Phylogeny of galactolipid synthase homologs together with their enzymatic analyses revealed a possible origin and divergence time for photosynthetic membrane biogenesis

DNA Research

Volumn 19, Issue 1, 2012, Pages 91-102

  Yuzawa, Yuichi ^a   Nishihara, Hidenori ^a   Haraguchi, Tsuyoshi ^a   Masuda, Shinji ^a   Shimojima, Mie ^a   Shimoyama, Atsushi ^a   Yuasa, Hideya ^a   Okada, Norihiro ^a   Ohta, Hiroyuki ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

galactolipid; MGDG synthase; monogalactosyldiacylglycerol; plastid evolution; Roseiflexus castenholzii

Indexed keywords

GALACTOLIPID; GALACTOLIPID SYNTHASE; GALACTOSYLDIACYLGLYCEROL; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CHLOROPLAST; CYANOBACTERIUM; LIPID ANALYSIS; MOLECULAR EVOLUTION; NONHUMAN; PHOTOSYNTHESIS; PHYLOGENY; PLANT; PLASTID; PROTON NUCLEAR MAGNETIC RESONANCE;

ARABIDOPSIS; CHLOROFLEXI; EVOLUTION, MOLECULAR; GALACTOSYLTRANSFERASES; GLYCOLIPIDS; LIPIDS; MODELS, GENETIC; PHOTOSYNTHESIS; PHYLOGENY; PLASTIDS; SEQUENCE HOMOLOGY; THYLAKOIDS;

CHLOROFLEXI; CHLOROFLEXI (CLASS); CHLOROPHYTA; CYANOBACTERIA; EMBRYOPHYTA; ROSEIFLEXUS CASTENHOLZII; SPERMATOPHYTA; VIRIDIPLANTAE;

EID: 84856909729     PISSN: 13402838     EISSN: 17561663     Source Type: Journal    
DOI: 10.1093/dnares/dsr044     Document Type: Article

References (55)

1. McFadden, G.I. 2001, Primary and secondary endosymbiosis and the origin of plastids, J. Phycol., 37, 951-9. (Pubitemid 34067654)
2. Nelissen, B., Van de Peer, Y., Wilmotte, A. and De Wachter, R. 1995, An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences, Mol. Biol. Evol., 12, 1166-73.
3. Martin, W., Rujan, T., Richly, E., et al. 2002, Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus, Proc. Natl Acad. Sci. USA, 99, 12246-51.
4. Wolfe, G.R., Cunningham, F.X., Durnford, D., Green, B.R. and Gantt, E. 1994, Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation, Nature, 367, 566-8. (Pubitemid 24055516)
5. Osteryoung, K.W. and Vierling, E. 1995, Conserved cell and organelle division, Nature, 376, 473-4.
6. Joyard, J., Marechal, E., Miege, C., Block, M.A., Dorne, A.J. and Douce, R. 1998, Structure, distribution and biosynthesis of glycerolipids from higher plant chloroplasts. In: Siegenthaler, P.A. and Murata, N., eds. Lipid in Photosynthesis: Structure, Function and Genetics, Kluwer Academic Publishers: Dordrecht, pp. 21-52.
7. Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W. and Krauss, N. 2001, Three-dimensional structure of cyanobacterial photosystem I at 2.5A° resolution, Nature, 411, 909-17. (Pubitemid 32601481)
8. Loll, B., Kern, J., Saenger, W., Zouni, A. and Biesiadka, J. 2005, Towards complete cofactor arrangement in the 3.0A° resolution structure of photosystem II, Nature, 438, 1040-4. (Pubitemid 43093979)
9. Kobayashi, K., Kondo, M., Fukuda, H., Nishimura, M. and Ohta, H. 2007, Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis, Proc. Natl Acad. Sci. USA, 104, 17216-21. (Pubitemid 350211017)
10. Sato, N. and Murata, N. 1982, Lipid biosynthesis in the blue-green alga, Anabaena variabilis I. Lipid classes, Biochim. Biophys. Acta, 710, 271-8.
11. Shimojima, M., Ohta, H., Iwamatsu, A., Masuda, T., Shioi, Y. and Takamiya, K. 1997, Cloning of the gene for monogalactosyldiacylglycerol synthase and its evolutionary origin, Proc. Natl Acad. Sci. USA, 94, 333-7. (Pubitemid 27027210)
12. Dörmann, P. and Benning, C. 2002, Galactolipids rule in seed plants, Trends Plant. Sci., 7, 112-8. (Pubitemid 36726436)
13. Awai, K., Kakimoto, T., Awai, C., et al. 2006, Comparative genomic analysis revealed a gene for monoglucosyldiacylglycerol synthase, an enzyme for photosynthetic membrane lipid synthesis in cyanobacteria, Plant Physiol., 141, 1120-7. (Pubitemid 44061617)
14. Hölzl, G. and Dörmann, P. 2007, Structure and function of glycoglycerolipids in plants and bacteria, Prog. Lipid Res., 46, 225-43. (Pubitemid 47095009)
15. Woese, C.R. 1987, Bacterial evolution, Microbiol. Rev., 51, 221-71. (Pubitemid 17082512)
16. Gupta, R.S., Mukhtar, T. and Singh, B. 1999, Evolutionary relationships among photosynthetic prokaryotes (Heliobacterium chlorum, Chloroflexus aurantiacus, cyanobacteria, Chlorobium tepidum and proteobacteria): implications regarding the origin of photosynthesis, Mol. Microbiol., 32, 893-906. (Pubitemid 29255757)
17. Xiong, J., Fischer, W.M., Inoue, K., Nakahara, M. and Bauer, C.E. 2000, Molecular evidence for the early evolution of photosynthesis, Science, 289, 1724-30.
18. Pierson, B.K. and Castenholz, R.W. 1974, A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov, Arch. Microbiol., 100, 5-24.
19. Hölzl, G., Zähringer, U., Warnecke, D. and Heinz, E. 2005, Glycoengineering of cyanobacterial thylakoid membranes for future studies on the role of glycolipids in photosynthesis, Plant Cell Physiol., 46, 1766-78. (Pubitemid 41746559)
20. Hanada, S., Takaichi, S., Matsuura, K. and Nakamura, K. 2002, Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes, Int. J. Syst. Evol. Microbiol., 52, 187-93. (Pubitemid 34105705)
21. Awai, K., Maréchal, E., Block, M.A., et al. 2001, Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana, Proc. Natl Acad. Sci. USA, 98, 10960-5. (Pubitemid 32878726)
22. Kobayashi, K., Awai, K., Nakamura, M., Nagatani, A., Masuda, T. and Ohta, H. 2009, Type-B monogalactosyldiacylglycerol synthases are involved in phosphate starvation-induced lipid remodeling, and are crucial for low-phosphate adaptation, Plant J., 57, 322-31.
23. Andersson, M.X., Stridh, M.H., Larsson, K.E., Liljenberg, C. and Sandelius, A.S. 2003, Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol, FEBS Lett., 537, 128-32. (Pubitemid 36246689)
24. Gaude, N., Tippmann, H., Flemetakis, E., Katinakis, P., Udvardi, M. and Dörmann, P. 2004, The galactolipid digalactosyldiacylglycerol accumulates in the peribacteroid membrane of nitrogen-fixing nodules of soybean and Lotus, J. Biol. Chem., 279, 34624-30. (Pubitemid 39318092)
25. Jouhet, J., Maréchal, E., Baldan, B., Bligny, R., Joyard, J. and Block, M.A. 2004, Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria, J. Cell Biol., 167, 863-74. (Pubitemid 39628109)
26. Russo, M.A., Quartacci, M.F., Izzo, R., Belligno, A. and Navari-Izzo, F. 2007, Long-and short-term phosphate deprivation in bean roots: plasma membrane lipid alterations and transient stimulation of phospholipases, Phytochemistry, 68, 1564-71. (Pubitemid 46764777)
27. Kobayashi, K., Awai, K., Takamiya, K. and Ohta, H. 2004, Arabidopsis type B monogalactosyldiacylglycerol synthase genes are expressed during pollen tube growth and induced by phosphate starvation, Plant Physiol., 134, 640-8. (Pubitemid 38261537)
28. Thompson, J.D., Muller, A., Waterhouse, A., et al. 2006, MACSIMS: multiple alignment of complete sequences information management system, BMC Bioinformatics, 7, 318.
29. Edgar, R.C. 2004, MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic. Acids Res., 32, 1792-7. (Pubitemid 38832724)
30. Ronquist, F. and Huelsenbeck, J.P. 2003, MrBayes 3: Bayesian phylogenetic inference under mixed models, Bioinformatics, 19, 1572-4. (Pubitemid 37038874)
31. Jobb, G., von Haeseler, A. and Strimmer, K. 2004, TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics, BMC Evol. Biol., 4, 18.
32. Stamatakis, A. 2006, RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models, Bioinformatics, 22, 2688-90. (Pubitemid 44642609)
33. Yang, Z. 2007, PAML 4: phylogenetic analysis by maximum likelihood, Mol. Biol. Evol., 24, 1586-91. (Pubitemid 47236688)
34. Yoon, H.S., Hackett, J.D., Ciniglia, C., Pinto, G. and Bhattacharya, D. 2004, A molecular timeline for the origin of photosynthetic eukaryotes, Mol. Biol. Evol., 21, 809-18. (Pubitemid 38529723)
35. Kenrick, P. and Crane, P.R. 1997, The origin and early evolution of plants on land, Nature, 389, 33-9. (Pubitemid 27387682)
36. Gillespie, W.H., Rothwell, G.W. and Scheckler, S.E. 1981, The earliest seeds, Nature, 293, 462-4.
37. Crane, P.R., Friis, E.M. and Pedersen, K.R. 1995, The origin and early diversification of angiosperms, Nature, 374, 27-33.
38. Bligh, E.G. and Dyer, W.J. 1959, A rapid method of total lipid extraction and purification, Can. J. Biochem. Physiol., 37, 911-7.
39. Yamada, M., Zhang, H., Hanada, S., Nagashima, K.V., Shimada, K. and Matsuura, K. 2005, Structural and spectroscopic properties of a reaction center complex from the chlorosome-lacking filamentous anoxygenicphototrophic bacterium Roseiflexus castenholzii, J. Bacteriol., 187, 1702-9. (Pubitemid 40289371)
40. Yoon, H.S., Hackett, J.D., Pinto, G. and Bhattacharya, D. 2002, The single, ancient origin of chromist plastids, Proc. Natl Acad. Sci. USA, 99, 15507-12. (Pubitemid 35403964)
41. Harper, J.T. and Keeling, P.J. 2003, Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids, Mol. Biol. Evol., 20, 1730-5. (Pubitemid 41070836)
42. Hanada, S., Hiraishi, A., Shimada, K. and Matsuura, K. 1995, Chloroflexus aggregans sp. nov., a filamentous phototrophic bacterium which forms dense cell aggregates by active gliding movement, Int. J. Syst. Bacteriol., 45, 676-81.
43. Botté, C.Y., Yamaryo-Botté, Y., Janouskovec, J., et al. 2011, Identification of plant-like galactolipids in Chromera velia, a photosynthetic relative of malaria parasites, J. Biol. Chem., 286, 29893-903.
44. Knudsen, E., Jantzen, E., Bryn, K., Ormerod, J. and Sireva°g, R. 1982, Quantitative and structural characterization of lipids in Chlorobium and Chloroflexus, Arch. Microbiol., 132, 149-54. (Pubitemid 12062458)
45. Masuda, S., Harada, J., Yokono, M., et al. 2011, A monogalactosyldiacylglycerol synthase found in the green sulfur bacterium Chlorobaculum tepidum reveals important roles for galactolipids in photosynthesis, Plant Cell, 23, 2644-58.
46. Suzuki, K. and Miyagishima, S.Y. 2010, Eukaryotic and eubacterial contributions to the establishment of plastid proteome estimated by large-scale phylogenetic analyses, Mol. Biol. Evol., 27, 581-90.
47. Jiao, Y., Wickett, N.J., Ayyampalayam, S., et al. 2011, Ancestral polyploidy in seed plants and angiosperms, Nature, 473, 97-100.
48. DiMichele, W.A., Pfefferkorn, H.W. and Gastaldom, R.A. 2001, Response of late carboniferous and early Permian plant communities to climate change, Annu. Rev. Earth Planet Sci., 29, 461-87. (Pubitemid 32554925)
49. Kobayashi, K., Masuda, T., Takamiya, K. and Ohta, H. 2006, Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk, Plant J., 47, 238-48. (Pubitemid 43977753)
50. Raymond, J., Zhaxybayeva, O., Gogarten, J.P., Gerdes, S.Y. and Blankenship, R.E. 2002, Whole-genome analysis of photosynthetic prokaryotes, Science, 298, 1616-20. (Pubitemid 35387199)
51. Keeling, P.J. and Palmer, J.D. 2008, Horizontal gene transfer in eukaryotic evolution, Nat. Rev. Genet., 9, 605-18.
52. Turner, S., Pryer, K.M., Miao, V.P. and Palmer, J.D. 1999, Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis, J. Eukaryot. Microbiol., 46, 327-38. (Pubitemid 29400753)
53. Blankenship, R.E. 2010, Early evolution of photosynthesis, Plant Physiol., 154, 434-8.
54. Pryer, K.M., Schneider, H., Smith, A.R., et al. 2001, Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants, Nature, 409, 618-22.
55. Palmer, J.D., Soltis, D.E. and Chase, M.W. 2004, The plant tree of life: an overview and some points of view, Am. J. Bot., 91, 1437-45. (Pubitemid 43193712)