Does the Cyanophora paradoxa genome revise our view on the evolution of photorespiratory enzymes?

Plant Biology

Volumn 15, Issue 4, 2013, Pages 759-768

  Kern, R ^a   Eisenhut, M ^b   Bauwe, H ^a   Weber, A P M ^b   Hagemann, M ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Cyanobacteria; Cyanophora; Eukaryotic algae; Evolution; Photorespiration

Indexed keywords

ALCOHOL DEHYDROGENASE; AMINOTRANSFERASE; CARBON DIOXIDE; GLYOXYLATE AMINOTRANSFERASE; HYDROXY ACID OXIDASE A; HYDROXYPYRUVATE REDUCTASE; OXYGEN; PHOSPHATASE; PHOSPHOGLYCOLATE PHOSPHATASE; PLANT DNA; RIBOSOME DNA; RNA 16S; VEGETABLE PROTEIN;

ALGA; CYANOBACTERIUM; ENDOSYMBIONT; ENZYME ACTIVITY; EUKARYOTE; EVOLUTIONARY BIOLOGY; GENOME; GENOMICS; PHOTOAUTOTROPHY; PHOTOSYNTHESIS; PHYLOGENY; RESPIRATION;

ARTICLE; CELL RESPIRATION; CHEMISTRY; CYANOBACTERIUM; CYANOPHORA; DNA SEQUENCE; ENZYMOLOGY; EUKARYOTE; EVOLUTION; GENETICS; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYLOGENY; PLANT GENOME; RADIATION EXPOSURE; SYMBIOSIS;

ALCOHOL OXIDOREDUCTASES; BIOLOGICAL EVOLUTION; CARBON DIOXIDE; CELL RESPIRATION; CYANOBACTERIA; CYANOPHORA; DNA, PLANT; DNA, RIBOSOMAL; EUKARYOTA; GENOME, PLANT; HYDROXYPYRUVATE REDUCTASE; LIGHT; OXYGEN; PHOSPHORIC MONOESTER HYDROLASES; PHOTOSYNTHESIS; PHYLOGENY; PLANT PROTEINS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS; TRANSAMINASES;

ALGAE; CYANOBACTERIA; CYANOPHORA; CYANOPHORA PARADOXA; EMBRYOPHYTA; EUKARYOTA; GLAUCOCYSTOPHYCEAE; PROTEOBACTERIA;

EID: 84879498786     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/plb.12003     Document Type: Article

References (47)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
2. 2 concentrating mechanisms in cyanobacteria. Functional Plant Biology, 29, 161-173.
3. Bartsch O., Hagemann M., Bauwe H. (2008) Only plant-type (GLYK) glycerate kinases produce D-glycerate 3-phosphate. FEBS Letters, 582, 3025-3028.
4. Bauwe H., Hagemann M., Fernie A.R. (2010) Photorespiration: players, partners and origin. Trends in Plant Sciences, 15, 330-336.
5. Bauwe H., Hagemann M., Kern R., Timm S. (2012) Photorespiration has a dual origin and manifold links to central metabolism. Current Opinion in Plant Biology, 15, 269-275.
6. Blankenship R.E., Hartman H. (1998) The origin and evolution of oxygenic photosynthesis. Trends in Biochemical Sciences, 23, 94-97.
7. Boldt R., Edner C., Kolukisaoglu U., Hagemann M., Weckwerth W., Wienkoop S., Morgenthal K., Bauwe H. (2005) D-GLYCERATE 3-KINASE, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. The Plant Cell, 17, 2413-2420.
8. Burki F., Shalchian-Tabrizi K., Pawlowski J. (2008) Phylogenomics reveals a new 'megagroup' including most photosynthetic eukaryotes. Biology Letters, 4, 366-369.
9. Castresana J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540-552.
10. Colman B. (1989) Photosynthetic carbon assimilation and the suppression of photorespiration in the cyanobacteria. Aquatic Botany, 34, 211-231.
11. Delwiche C.F., Palmer J.D. (1996) Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Molecular Biology and Evolution, 13, 873-882.
12. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.F., Guindon S., Lefort V., Lescot M., Claverie J.M., Gascuel O. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research, 36, W465-W469.
13. Deusch O., Landan G., Roettger M., Gruenheit N., Kowallik K.V., Allen J.F., Martin W., Dagan T. (2008) Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Molecular Biology and Evolution, 25, 748-761.
14. Edgar R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797.
15. 2 glycolate cycle and the bacterial-like glycerate pathway cooperate in phosphoglycolate metabolism in cyanobacteria. Plant Physiology, 142, 333-342.
16. Eisenhut M., Ruth W., Haimovich M., Bauwe H., Kaplan A., Hagemann M. (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proceedings of the National Academy of Sciences USA, 105, 17199-17204.
17. Gupta R.S., Mathews D.W. (2010) Signature proteins for the major clades of cyanobacteria. BMC Evolutionary Biology, 10, 24.
18. 2 fixation and evolved into photorespiratory glycolate oxidases in plants. The Plant Cell, 23, 2978-2990.
19. 2 cycle. Plant Biology, 15, 639-647.
20. Hess W.R., Rocap G., Ting C.S., Larimer F., Stilwagen S., Lamerdin J., Chisholm S.W. (2001) The photosynthetic apparatus of Prochlorococcus: insights through comparative genomics. Photosynthesis Research, 70, 53-71.
21. Igamberdiev A.U., Lea P.J. (2002) The role of peroxisomes in the integration of metabolism and evolutionary diversity of photosynthetic organisms. Phytochemistry, 60, 651-674.
22. Janoušíkovec N., Horák A., Oborník M., Lukeš J., Keeling P.J. (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proceedings of the National Academy of Sciences USA, 107, 10949-10954.
23. Keeling P.J. (2004) Diversity and evolutionary history of plastids and their hosts. American Journal of Botany, 91, 1481-1493.
24. Kehlenbeck P., Goyal A., Tolbert N.E. (1995) Factors affecting development of peroxisomes and glycolate metabolism among algae of different evolutionary lines of the Prasinophyceae. Plant Physiology, 109, 1363-1370.
25. Kern R., Bauwe H., Hagemann M. (2011) Evolution of enzymes involved in the photorespiratory 2-phosphoglycolate cycle from cyanobacteria via algae toward plants. Photosynthesis Research, 109, 103-114.
26. Kroth P.G., Chiovitti A., Gruber A., Martin-Jezequel V., Mock T., Parker M.S., Stanley M.S., Kaplan A., Caron L., Weber T., Maheswari U., Armbrust E.V., Bowler C. (2008) A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS ONE, 3, e1426.
27. Liepman A.H., Olsen L.J. (2001) Peroxisomal alanine:glyoxylate aminotransferase (AGT1) is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. Plant Journal, 25, 487-498.
28. Löffelhardt W., Bohnert H.J., Bryant D.A. (1997) The cyanelles of Cyanophora paradoxa. Critical Reviews in Plant Sciences, 16, 393-413.
29. Mereschkowsky C. (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biologisches Centralblatt, 25, 593-604.
30. 2-requiring mutant HCR89 of Chlamydomonas reinhardtii. Canadian Journal of Botany, 83, 820-833.
31. Olson J.M., Blankenship R.E. (2004) Thinking about the evolution of photosynthesis. Photosynthesis Research, 80, 373-386.
32. Pellicer M.T., Nunez M.F., Aguilar J., Badia J., Baldoma L. (2003) Role of 2-phosphoglycolate phosphatase of Escherichia coli in metabolism of the 2-phosphoglycolate formed in DNA repair. Journal of Bacteriology, 185, 5815-5821.
33. Pfreundt U., Stal L.J., Voß B., Hess W.R. (2012) Dinitrogen fixation in a unicellular chlorophyll d-containing cyanobacterium. ISME Journal, 6, 1367-1377.
34. Price D.C., Chan C.X., Yoon H.S., Yang E.C., Qiu H., Weber A.P.M., Schwacke R., Gross J., Blouin N.A., Lane C., Reyes-Prieto A., Durnford D.G., Neilson J.A., Lang B., Burger G., Steiner J.M., Löffelhardt W., Meuser J.E., Posewitz M.C., Ball S., Arias M.C., Henrissat B., Coutinho P.M., Rensing S.A., Symeonidi A., Doddapaneni H., Green B.R., Rajah V.D., Boore J., Bhattacharya D. (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science, 335, 843-847.
35. Reyes-Prieto A., Bhattacharya D. (2007) Phylogeny of Calvin cycle enzymes supports Plantae monophyly. Molecular Phylogenetics and Evolution, 45, 384-391.
36. Schwarte S., Bauwe H. (2007) Identification of the photorespiratory 2-phosphoglycolate phosphatase, PGLP1, in Arabidopsis. Plant Physiology, 144, 1580-1586.
37. Suzuki K., Marek L.F., Spalding M.H. (1990) A photorespiratory mutant of Chlamydomonas reinhardtii. Plant Physiology, 93, 231-237.
38. Tabita F.R., Hanson T.E., Li H., Satagopan S., Singh J., Chan S. (2007) Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiology and Molecular Biology Reviews, 71, 576-599.
39. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739.
40. Thrash J.C., Boyd A., Huggett M.J., Grote J., Carini P., Yoder R.J., Robbertse B., Spatafora J.W., Rappe M.S., Giovannoni S.J. (2011) Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade. Scientific Reports, 1, 13.
41. Timm S., Bauwe H. (2012) The variety of photorespiratory phenotypes - employing the current status for future research directions on photorespiration. Plant Biology, 15, 737-747.
42. Timm S., Nunes-Nesi A., Pamik T., Morgenthal K., Wienkoop S., Keerberg O., Weckwerth W., Kleczkowski L.A., Fernie A.R., Bauwe H. (2008) A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. The Plant Cell, 20, 2848-2859.
43. Timme R.E., Bachvaroff T.R., Delwiche C.F. (2012) Broad phylogenomic sampling and the sister lineage of land plants. PLoS One, 7, e29696.
44. Tolbert N.E. (1997) The C-2 oxidative photosynthetic carbon cycle. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 1-23.
45. Whelan S., Goldman N. (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood appr-oach. Molecular Biology and Evolution, 18, 691-699.
46. Winkler U., Stabenau H. (1995) Isolation and characterization of peroxisomes from diatoms. Planta, 195, 403-407.
47. Yoon H.S., Hackett J.D., Ciniglia C., Pinto G., Bhattacharya D. (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution, 21, 809-818.