Journal of Plant Research

, Volume 127, Issue 3, pp 389–397 | Cite as

Analysis of the complete plastid genome of the unicellular red alga Porphyridium purpureum

  • Naoyuki Tajima
  • Shusei Sato
  • Fumito Maruyama
  • Ken Kurokawa
  • Hiroyuki Ohta
  • Satoshi Tabata
  • Kohsuke Sekine
  • Takashi Moriyama
  • Naoki Sato
Regular Paper

Abstract

We determined the complete nucleotide sequence of the plastid genome of the unicellular marine red alga Porphyridium purpureum strain NIES 2140, belonging to the unsequenced class Porphyridiophyceae. The genome is a circular DNA composed of 217,694 bp with the GC content of 30.3 %. Twenty-nine of the 224 protein-coding genes contain one or multiple intron(s). A group I intron was found in the rpl28 gene, whereas the other introns were group II introns. The P. purpureum plastid genome has one non-coding RNA (ncRNA) gene, 29 tRNA genes and two nonidentical ribosomal RNA operons. One rRNA operon has a tRNAAla(UGC) gene between the rrs and the rrl genes, whereas another has a tRNAIle(GAU) gene. Phylogenetic analyses suggest that the plastids of Heterokontophyta, Cryptophyta and Haptophyta originated from the subphylum Rhodophytina. The order of the genes in the ribosomal protein cluster of the P. purpureum plastid genome differs from that of other Rhodophyta and Chromalveolata. These results suggest that a large-scale rearrangement occurred in the plastid genome of P. purpureum after its separation from other Rhodophyta.

Keywords

Genome rearrangement Plastid genome Porphyridium purpureum Rhodophyta rRNA operon 

Supplementary material

10265_2014_627_MOESM1_ESM.pdf (400 kb)
Supplementary material 1 (PDF 400 kb)
10265_2014_627_MOESM2_ESM.xls (42 kb)
Supplementary material 2 (XLS 42 kb)
10265_2014_627_MOESM3_ESM.xls (34 kb)
Supplementary material 3 (XLS 33 kb)
10265_2014_627_MOESM4_ESM.aln (1.2 mb)
Supplementary material 4 (ALN 1276 kb)
10265_2014_627_MOESM5_ESM.aln (1.3 mb)
Supplementary material 5 (ALN 1354 kb)
10265_2014_627_MOESM6_ESM.aln (758 kb)
Supplementary material 6 (ALN 757 kb)
10265_2014_627_MOESM7_ESM.aln (901 kb)
Supplementary material 7 (ALN 900 kb)
10265_2014_627_MOESM8_ESM.aln (262 kb)
Supplementary material 8 (ALN 261 kb)
10265_2014_627_MOESM9_ESM.aln (170 kb)
Supplementary material 9 (ALN 170 kb)
10265_2014_627_MOESM10_ESM.doc (26 kb)
Supplementary material 10 (DOC 25 kb)

References

  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105PubMedCrossRefGoogle Scholar
  2. Alkatib S, Fleischmann TT, Scharff LB, Bock R (2012) Evolutionary constraints on the plastid tRNA set decoding methionine and isoleucine. Nucleic Acids Res 40:6713–6724PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bernard C, Thomas JC, Mazel D, Mousseau A, Castets AM, Tandeau de Marsac N, Dubacq JP (1992) Characterization of the genes encoding phycoerythrin in the red alga Rhodella violacea: evidence for a splitting of the rpeB gene by an intron. Proc Natl Acad Sci USA 89:9564–9568PubMedCentralPubMedCrossRefGoogle Scholar
  4. Bhattacharya D, Price DC, Chan CX, Qiu H, Rose N, Ball S, Weber APM, Arias MC, Henrissat B, Coutinho PM, Krishnan A, Zäuner S, Morath S, Hilliou F, Egizi A, Perrineau MM, Yoon HS (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4:1941PubMedCentralPubMedCrossRefGoogle Scholar
  5. Burki F, Okamoto N, Pombert JF, Keeling PJ (2012) The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proc Biol Sci 279:2246–2254PubMedCentralPubMedCrossRefGoogle Scholar
  6. Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev 73:203–266PubMedCrossRefGoogle Scholar
  7. Cech TR (1988) Conserved sequences and structures of group I introns: building an active site for RNA catalysis––a review. Gene 73:259–271PubMedCrossRefGoogle Scholar
  8. Chan CX, Yang EC, Banerjee T, Yoon HS, Martone PT, Estevez JM, Bhattacharya D (2011) Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr Biol 21:328–333PubMedCrossRefGoogle Scholar
  9. DePriest MS, Bhattacharya D, López-Bautista JM (2013) The plastid genome of the red macroalga Grateloupia taiwanensis (Halymeniaceae). PLoS One 8:e68246PubMedCentralPubMedCrossRefGoogle Scholar
  10. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedCentralPubMedCrossRefGoogle Scholar
  11. Francis MA, Dudock BS (1982) Nucleotide sequence of a spinach chloroplast isoleucine tRNA. J Biol Chem 257:1195–1198Google Scholar
  12. Glöckner G, Rosenthal A, Valentin K (2000) The structure and gene repertoire of an ancient red algal plastid genome. J Mol Evol 51:382–390PubMedGoogle Scholar
  13. Hagopian JC, Reis M, Kitajima JP, Bhattacharya D, Oliveria MC (2004) Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights into the evolution of Rhodoplasts and their relationship to other plastids. J Mol Evol 59:464–477PubMedCrossRefGoogle Scholar
  14. Harper JT, Keeling PJ (2003) Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol 20:1730–1735PubMedCrossRefGoogle Scholar
  15. Janouškovec J, Liu SL, Martone PT, Carré W, Leblanc C, Collén J, Keeling PJ (2013) Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. PLoS One 8:e59001PubMedCentralPubMedCrossRefGoogle Scholar
  16. Jobb G, von Haeseier A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18PubMedCentralPubMedCrossRefGoogle Scholar
  17. Kim E, Archibald JM (2009) Diversity and evolution of plastids and their genomes. The chloroplast––interactions with the environment. In: Aronsson H, Sandelius AS (eds) Plant cell monographs, vol 13. Springer, Berlin, pp 1–39Google Scholar
  18. Konishi T, Shinohara K, Yamada K, Sasaki Y (1996) Acetyl-CoA carboxylase in higher plants: most plants other than gramineae have both the prokaryotic and the eukaryotic forms of this enzyme. Plant Cell Physiol 37:117–122PubMedCrossRefGoogle Scholar
  19. Lang BF, Laforest MJ, Burger G (2007) Mitochondrial introns: a critical view. Trends Genet 23:119–125PubMedCrossRefGoogle Scholar
  20. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948Google Scholar
  21. Livne A, Sukenik A (1990) Acetyl-coenzyme-A carboxylase from the marine prymnesiophyte Isochrysis galbana. Plant Cell Physiol 31:851–858Google Scholar
  22. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964PubMedCentralPubMedCrossRefGoogle Scholar
  23. Nakanishi K, Bonnefond L, Kimura S, Suzuki T, Ishitani R, Nureki O (2009) Structural basis for translational fidelity ensured by transfer RNA lysidine synthetase. Nature 461:1144–1148PubMedCrossRefGoogle Scholar
  24. Neuhaus H, Link G (1987) The chloroplast tRNALys(UUU) gene from mustard (Sinapis alba) contains a class II intron potentially coding for a maturase-related polypeptide. Curr Genet 11:251–257PubMedCrossRefGoogle Scholar
  25. Noguchi H, Taniguchi T, Itoh T (2008) MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Res 15:387–396PubMedCentralPubMedCrossRefGoogle Scholar
  26. O’Brien EA, Zhang Y, Wang E, Marie V, Badejoko W, Lang BF, Burger G (2009) GOBASE: an organelle genome database. Nucleic Acids Res 37:D946–D950PubMedCentralPubMedCrossRefGoogle Scholar
  27. Ohta N, Sato N, Nozaki H, Kuroiwa T (1997) Analysis of the cluster of ribosomal protein genes in the plastid genome of a unicellular red alga Cyanidioschyzon merolae: translocation of the str cluster as an early event in the Rhodophyte–Chromophyte lineage of plastid evolution. J Mol Evol 45:688–695PubMedCrossRefGoogle Scholar
  28. Ohta N, Matsuzaki M, Misumi O, Miyagishima S, Nozaki H, Tanaka K, Shin-I T, Kohara Y, Kuroiwa T (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10:67–77PubMedCrossRefGoogle Scholar
  29. Okaichi T, Nishio S, Imatomi Y (1982) Collection and mass culture. In: Jpn Fish Soc (ed) In toxic phytoplankton––occurrence, mode of action, and toxins. Koseisya-Koseikaku, Tokyo, pp 22–34Google Scholar
  30. Qiu H, Yang EC, Bhattacharya D, Yoon HS (2012) Ancient gene paralogy may mislead inference of plastid phylogeny. Mol Biol Evol 29:3333–3343PubMedCrossRefGoogle Scholar
  31. Reith M, Munholland J (1995) Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol Biol Rep 13:333–335CrossRefGoogle Scholar
  32. Roessler PG, Ohlrogge JB (1993) Cloning and characterization of the gene that encodes acetyl-coenzyme A carboxylase in the alga Cyclotella cryptica. J Biol Chem 268:19254–19259PubMedGoogle Scholar
  33. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  34. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945PubMedCrossRefGoogle Scholar
  35. Sasaki NV, Sato N (2010) CyanoClust: comparative genome resources of cyanobacteria and plastids. Database 2010:bap025PubMedCentralPubMedCrossRefGoogle Scholar
  36. Sato N (2000) SISEQ: manipulation of multiple sequence and large database files for common platforms. Bioinformatics 16:180–181PubMedCrossRefGoogle Scholar
  37. Sato N (2009) Gclust: trans-kingdom classification of proteins using automatic individual threshold setting. Bioinformatics 25:599–605PubMedCrossRefGoogle Scholar
  38. Soma A, Ikeuchi Y, Kanemasa S, Kobayashi K, Ogasawara N, Ote T, Kato J, Watanabe K, Sekine Y, Suzuki T (2003) An RNA-modifying enzyme that governs both the codon and amino acid specificities of isoleucine tRNA. Mol Cell 12:689–698PubMedCrossRefGoogle Scholar
  39. Stirewalt VL, Michalowski CB, Löffelhardt W, Bohnert HJ, Bryant DA (1995) Nucleotide sequence of the cyanelle genome from Cyanophora paradoxa. Plant Mol Biol Rep 13:327–332CrossRefGoogle Scholar
  40. 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. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  41. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCentralPubMedCrossRefGoogle Scholar
  42. Verbruggen H, Maggs CA, Saunders GW, Le Gall L, Yoon HS, De Clerck O (2010) Data mining approach identifies research priorities and data requirements for resolving the red algal tree of life. BMC Evol Biol 10:16PubMedCentralPubMedCrossRefGoogle Scholar
  43. Wang L, Mao Y, Kong F, Li G, Ma F, Zhang B, Sun P, Bi G, Zhang F, Xue H, Cao M (2013) Complete sequence and analysis of plastid genomes of two economically important red algae: Pyropia haitanensis and Pyropia yezoensis. PLoS One 8:e65902PubMedCentralPubMedCrossRefGoogle Scholar
  44. Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99:15507–15512PubMedCentralPubMedCrossRefGoogle Scholar
  45. Yoon HS, Müller KM, Sheath RG, Ott FD, Bhattacharya D (2006) Defining the major lineages of red algae (Rhodophyta). J Phycol 42:482–492CrossRefGoogle Scholar
  46. Zimmerly S, Hausner G, Wu XC (2001) Phylogenetic relationships among group II intron ORFs. Nucleic Acids Res 29:1238–1250PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2014

Authors and Affiliations

  • Naoyuki Tajima
    • 1
    • 2
  • Shusei Sato
    • 3
  • Fumito Maruyama
    • 4
  • Ken Kurokawa
    • 2
    • 5
  • Hiroyuki Ohta
    • 2
    • 6
  • Satoshi Tabata
    • 7
  • Kohsuke Sekine
    • 1
    • 2
  • Takashi Moriyama
    • 1
    • 2
  • Naoki Sato
    • 1
    • 2
  1. 1.Department of Life Sciences, Graduate School of Arts and SciencesUniversity of TokyoTokyoJapan
  2. 2.JST, CRESTTokyoJapan
  3. 3.Department of Environmental Life Sciences, Graduate School of Life SciencesTohoku UniversitySendaiJapan
  4. 4.Section of Bacterial Pathogenesis, Graduate School of Medical and Dental ScienceTokyo Medical and Dental UniversityTokyoJapan
  5. 5.Earth-Life Science InstituteTokyo Institute of TechnologyTokyoJapan
  6. 6.Center for Biological Resources and InformaticsTokyo Institute of TechnologyYokohamaJapan
  7. 7.Kazusa DNA Research InstituteKisarazuJapan

Personalised recommendations