Molecular Genetics and Genomics

, Volume 279, Issue 4, pp 385–401 | Cite as

Transposable elements in Coffea (Gentianales: Rubiacea) transcripts and their role in the origin of protein diversity in flowering plants

  • Fabrício Ramon Lopes
  • Marcelo Falsarella Carazzolle
  • Gonçalo Amarante Guimarães Pereira
  • Carlos Augusto Colombo
  • Claudia Marcia Aparecida Carareto
Original Paper


Transposable elements are major components of plant genomes and they influence their evolution, acting as recombination hot spots, acquiring specific cell functions or becoming part of protein-coding regions. The latter is the subject of the present analysis. This study is a report on the annotation of transposable elements (TEs) in expressed sequences of Coffea arabica, Coffea canephora and Coffea racemosa, showing the occurrence of 383 ESTs and 142 unigenes with TE fragments in these three Coffea species. Based on selected unigenes, it was possible to suggest 26 putative proteins with TE-cassette insertions, demonstrating a likely contribution to protein variability. The genes for two of those proteins, the fertility restorer (FR) and the pyrophosphate-dependent phosphofructokinase (PPi-PFKs) genes, were selected for evaluating the impact of TE-cassettes on host gene evolution of other plant genomes (Arabidopsis thaliana, Oryza sativa and Populus trichocarpa). This survey allowed identifying a FR gene in O. sativa harboring multiple insertions of LTR retrotransposons that originated new exons, which however does not necessarily mean a case of molecular domestication. A possible transduction event of a fragment of the PPi-PFK β-subunit gene mediated by Helitron ATREPX1 in Arabidopsis thaliana was also highlighted.


Transposable elements Coffea genome Protein diversity Molecular domestication Gene transduction 



We thank V.V. Kapitonov (GIRINST, Mountain View, USA) for valuable suggestions, L.M. Almeida (University of Alberta, Edmonton, Canada) for the drawing of Fig. 1 and three anonymous referees for critically reviewing the manuscript. This work was supported by grants provided by the Brazilian agencies FAPESP (fellowship 05/57212-3 to F.R.L) and CNPq (to C.M.A.C and G.A.G.P.).


  1. Almeida LM, Silva IT, Silva WAS Jr, Castro JP, Riggs PK, Carareto CMA, Amaral MEJ (2007) The contribution of transposable elements to Bos taurus gene structure. Gene 390:180–189PubMedCrossRefGoogle Scholar
  2. Alves AMCR, Meijer WG, Vrijbloed JW, Dijkhuizen L (1996) Characterization and phylogeny of the pfp gene of Amycolatopsis methanolica encoding PPi-dependent phosphofructokinase. J Bacteriol 178:149–155PubMedGoogle Scholar
  3. Andrés C, Lurin C, Small ID (2007) The multifarious roles of PPR proteins in plant mitochondrial gene expression. Physiol Plant 129:14–22CrossRefGoogle Scholar
  4. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  5. Arkhipova IR, Meselson M (2005) Diverse DNA transposons in rotifers of the class Bdelloidea. Proc Natl Acad Sci USA 102:11781–11786PubMedCrossRefGoogle Scholar
  6. Bennetzen JL (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269PubMedCrossRefGoogle Scholar
  7. Bennetzen JL (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica 115:29–36PubMedCrossRefGoogle Scholar
  8. Bennetzen JL (2005) Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev 15:621–627PubMedCrossRefGoogle Scholar
  9. Biemont C, Vieira C (2006) Genetics: junk DNA as an evolutionary force. Nature 443:521–524PubMedCrossRefGoogle Scholar
  10. Blakeley SD, Crews L, Todd JF, Dennis DT (1992) Expression of the genes for the α-and β-subunits of pyrophosphate-dependent phosphofructokinase in germinating and developing seeds from Ricinus communis. Plant Physiol 99:1245–1250PubMedCrossRefGoogle Scholar
  11. Britten RJ (2004) Coding sequence of functioning human genes derived entirely from mobile elements sequences. Proc Natl Acad Sci USA 101:16825–16830CrossRefGoogle Scholar
  12. Brosius J (2003) The contribution of RNAs and retroposition to evolutionary novelties. Genetica 118:99–116PubMedCrossRefGoogle Scholar
  13. Brosius J, Gould SJ (1992) On ‘genomenclature’: a comprehensive (and respectful) taxonomy for pseudogenes and other ‘junk DNA’. Proc Natl Acad Sci USA 89:10706–10710PubMedCrossRefGoogle Scholar
  14. Carlisle SM, Blakeley SD, Hemmingsen SM, Trevanion SJ, Hiyoshi T, Kruger NJ, Dennis DT (1990) Pyrophosphate-dependent phosphofructokinase. Conservation of protein sequence between the subunits and with the ATP-dependent phosphofructokinase. J Biol Chem 265:18366–18371PubMedGoogle Scholar
  15. DeBarry JD, Ganko E, McDonald JF (2005) The contribution of LTR retrotransposon sequences to gene evolution in Mus musculus. Mol Biol Evol 23:479–481PubMedCrossRefGoogle Scholar
  16. Deng Z, Huang M, Singh K, Albach RA, Latshaw SP, Chang KP, Kemp RG (1998) Cloning and expression of the gene for the active PPi-dependent phosphofructokinase of Entamoeba histolytica. Biochem J 329:659–664PubMedGoogle Scholar
  17. Deng Z, Roberts D, Wang X, Kemp RG (1999) Expression, characterization, and crystallization of the pyrophosphate dependent phosphofructo-1-kinase of Borrelia burgdorferi. Arch Biochem Biophys 371:326–331PubMedCrossRefGoogle Scholar
  18. Deininger PL, Batzer MA (1999) Alu repeats and human disease. Mol Genet Metab 67:183–193PubMedCrossRefGoogle Scholar
  19. Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603PubMedCrossRefGoogle Scholar
  20. Eickler EE, Sankoff D (2003) Structural dynamics and eukaryotic chromosomal evolution. Science 301:793–797CrossRefGoogle Scholar
  21. Fedoroff N (2000) Transposon and genome evolution in plants. Proc Natl Acad Sci USA 97:7002–7007PubMedCrossRefGoogle Scholar
  22. Ganko EW, Bhattacharjee V, Schliekelman P, McDonald JF (2003) Evidence for the contribution of LTR retrotransposon to C. elegans gene evolution. Mol Biol Evol 20:1925–1931PubMedCrossRefGoogle Scholar
  23. Ganko EW, Greene CS, Lewis JA, Bhattacharjee VM, McDonald JF (2006) LTR retrotransposon-gene associations in Drosophila melanogaster. J Mol Evol 62:111–120PubMedCrossRefGoogle Scholar
  24. Gerber A, O’Connell MA, Keller W (1997) Two forms of human double-stranded RNA-specific editase 1 (hRED1) generated by the insertion of an Alu cassette. RNA 3:453–463PubMedGoogle Scholar
  25. Gotea V, Makalowski W (2006) Do transposable elements really contribute to proteomes? Trends Genet 22:260–267PubMedCrossRefGoogle Scholar
  26. Gupta S, Gallavotti A, Stryker GA, Schmidt RJ, Lal SK (2005) A novel class of Helitron-related transposable elements in maize contain portions of multiple pseudogenes. Plant Mol Biol 57:115–127PubMedCrossRefGoogle Scholar
  27. Hayashi Y, Sakata H, Makino Y, Urabe I, Yomo T (2003) Can an arbitrary sequence evolve towards acquiring a biological function? J Mol Evol 56:162–168PubMedCrossRefGoogle Scholar
  28. Hilgard P, Huang TM, Wolkoff AW, Stockert RJ (2002) Translated Alu sequence determines nuclear localization of a novel catalytic subunit of casein kinase 2. Am J Physiol Cell Physiol 283:C472–C483PubMedGoogle Scholar
  29. Hoenicka J, Arrasate M, de Yebenes JG, Avila J (2002) A two-hybrid screening of human Tau protein: interactions with Alu-derived domain. Neuroreport 13:343–349PubMedCrossRefGoogle Scholar
  30. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–77PubMedCrossRefGoogle Scholar
  31. International Human Genome Sequencing Consortium (2001) A physical map of the human genome. Nature 409:934–941CrossRefGoogle Scholar
  32. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  33. Jordan IK, Rogozin IB, Glazko GV, Koonin EV (2003) Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 19:68–72PubMedCrossRefGoogle Scholar
  34. Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573PubMedCrossRefGoogle Scholar
  35. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) RepBase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467PubMedCrossRefGoogle Scholar
  36. Kapitonov VV, Jurka J (2000) Non autonomous DNA transposon ATDNA1T9A—a consensus sequence. Repbase Update.
  37. Kapitonov VV, Jurka J (2001a) ATMU6N1 is a non-autonomous DNA transposon—a consensus sequence. Repbase Update.
  38. Kapitonov VV, Jurka J (2001b) Rolling-circle transposon in eukaryotes. Proc Natl Acad Sci USA 98:8714–8719PubMedCrossRefGoogle Scholar
  39. Kapitonov VV, Jurka J (2003) Molecular paleontology of the transposable elements in the Drosophila melanogaster genome. Proc Natl Acad Sci USA 100:6569–6574PubMedCrossRefGoogle Scholar
  40. Kapitonov VV, Jurka J (2005) Helitron4_OS: a new, possibly active helitron from rice. Repbase Rep 5:181–181Google Scholar
  41. Kapitonov VV, Jurka J (2007) Helitrons on a roll: eukaryotic rolling-circle transposons. Trends Genet 23:521–529PubMedCrossRefGoogle Scholar
  42. Kidwell MG (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115:49–63PubMedCrossRefGoogle Scholar
  43. Kidwell MG, Lish D (1997) Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci USA 94:7704–7711PubMedCrossRefGoogle Scholar
  44. Lal SK, Giroux MJ, Brendel V, Vallejos CE, Hannah LC (2003) The maize genome contains a Helitron insertion. Plant Cell 15:381–391PubMedCrossRefGoogle Scholar
  45. Li WH, Gu ZL, Wang HD, Nekrutenko A (2001) Evolutionary analyses of the human genome. Nature 409:847–849PubMedCrossRefGoogle Scholar
  46. Lin C, Mueller LA, Carthy JM, Crouzillat D, Pétiard V, Tanksley SD (2005) Coffee and tomato share common gene repertories as revealed by deep sequencing of seed and cherry transcripts. Theor Appl Genet 112:114–130PubMedCrossRefGoogle Scholar
  47. Lorenc A, Makalowski W (2003) Transposable elements and vertebrate protein diversity. Genetica 118:183–191PubMedCrossRefGoogle Scholar
  48. Makalowski W (2000) Genomic scrap yard: how genomes utilize all that junk. Gene 259:61–67PubMedCrossRefGoogle Scholar
  49. Makalowski W, Mitchel GA, Labuda D (1994) Alu sequences in the coding regions of mRNA: a source of protein variability. Trends Genet 10:188–193PubMedCrossRefGoogle Scholar
  50. Mao L, Wood TC, Yu Y, Budiman MA, Tomkins J, Woo S, Sasinonowski M, Presting G, Frish D, Goff S, Dean RA, Wing RA (2000) Rice transposable elements: a survey of 73,000 sequence-tagged-connectors. Genome Res 10:982–990PubMedCrossRefGoogle Scholar
  51. Mertens E, Ladror US, Lee JA, Miretsky A, Morris A, Rozario C, Kemp RG, Muller M (1998) The pyrophosphate-dependent phosphofructokinase of the protist, Trichomonas vaginalis, and the evolutionary relationships of protist phosphofructokinases. J Mol Evol 47:739–750PubMedCrossRefGoogle Scholar
  52. Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR, Yu Y, Wei FS, Fuks G, Soderlund CA, Mayer KFX, Wing RA (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101:14349–14354PubMedCrossRefGoogle Scholar
  53. Meyers BC, Tingey SV, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11:1660–1676PubMedCrossRefGoogle Scholar
  54. Miller WJ, McDonald JF, Nouaud D, Anxolabéhère D (1999) Molecular domestication—more than a sporadic episode in evolution. Genetica 107:197–207PubMedCrossRefGoogle Scholar
  55. Mitchell GA et al (1991) Splice-mediated insertion of an Alu sequence inactivates ornithine delta-aminotransferase: a role for Alu elements in human mutation. Proc Natl Acad Sci USA 88:815–819PubMedCrossRefGoogle Scholar
  56. Möhlmann T, Tjaden J, Schwoppe C, Winkler HH, Kampfenkel K, Neuhaus HE (1998) Occurrence of two plastidic ATP/ADP transporters in Arabidopsis thaliana L—molecular characterisation and comparative structural analysis of similar ATP/ADP translocators from plastids and Rickettsia prowazekii. Eur J Biochem 252:353–359PubMedCrossRefGoogle Scholar
  57. Moore SA, Ronimus RS, Roberson RS, Morgan HW (2002) The structure of a pyrophosphate-dependent phosphofructokinase from the Lyme disease spirochete Borrelia burgdoferi. Structure 10:659–671PubMedCrossRefGoogle Scholar
  58. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by Helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002PubMedCrossRefGoogle Scholar
  59. Mustroph A, Sonnewald U, Biemelt S (2007) Characterization of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana. FEBS Lett 581:2401–2410PubMedCrossRefGoogle Scholar
  60. Nekrutenko A, Li WH (2001) Transposable elements are found in a large number of human protein-coding genes. Trends Genet 17:619–621PubMedCrossRefGoogle Scholar
  61. Ohno S (1970) Evolution by gene duplication. Springer, BerlinGoogle Scholar
  62. Orgel LE, Crick FH (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607PubMedCrossRefGoogle Scholar
  63. Poulter RTM, Goodwin TJD, Butler MI (2003) Vertebrate helentrons and other novel Helitrons. Gene 313:201–212PubMedCrossRefGoogle Scholar
  64. Pritham EJ, Feschotte C (2007) Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus. Proc Natl Acad Sci USA 104:1895–1900PubMedCrossRefGoogle Scholar
  65. Pruitt KD, Maglott DR (2001) RefSeq and LocusLink: NCBI gene-centered resources. Nucleic Acids Res 29:137–140PubMedCrossRefGoogle Scholar
  66. Roberson RS, Ronimus RS, Gephart S, Morgan HW (2000) Biochemical characterization of an active pyrophosphate-dependent phosphofructokinase from Treponema pallidum. FEMS Microbiol Lett 9735:1–4Google Scholar
  67. Sakai H, Tanaka T, Itoh T (2007) Birth and death of genes promoted by transposable elements in Oryza sativa. Gene 392:59–63PubMedCrossRefGoogle Scholar
  68. SanMiguel P, Tihkonov A, Jin YK, Motchoulskaia N, Zkharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposon in the intergenic regions of the maize genome. Science 274:765–768PubMedCrossRefGoogle Scholar
  69. Sarkar A, Sim C, Hong YS, Hogan JR, Fraser MJ, Robertson HM, Collins FH (2003) Molecular evolutionary analysis of widespread piggy-back transposon family and related domesticated sequences. Mol Genet Genomics 270:173–180PubMedCrossRefGoogle Scholar
  70. Shapiro JA, von Sternberg R (2005) Why repetitive DNA is essential to genome function. Biol Rev 80:227–250PubMedCrossRefGoogle Scholar
  71. Siebers B, Klenk HP, Hensel R (1998) PPi-dependent phophofructokinase from Thermoproteus tenax, an archaeal descendant of an ancient line in phosphofructokinase evolution. J Bacteriol 180:2137–2143PubMedGoogle Scholar
  72. Sigrell JA, Cameron AD, Jones TA, Mowbray SL (1998) Structure of the Escherichia coli ribokinase in complex with ribose and dinucleotide determined to 1.8 Å resolution: insights into a new family of kinase structures. Structure 6:183–193PubMedCrossRefGoogle Scholar
  73. Sorek R, Ast G, Graur D (2002) Alu-containing exons are alternatively spliced. Genome Res 12:1060–1067PubMedCrossRefGoogle Scholar
  74. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Arvind L, Mitchell W, Olinger L, Tatusov RL, Zhao Q (1998) Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754–759PubMedCrossRefGoogle Scholar
  75. Swofford DL (1998) PAUP*: phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, SunderlandGoogle Scholar
  76. The Gene Ontology Consortium (2001) Creating the gene ontology resource: design and implementation. Genome Res 11:1425–1433CrossRefGoogle Scholar
  77. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  78. Thornburg BG, Gotea V, Makalowski W (2006) Transposable elements as source of transcription regulation signals. Gene 365:104–110PubMedCrossRefGoogle Scholar
  79. Tikhonov AP et al. (1999) Collinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci USA 96:7409–7414PubMedCrossRefGoogle Scholar
  80. Tjaden J, Schwoppe C, Mohlmann T, Quick PW, Neuhaus HE (1998) Expression of a plastidic ATP/ADP transporter gene in Escherichia coli leads to a functional adenine nucleotide transport system in the bacterial cytoplasmic membrane. J Biol Chem 273:9630–9636PubMedCrossRefGoogle Scholar
  81. Turcotte K, Srinivasan S, Bureau T (2001) Survey of transposable elements from rice genomic sequences. Plant J 25:169–179PubMedCrossRefGoogle Scholar
  82. Tuskan GA et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604PubMedCrossRefGoogle Scholar
  83. van de Lagemaat LN, Landry JR, Mager DL, Medstrand P (2003) Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 19:530–536PubMedCrossRefGoogle Scholar
  84. Vieira LGE, Andrade AC, Colombo CA et al (2006) Brazilian coffee genome project: an EST-based genomic resource. Braz J Plant Physiol 18:95–108Google Scholar
  85. Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukariotes. BioEssays 28:913–922PubMedCrossRefGoogle Scholar
  86. Wu LF, Reizer A, Reizer J, Cai B, Tomich JM, Saier MH (1991) Nucleotide sequence of the Rhodobacter capsulatus fruK gene, which encodes fructose-1-phosphate kinase: superfamily including both phosphofructokinases of E. coli. J Bacteriol 173:3117–3127PubMedGoogle Scholar
  87. Xu JH, Messing J (2006) Maize haplotyple with a Helitron-amplified cytidine deaminase gene copy. BMC Genetics 9:7–52Google Scholar
  88. Zhang J, Peterson T (1999) Genome rearrangements by nonlinear transposons in maize. Genetics 153:1403–1410PubMedGoogle Scholar
  89. Zhou Q et al (2006) Helitron transposons on the sex chromosomes of the platyfish Xiphophorus maculatus and their evolution in animal genomes. Zebrafish 3:39–52PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Fabrício Ramon Lopes
    • 1
  • Marcelo Falsarella Carazzolle
    • 2
  • Gonçalo Amarante Guimarães Pereira
    • 2
  • Carlos Augusto Colombo
    • 3
  • Claudia Marcia Aparecida Carareto
    • 1
  1. 1.Laboratory of Molecular Evolution, Department of BiologyUNESP, São Paulo State UniversitySão José do Rio PretoBrazil
  2. 2.Laboratory of Genomics and Expression, Department of Genetics and Evolution, Institute of BiologyUNICAMP, State University of CampinasCampinasBrazil
  3. 3.IAC, Agronomic Institute of CampinasCampinasBrazil

Personalised recommendations