Molecular Biology Reports

, Volume 38, Issue 6, pp 3787–3794 | Cite as

Ttd1a promoter is involved in DNA–protein binding by salt and light stresses

  • Pasqualina Woodrow
  • Giovanni Pontecorvo
  • Loredana F. Ciarmiello
  • Amodio Fuggi
  • Petronia Carillo


Stress modulation of retrotransposons may play a role in generating host genetic plasticity in response to environmental stress. Transposable elements have been suggested to contribute to the evolution of genes, by providing cis-regulatory elements leading to changes in expression patterns. Indeed, their promoter elements are similar to those of plant defence genes and may bind similar defence-induced transcription factors. We previously isolated a new Ty1-copia retrontrasposon named Ttd1a and showed its activation and mobilization in salt and light stresses. Here, using a retard mobility assay in Triticum durum L. crude extracts, we showed that the CAAT motif present in the Ttd1a retrotransposon promoter, is involved in DNA–protein binding under salt and light stresses and therefore in the regulation of Ttd1a activity. Data presented in this paper suggest that nuclear proteins can interact with the CAAT motif either directly or indirectly and enhance Ttd1a by a specific ligand-dependent activation under stress.


Abiotic stress Band shift Cis-acting element LTR retrotransposon Triticum durum 


  1. 1.
    Hirochika H, Hirochika R (1993) Ty1-copia group retrotransposons as ubiquitous components of plant genomes. Jpn J Genet 68:35–46PubMedCrossRefGoogle Scholar
  2. 2.
    Kumar A, Bennetzen JL (2000) Retrotransposons: central players in the structure, evolution and function of plant genomes. Trends Plant Sci 5:509–510PubMedCrossRefGoogle Scholar
  3. 3.
    Fantaccione S, Woodrow P, Pontecorvo G (2007) Identification of a family of SINEs and LINEs in Pipistrellus kuhli genome: a new structural and functional symbiotic relationship. Genomics 91:178–185CrossRefGoogle Scholar
  4. 4.
    SanMiguel P, Tikhonov A, Jin YK, Melake-Berhan A, Springer PS, Edwards KJ, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768PubMedCrossRefGoogle Scholar
  5. 5.
    Heslop-Harrison JS, Brandes A, Taketa S et al (1997) The chromosomal distribution of Ty1–copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica 100:197–204PubMedCrossRefGoogle Scholar
  6. 6.
    Sabot F, Simon D, Bernard M (2004) Plant transposable elements, with an emphasis on grass species. Euphytica 139(3):227–247CrossRefGoogle Scholar
  7. 7.
    Hirochika H, Otsuki H, Yoshikawa M, Otsuki Y, Sugimoto K, Takeda S (1996) Autonomous transposition of the tobacco retrotransposon Tto1 in rice. Plant Cell 8:725–734PubMedCrossRefGoogle Scholar
  8. 8.
    Grandbastien MA (2004) Stress activation and genomic impact of plant retrotransposons. Journal de la Société de biologie 198:425–432PubMedGoogle Scholar
  9. 9.
    Grandbastien MA, Audeon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa AP, Le QH, Melayah D, Petit M, Poncet C, Tam SM, Van Sluys MA, Mhiri C (2005) Stress activation and genomic impact of Tnt1 retrotransposon in Solanaceae. Cytogenet Genome Res 110:229–241PubMedCrossRefGoogle Scholar
  10. 10.
    Kimura Y, Tosa Y, Shimada S, Sogo R, Kusaba M, Sunaga T, Betsuyaku S, Eto Y, Nakayashiki H, Mayama S (2001) OARE-1, a Ty1-copia retrotransposon in oat activated by abiotic and biotic stresses. Plant Cell Physiol 42:1345–1354PubMedCrossRefGoogle Scholar
  11. 11.
    Woodrow P, Pontecorvo G, Fantaccione S, Kafantaris I, Fuggi A, Parisi D, Carillo P (2010) Polymorphism of a new Ty1-copia retrotransposon in durum wheat under salt and light stresses. Theor Appl Genet 121:311–322PubMedCrossRefGoogle Scholar
  12. 12.
    Silva JC, Loreto EL, Clark JB (2004) Factors that affect the horizontal transfer of transposable elements. Curr Issues Mol Biol 6:57–72PubMedGoogle Scholar
  13. 13.
    Kumar A, Bennetzen JL (1999) Plant retrotransposon. Annu Rev Genet 33:479–532PubMedCrossRefGoogle Scholar
  14. 14.
    Wicker T, Sabot F, Hua-Van A, Bennetzen J, Capy P, Chalhoub B, Flavell AJ, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982PubMedCrossRefGoogle Scholar
  15. 15.
    Wright DA, Voytas DF (2002) Athila of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12:122–131PubMedCrossRefGoogle Scholar
  16. 16.
    Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285PubMedCrossRefGoogle Scholar
  17. 17.
    Vitte C, Panaud O, Quesneville H (2007) LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 8:218PubMedCrossRefGoogle Scholar
  18. 18.
    Hirochika H (1995) Activation of plant retrotransposons by stress. In: Oono K (ed) Modification of gene expression and non-mendelian inheritance. Tsukuba, NIAR, pp 15–21Google Scholar
  19. 19.
    Wendel JF, Wessler SR (2000) Retrotransposon-mediated genome evolution on a local ecological scale. Proc Natl Acad Sci USA 97:6250–6252PubMedCrossRefGoogle Scholar
  20. 20.
    Grandbastien MA, Lucas H, More JB, Mhiri C, Vernhettes S, Casacuberta JM (1997) The expression of the tobacco Tnt1 is linked to the plant defence responses. Genetica 100:241–252PubMedCrossRefGoogle Scholar
  21. 21.
    Bradshaw VA, McEntee K (1989) DNA damage activates transcription and transposition of yeast Ty retrotransposons. Mol Gen Genet 218:465–474PubMedCrossRefGoogle Scholar
  22. 22.
    Strand DJ, McDonald JF (1985) Copia is transcriptionally responsive to environmental stress. Nucleic Acids Res 13:4401–4410PubMedCrossRefGoogle Scholar
  23. 23.
    Liu WM, Chu WM, Choudary PV, Schmid CW (1995) Cell stress and translational inhibitors transiently increase the abundance of mammalian SINE transcripts. Nucleic Acids Res 23:1758–1765PubMedCrossRefGoogle Scholar
  24. 24.
    Salazar M, González E, Casaretto JA, Casacuberta JM, Ruiz LS (2007) The promoter of the TLC1.1 retrotransposon from Solanum chilense is activated by multiple stress-related signaling molecules. Plant Cell Rep 26:1861–1868PubMedCrossRefGoogle Scholar
  25. 25.
    Pouteau S, Grandbastien MA, Boccara M (1994) Microbial elicitors of plant defence responses activate transcription of a retrotransposon. Plant J 5(4):535–542CrossRefGoogle Scholar
  26. 26.
    Takeda S, Sugimoto K, Otsuki H, Hirochika H (1999) A 13-pb cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J 18:383–393PubMedCrossRefGoogle Scholar
  27. 27.
    Vernhettes S, Grandbastien MA, Casacuberta JM (1998) The evolutionary analysis of the Tnt1 retrotransposon in Nicotiana species reveals the high variability of its regulatory sequences. Mol Biol Evol 15:827–836PubMedGoogle Scholar
  28. 28.
    Tapia G, Verdugo I, Yañez M, Ahumada I, Theoduloz C, Cordero C, Poblete F, González E, Ruiz-Lara S (2005) Involvement of ethylene in stress-induced expression of the TLC1.1 retrotransposon from Lycopersicon chilense Dun. Plant Physiol 138(4):2075–2086PubMedCrossRefGoogle Scholar
  29. 29.
    Suoniemi A, Navarro A, Schulman AH (1996) The BARE-1 retrotransposon is transcribed in barley from an LTR promoter active in transient assays. Plant Mol Biol 31:295–306PubMedCrossRefGoogle Scholar
  30. 30.
    Beguiristain T, Grandbastien MA, Puigdomenech P, Casacuberta JM (2001) Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco: consequences for retrotransposon control and evolution in plants. Plant Physiol 127:212–221PubMedCrossRefGoogle Scholar
  31. 31.
    Casacuberta JM, Santiago N (2003) Plant LTR-retrotransposons and MITEs: control of transposition and impact on the evolution of plant genes and genomes. Gene 311:1–11PubMedCrossRefGoogle Scholar
  32. 32.
    Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  33. 33.
    Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300PubMedCrossRefGoogle Scholar
  34. 34.
    Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327PubMedCrossRefGoogle Scholar
  35. 35.
    Hayashi T, Kobayashi D, Kariu T, Tahara M, Hada K, Kouzuma Y, Kimura M (2003) Genomic cloning of ribonucleases in Nicotiana glutinosa leaves, as induced in response to wounding or to TMV-infection, and characterization of their promoters. Biosci Biotechnol Biochem 67:2574–2583PubMedCrossRefGoogle Scholar
  36. 36.
    Kidwell MG, Lisch D (1997) Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci USA 94:7704–7711PubMedCrossRefGoogle Scholar
  37. 37.
    McDonald JF (1995) Transposable elements: possible catalysts of organismic evolution. Trends Ecol Evol 10(3):123–126PubMedCrossRefGoogle Scholar
  38. 38.
    Wessler SR, Bureau TE, White SE (1995) LTR retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev 5:814–821PubMedCrossRefGoogle Scholar
  39. 39.
    Shapiro JA, von Sternberg R (2005) Why repetitive DNA is essential to genome function. Biol Rev 80:227–250PubMedCrossRefGoogle Scholar
  40. 40.
    Bichler J, Herrmann RG (1990) Analysis of the promotors of the single-copy genes for plastocyanin and subunit 6 of the chloroplast ATP synthase from spinach. Eur J Biochem 190:415–426PubMedCrossRefGoogle Scholar
  41. 41.
    Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471PubMedCrossRefGoogle Scholar
  42. 42.
    Pastuglia M, Roby D, Dumas C, Cockagi JM (1997) Rapíd induction by Wsunding and bacterial infection of an S gene family receptor-like kinase gene in Brassica oleracea. Plant Cell 9:49–60PubMedCrossRefGoogle Scholar
  43. 43.
    Ross C, Shen QJ (2006) Computational prediction and experimental verification of HVA1-like abscisic acid responsive promoters in rice (Oryza sativa). Plant Mol Biol 62:233–246PubMedCrossRefGoogle Scholar
  44. 44.
    Dahl MK, Degenkolb J, Hillen W (1994) Transcription of the xyl operon is controlled in Bacillus subtilis by tandem overlapping operators spaced by 4 bp. J Mol Biol 243:413–424PubMedCrossRefGoogle Scholar
  45. 45.
    Giuliano G, Pichersky E, Malik VS, Timko MP, Scolnik PA, Cashmore AR (1988) An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci USA 85:7089–7093PubMedCrossRefGoogle Scholar
  46. 46.
    Schulze-Letert P, Becker-Andr M, Schulz W, Hahibrock K, Dangl JL (1989) Functional architecture of the light responsive chalcone synthase promoter from parsley. Plant Cell 1:707–714CrossRefGoogle Scholar
  47. 47.
    McKendree WL Jr, Ferl RJ (1992) Functional elements of the Arabidopsis Adh promoter include the G-box. Plant Mol Biol 19:859–862PubMedCrossRefGoogle Scholar
  48. 48.
    Liu LB, Ulmasov T, Shi X, Hagen G, Guilfoyle L (1994) Soybean GH3 promoter contains multiple auxin inducible elements. Plant Cell 6:645–657PubMedCrossRefGoogle Scholar
  49. 49.
    Mason HS, DeWald DB, Mullet JE (1993) Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell 5:241–251PubMedCrossRefGoogle Scholar
  50. 50.
    Qin XF, Holuigue L, Horvath DM, Chua NH (1994) Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-7 element. Plant Cell 6:863–874PubMedCrossRefGoogle Scholar
  51. 51.
    Rapacz M, Wolanin B, Hura K, Tyrka M (2008) The effects of cold acclimation on photosynthetic apparatus and the expression of COR14b in four genotypes of barley (Hordeum vulgare) contrasting in their tolerance to freezing and high-light treatment in cold conditions. Ann Bot 101(5):689–699PubMedCrossRefGoogle Scholar
  52. 52.
    Egawa C, Fuminori K, Ishibash M, Nakamura T, Nakamura C, Takumi S (2006) Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. Genes Genet Syst 81:77–91PubMedCrossRefGoogle Scholar
  53. 53.
    Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A (2008) Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Functional Plant Biol 35:412-426CrossRefGoogle Scholar
  54. 54.
    Sugimoto K, Takeda S, Hirochika H (2000) MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defence-related genes. Plant Cell 12:2511–2528PubMedCrossRefGoogle Scholar
  55. 55.
    Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586PubMedCrossRefGoogle Scholar
  56. 56.
    Hayashi K, Yoshida H (2009) Refunctionalization of the ancient rice blast disease resistance gene pit by the recruitment of a retrotransposon as a promoter. Plant J 57:413–425PubMedCrossRefGoogle Scholar
  57. 57.
    Le QH, Melayah D, Bonnivard E, Petit M, Grandbastien MA (2007) Distribution dynamics of the Tnt1 retrotransposon in tobacco. Mol Genet Gen 278:639–651Google Scholar
  58. 58.
    Lenoir A, Lavie L, Prieto JL, Goubely C, Coté JC, Pélissier T, Deragon JM (2001) The evolutionary origin and genomic organization of SINEs in Arabidopsis thaliana. Mol Biol Evol 18:2315–2322PubMedGoogle Scholar
  59. 59.
    White SE, Habera LF, Wessler SR (1994) Retrotransposons in the flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and expression. Proc Natl Acad Sci USA 91:11792–11796PubMedCrossRefGoogle Scholar
  60. 60.
    Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405PubMedCrossRefGoogle Scholar
  61. 61.
    McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Pasqualina Woodrow
    • 1
  • Giovanni Pontecorvo
    • 1
  • Loredana F. Ciarmiello
    • 2
  • Amodio Fuggi
    • 1
  • Petronia Carillo
    • 1
  1. 1.Department of Life ScienceII University of NaplesCasertaItaly
  2. 2.C.R.A. – Fruit Tree Research UnitCasertaItaly

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