriate eukaryotes Giardia intestinalis, Spironucleus barkhanus and Trichomonas vaginalis. K Henze DS Horner S Suguri DV Moore LB Sánchez M Müller TM Embley, Gene 2001 281 123 131 10.1016/S0378-1119(01)00773-9 11750134
15. A cyanobacterial gene in nonphotosynthetic protists - an early chloroplast acquisition in eukaryotes? JO Andersson AJ Roger, Curr Biol 2002 12 115 119 10.1016/S0960-9822(01)00649-2 11818061
16. Cyanobacterial genes transmitted to the nucleus before divergence of red algae in the Chromista. H Nozaki M Matsuzaki O Misumi H Kuroiwa M Hasegawa T Higashiyama T Shin-I Y Kohara N Ogasawara T Kuroiwa, J Mol Evol 2004 59 103 113 10.1007/s00239-003-2611-1 15383913
17. Purification and cloning of chloroplast 6-phosphogluconate dehydrogenase from spinach. Cyanobacterial genes for chloroplast and cytosolic isoenzymes encoded in eukaryotic chromosomes. K Krepinsky M Plaumann W Martin C Schnarrenberger, Eur J Biochem 2001 268 2678 2686 10.1046/j.1432-1327.2001. 02154.x 11322889
18. Discovery of signaling effect of UV-B/C light in the extended UV-A/blue-type action spectra for step-down and step-up photophobic responses in the unicellular flagellate alga Euglena gracilis. S Matsunaga T Hori T Takahashi M Kubota M Watanabe K Okamoto K Masuda M Sugai, Protoplasma 1998 201 45 52 10.1007/BF01280710
19. Phylogeny of primary photosynthetic eukaryotes as deduced from slowly evolving nuclear genes. H Nozaki M Iseki M Hasegawa K Misawa T Nakada N Sasaki M Watanabe, Mol Biol Evol 2007 24 1592 1595 10.1093/molbev/msm091 17488739
20. Amitochondriate amoebae and the evolution of DNA-dependent RNA polymerase II. JW Stiller EC Duffield BD Hall, Proc Natl Acad Sci USA 1998 95 11769 11774 9751740 10.1073/pnas.95.20.11769
21. Are red algae plants? A critical evaluation of three key molecular data sets. JW Stiller J Riley BD Hall, J Mol Evol 2001 52 527 539 11443356
22. The Galdieria sulphuraria genome database. http://genomics.msu.edu/ galdieria/index.html
23. The Joint Genome Institute. http://www.jgi.doe.gov/
24. The taxonomically broad EST database TBestDB. http://tbestdb.bcm. umontreal.ca/
25. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins, Nucleic Acids Res 1997 25 4876 4882 9396791 10.1093/nar/25.24.4876
26. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. N Galtier M Gouy C Gautier, Comput Appl Biosci 1996 12 543 548 9021275
27. MRBAYES: Bayesian inference of phylogenetic trees. JP Huelsenbeck F Ronquist, Bioinformatics 2001 17 754 755 10.1093/bioinformatics/17.8.754 11524383
28. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. S Guindon O Gascuel, Syst Biol 2003 52 696 704 10.1080/10635150390235520 14530136
29. PAUP* Phylogenetic Analysis Using Parsimony, Version 4.0b10. DL Swofford, Sinauer Associates, Sunderland, MA 2002 12504223
30. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. HA Schmidt K Strimmer M Vingron A von Haeseler, Bioinformatics 2002 18 502 504 10.1093/bioinformatics/18.3.502 11934758
31. CONSEL: for assessing the confidence of phylogenetic tree selection. H Shimodaira M Hasegawa, Bioinformatics 2001 17 1246 1247 10.1093/bioinformatics/ 17.12.1246 11751242
32. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. H Kishino M Hasegawa, J Mol Evol 1989 29 170 179 10.1007/BF02100115 2509717
33. Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. H Kishino T Miyata M Hasegawa, Journal of Molecular Evolution 1990 31 151 160 10.1007/BF02109483
34. Rooting the eukaryote tree by using a derived gene fusion. A Stechmann T Cavalier-Smith, Science 2002 297 89 91 10.1126/science.1071196 12098695
35. The excavate protozoan phyla Metamonada Grassé emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa. T Cavalier-Smith, Int J Syst Evol Microbiol 2003 53 1741 1758 10.1099/ijs.0.02548- 0 14657102
36. The deep roots of eukaryotes. SL Baldauf, Science 2003 300 1703 1706 10.1126/science.1085544 12805537
37. Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of "primitive" eukaryotes. AG Simpson Y Inagaki AJ Roger, Mol Biol Evol 2006 23 615 625 10.1093/molbev/msj068 16308337
38. Phylogeny of Nuclear-Encoded Plastid-Targeted Proteins Supports an Early Divergence of Glaucophytes within Plantae. A Reyes-Prieto D Bhattacharya, Mol Biol Evol 2007 24 2358 2361 10.1093/molbev/msm186 17827169
39. A "green" phosphoribulokinase in complex algae with red plastids: evidence for a single secondary endosymbiosis leading to haptophytes, cryptophytes, heterokonts, and dinoflagellates. J Petersen R Teich H Brinkmann R Cerff, J Mol Evol 2006 62 143 157 10.1007/s00239-004-0305-3 16474987
40. Origin and distribution of Calvin cycle fructose and sedoheptulose bisphosphatases in plantae and complex algae: a single secondary origin of complex red plastids and subsequent propagation via tertiary endosymbioses. R Teich S Zauner D Baurain H Brinkmann J Petersen, Protist 2007 158 263 276 10.1016/j.protis.2006.12.004 17368985
41. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. JM Archibald MB Rogers M Toop K Ishida PJ Keeling, Proc Natl Acad Sci USA 2003 100 7678 7683 12777624 10.1073/pnas.1230951100
42. Lateral gene transfer of a multigene region from cyanobacteria to dinoflagellates resulting in a novel plastid-targeted fusion protein. RF Waller CH Slamovits PJ Keeling, Mol Biol Evol 2006 23 1437 1443 10.1093/molbev/msl008 16675503
43. The ancestor of the Paulinella chromatophore obtained a carboxysomal operon by horizontal gene transfer from a Nitrococcus-like γ- proteobacterium. B Marin EC Nowack G Glöckner M Melkonian, BMC Evol Biol 2007 7 85 17550603 10.1186/1471-2148-7-85
44. Horizontal gene transfer in chromalveolates. T Nosenko D Bhattacharya, BMC Evol Biol 2007 7 173 17894863 10.1186/1471-2148-7-173
45. Toward resolving the eukaryotic tree: the phylogenetic positions of jakobids and cercozoans. N Rodríguez-Ezpeleta H Brinkmann G Burger AJ Roger MW Gray H Philippe BF Lang, Curr Biol 2007 17 1420 1425 10.1016/j.cub.2007.07.036 17689961
46. Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. JD Hackett HS Yoon S Li A Reyes-Prieto SE Rümmele D Bhattacharya, Mol Biol Evol 2007 24 1702 1713 10.1093/molbev/msm089 17488740
47. Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. NJ Patron Y Inagaki PJ Keeling, Curr Biol 2007 17 887 891 10.1016/j.cub.2007.03.069 17462896
48. Phylogenomics reshuffles the eukaryotic supergroups. F Burki K Shalchian-Tabrizi M Minge A Skjaeveland SI Nikolaev KS Jakobsen J Pawlowski, PLoS ONE 2007 2 e790 17726520 10.1371/journal.pone.0000790
49. Broadly sampled multigene trees of eukaryotes. HS Yoon J Grant YI Tekle M Wu BC Chaon JC Cole JM Logsdon DJ Patterson D Bhattacharya LA Katz, BMC Evol Biol 2008 8 14 18205932 10.1186/1471-2148-8-14
50. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. M Matsuzaki O Misumi T Shin-I S Maruyama M Takahara SY Miyagishima T Mori K Nishida F Yagisawa K Nishida Y Yoshida Y Nishimura S Nakao T Kobayashi Y Momoyama T Higashiyama A Minoda M Sano H Nomoto K Oishi H Hayashi F Ohta S Nishizaka S Haga S Miura T Morishita Y Kabeya K Terasawa Y Suzuki Y Ishii S Asakawa H Takano N Ohta H Kuroiwa K Tanaka N Shimizu S Sugano N Sato H Nozaki N Ogasawara Y Kohara T Kuroiwa, Nature 2004 428 653 657 10.1038/nature02398 15071595
51. Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane-derived ancestor. AP Weber M Linka D Bhattacharya, Eukaryotic Cell 2006 5 609 612 16524915 10.1128/EC.5.3.609-612.2006
52. Phylogeny of Calvin cycle enzymes supports Plantae monophyly. A Reyes-Prieto D Bhattacharya, Mol Phylogenet Evol 2007 45 384 391 10.1016/j.ympev.2007.02.026 17482838
53. Shopping for plastids. AW Larkum PJ Lockhart CJ Howe, Trends Plant Sci 2007 12 189 195 10.1016/j.tplants.2007.03.011 17416546
54. Plastid endosymbiosis, genome evolution and the origin of green plants. JW Stiller, Trends Plant Sci 2007 12 391 396 10.1016/j.tplants.2007.08.002 17698402
55. The Toxoplasma gondii Genome resource ToxoDB. http://toxodb.org/toxo/ home.jsp