AJPS  Vol.4 No.4 , April 2013
AtL1 a Non-LTR Retrotrasposon Fragment in the Genome of Arabidopsis thaliana with Homology to Plants and Animals
Abstract: We report the isolation of AtL1, a 249 bp non-LTR retrotransposon fragment from Arabidopsis thaliana by fingerprinting mRNAs extracted from A. thaliana plants, ecotype Columbia, in different heat stress conditions. Southern blot and PCR analysis suggested that AtL1 occurs as a single- or low-copy insert in the genome of A. thaliana ecotype Columbia. The presence of AtL1 in the genome of different Arabidopsis ecotypes was confirmed by PCR amplification and sequencing thus excluding all possible contamination. A preliminary scan of the AtL1 nucleotide sequence against the EMBL and NCBI databases revealed a high degree of similarity to a group of LINE type L1 retrotransposons of mammals and with a cDNA sequence of Artemisia annua. A phylogenetic analysis of LINE elements from animals and plants placed AtL1 and A. annua sequences in close proximity to some mammalian sequences but distant from the other plants LINE elements including those from Arabidopsis.
Cite this paper: G. Visioli, E. Maestri, E. Polverini, A. Pavesi and N. Marmiroli, "AtL1 a Non-LTR Retrotrasposon Fragment in the Genome of Arabidopsis thaliana with Homology to Plants and Animals," American Journal of Plant Sciences, Vol. 4 No. 4, 2013, pp. 806-816. doi: 10.4236/ajps.2013.44099.

[1]   A. Kumar and J. L. Bennetzen, “Plant Retrotransposons,” Annual Review of Genetics, Vol. 33, 1999, pp. 479-532. doi:10.1146/annurev.genet.33.1.479

[2]   H. L. Levin and J. V. Moran, “Dynamic Interactions between Transposable Elements and Their Hosts,” Nature Reviews Genetics, Vol. 12, No. 9, 2011, pp. 615-627. doi:10.1038/nrg3030

[3]   D. F. Voytas, M. P. Cummings, A. Koniczny, F. M. Ausubel and S. R. Rodermel “Copia-Like Retrotransposons Are Ubiquitous among Plants,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 89, No. 15, 1992, pp. 7124-7128. doi:10.1073/pnas.89.15.7124

[4]   B. A. Dombroski, S. L. Mathias, E. Nanthakumar, A. F. Scott and H. H. Kazazian Jr., “Isolation of an Active Human Transposable Element,” Science, Vol. 254, No. 5039, 1991, pp. 1805-1808. doi:10.1126/science.1662412

[5]   D. D. Loeb, R. W. Padgett, S. C. Hardies, W. R. Shehee, M. B. Comer, M. H. Edgell and C. A. Hutchison III, “The Sequence of a Large L1Md Element Reveals a Tandemly Repeated 5’ End and Several Features Found in Retrotransposons,” Molecular and Cellular Biology, Vol. 6, No. 1, 1986, pp. 168-182. doi:10.1128/MCB.6.1.168

[6]   Z. Schwarz-Sommer, L. Leclercq, E. Goebel and H. Saedler, “Cin4, an Insert Altering the Structure of the A1Gene in Zea mays, Exhibits Properties of Nonviral Retrotransposons,” The EMBO Journal, Vol. 6, No. 13, 1987, pp. 3873-3880.

[7]   P. R. J. Leeton and D. R. Smyth, “An Abundant LINE-Like Element Amplified in the Genome of Lilium speciosum,” Molecular and General Genetics, Vol. 237, No. 1-2, 1993, pp. 97-104. doi:10.1007/BF00282789

[8]   D. A. Wright, N. Ke, J. Smalle, B. M. Hauge, H. M. Goodman and D. F. Voytas, “Multiple Non-LTR Retrotransposons in the Genome of Arabidopsis thaliana,” Genetics, Vol. 142, No. 2, 1996, pp. 569-578.

[9]   T. Higashiyama, Y. Noutoshi, M. Fujie and T. Yamada, “Zepp, a LINE-Like Retrotransposon Accumulated in the Chlorella Telomeric Region,” The EMBO Journal, Vol. 16, No. 12, 1997, pp. 3715-3723. doi:10.1093/emboj/16.12.3715

[10]   M. Komatsu, K. Shimamoto and J. Kyozuka, “Two-Step Regulation and Continuous Retrotransposition of the Rice LINE-Type Retrotransposon Karma,” The Plant Cell, Vol. 15, No. 8, 2003, pp. 1934-1944.doi:10.1105/tpc.011809

[11]   K. Noma, H. Ohtsubo and E. Ohtsubo, “ATLN Elements, LINEs from Arabidopsis thaliana: Identification and Characterisation,” DNA Research, Vol. 7, No. 5, 2000, pp. 291-303.doi:10.1093/dnares/7.5.291

[12]   K. Sakamoto, N. Ohmido, K. Fukui, H. Kamada and S. Satoh, “Site Specific Accumulation of a LINE-Like Retrotransposon in a Sex Chromosome of the Dioecious Plant Cannabis sativa,” Plant Molecular Biology, Vol. 44, No. 6, 2000, pp. 723-732.doi:10.1023/A:1026574405717

[13]   V. Vershinin, A. Druka, A. G. Alkhimova, A. Kleinhofs and J. S. Heslop-Harrison, “LINEs and gypsy-Like Retrotransposons in HordeumSpecies,” Plant Molecular Biology, Vol. 49, No. 1, 2002, pp. 1-14. doi:10.1023/A:1014469830680

[14]   H. Yamashita and M. Tahara, “A LINE-Type Retrotransposon Active in Meristem Stem Cells Causes Heritable Transpositions in the Sweet Potato Genome,” Plant Molecular Biology, Vol. 61, No. 1-2, 2006, pp. 79-94. doi:10.1007/s11103-005-6002-9

[15]   T. Schmidt, S. Kubis and J. S. Heslop-Harrison, “Analysis and Chromosomal Localization of Retrotransposons in Sugar Beet (Beta vulgaris L.): LINEs and Ty1-Copia-Like Elements as Major Components of the Genome,” Chromosome Research, Vol. 3, No. 6, 1995, pp. 335-345. doi:10.1007/BF00710014

[16]   T. Wenke, D. Holtgraewe, A. V. Horn, B. Weisshaar and T. Schmidt, “An Abundant and Heavily Truncated Non- LTR Retrotransposon (LINE) Family in Beta vulgaris,” Plant Molecular Biology, Vol. 71, No. 6, 2009, pp. 585- 597. doi:10.1007/s11103-009-9542-6

[17]   J. S. Hawkins, G. Hu, R. A. Rapp, J. L. Grafenberg and J. F. Wendel, “Phylogenetic Determination of the Pace of Transposable Element Proliferation in Plants: copia and LINE-Like Elements in Gossypium,” Genome, Vol. 51, No. 1, 2008, pp. 11-18. doi:10.1139/G07-099

[18]   S. E. Kubis, J. S. Heslop-Harrison, C. Desel and T. Schmidt, “The Genomic Organization of non-LTR Retransposons (LINEs) from Three Beta Species and Five Other Angiosperms,” Plant Molecular Biology, Vol. 36, No. 6, 1998, pp. 821-831. doi:10.1023/A:1005973932556

[19]   C. Feschotte, N. Jiang and S. R. Wessler, “Plant Transposable Elements: Where Genetics Meets Genomics,” Nature Reviews Genetics, Vol. 3, No. 5, 2002, pp. 329- 341. doi:10.1038/nrg793

[20]   V. Knoop, U. Unseld, J. Marienfeld, P. Brandt, S. Sunkel, H. Ullrich and A. Brennicke, “Copia-, gypsy- and LINE- Like Retrotransposon Fragments in the Mitochondrial Genome of Arabidopsis thaliana,” Genetics, Vol. 142, No. 2, 1996, pp. 579-585.

[21]   H. Ito, H. Gaubert, E. Bucher, M. Mirouze, I. Vaillant and J. Paszkowski, “An siRNA Pathway Prevents Transgenerational Retrotransposition in Plants Subjected to Stress,” Nature, Vol. 472, No. 7341, 2011, pp. 115-119. doi:10.1038/nature09861

[22]   M. A. Grandbastien, “Activation of Plant Retrotransposons under Stress Conditions,” Trends in Plant Science, Vol. 3, No. 5, 1998, pp. 181-187. doi:10.1016/S1360-1385(98)01232-1

[23]   J. M. Deragon, N. Gilbert, L. Rouquet, A. Lenoir, P. Arnaud and G. Picard, “A Transcriptional Analysis of the S1Bn (Brassica napus) Family of SINE Retroposons,” Plant Molecular Biology, Vol. 32, No. 5, 1996, pp. 869- 878. doi:10.1007/BF00020484

[24]   M. L. Chye, K. Y. Cheung and J. Xu, “Characterization of TSCL, a Nonviral Retroposon from Arabidopsis thaliana,” Plant Molecular Biology, Vol. 35, No. 6, 1997, pp. 893-904. doi:10.1023/A:1005947804227

[25]   T. Murashige and F. Skoog, “A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures,” Physiologia Plantarum, Vol. 15, No. 3, 1962, pp. 473-497. doi:10.1111/j.1399-3054.1962.tb08052.x

[26]   G. Visioli, E. Maestri and N. Marmiroli, “Differential Display-Mediated Isolation of a Genomic Sequence for a Putative Mitochondrial LMW HSP Specifically Expressed in Condition of Induced Thermotolerance in Arabidopsis thaliana (L.) Heynh,” Plant Molecular Biology, Vol. 34, No. 3, 1997, pp. 517-527. doi:10.1023/A:1005824314022

[27]   A. J. van Tunen, R. E. Koes, C. E. Spelt, A. R. van der Krol, A. R. Stuitje and J. N. M. Mol, “Cloning of the Two Chalcone Flavanone Isomerase Genes from Petunia hybrida: Coordinate, Light-Regulated and Differential Expression of Flavonoid Genes,” The EMBO Journal, Vol. 7, No. 5, 1988, pp. 1257-1263.

[28]   P. Liang and A. B. Pardee, “Differential Display of Eukaryotic Messenger RNA by Means of the Polymerase Chain Reaction,” Science, Vol. 257, No. 5072, 1992, pp. 967-971. doi:10.1126/science.1354393

[29]   J. Sambrook, E. F. Fritsch and T. Maniatis, “Molecular Cloning: A Laboratory Manual,” 2nd Edition, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 1989.

[30]   A. P. Feinberg and B. Vogelstein, “A Technique for Radiolabelling DNA Restriction Endonuclease Fragments to High Specific Activity,” Analytical Biochemistry, Vol. 132, No. 1, 1983, pp. 6-13. doi:10.1016/0003-2697(83)90418-9

[31]   W. R. Pearson and D. J. Lipman, “Improved Tools for Biological Sequence Comparisons,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 85, No. 8, 1988, pp. 2444-2448. doi:10.1073/pnas.85.8.2444

[32]   M. A. Larkin, G. Blackshields, N. P. Brown, et al., “Clustal W and Clustal X Version 2.0,” Bioinformatics, Vol. 23, No. 21, 2007, pp. 2947-2948. doi:10.1093/bioinformatics/btm404

[33]   S. Henikoff and J. G. Henikoff, “Amino Acid Substitution Matrices from Protein Blocks,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 89, No. 22, 1992, pp. 10915-10919. doi:10.1073/pnas.89.22.10915

[34]   M. Waterhouse, J. B. Procter, D. M. A Martin, M. Clamp and G. J. Barton, “Jalview Version 2—A Multiple Sequence Alignment Editor and Analysis Workbench,” Bio- informatics, Vol. 25, No. 9, 2009, pp. 1189-1191. doi:10.1093/bioinformatics/btp033

[35]   K. Tamura, J. Dudley, M. Nei and S. Kumar, “MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0,” Molecular Biology and Evolution, Vol. 24, No. 8, 2007, pp. 1596-1599. doi:10.1093/molbev/msm092

[36]   N. Saitou and M. Nei, “The Neighbor-Joining Method: A New Method for Reconstructing Phylogenetic Trees,” Molecular Biology and Evolution, Vol. 4, No. 4, 1987, pp. 406-425.

[37]   S. R. Wessler, “Plant Retrotransposons: Turned on by Stress,” Current Biology, Vol. 6, No. 8, 1996, pp. 959- 961. doi:10.1016/S0960-9822(02)00638-3

[38]   D. Lisch, “How Important Are Transposons for Plant Evolution?” Nature Reviews Genetics, Vol. 14, No. 1, 2013, pp. 49-61.doi:10.1038/nrg3374

[39]   S. Takeda, K. Sugimoto, H. Otsuki and H. Hirochika, “A 13-bp 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,” The Plant Journal, Vol. 18, No. 4, 1999, pp. 383-393. doi:10.1046/j.1365-313X.1999.00460.x

[40]   S. Vernhettes, M. A. Grandbastien and J. M. Casacuberta, “In Vivo Characterization of Transcriptional Regulatory Sequences Involved in the Defence-Associated Expression of the Tobacco Retrotransposon Tnt1,” Plant Molecular Biology, Vol. 35, No. 5, 1997, pp. 673-679. doi:10.1023/A:1005826605598

[41]   V. Zupunski, F. Gubensek and D. Kordis, “Evolutionary Dynamics and Evolutionary History in the RTE Clade of Non-LTR Retrotransposons,” Molecular Biology and Evolution, Vol. 18, No. 10, 2001, pp. 1849-1863. doi:10.1093/oxfordjournals.molbev.a003727

[42]   H. S. Malik, W. D. Burke and T. H. Eickbush, “The Age and Evolution of Non-LTR Retrotransposable Elements,” Molecular Biology and Evolution, Vol. 16, No. 6, 1999, pp. 793-805. doi:10.1093/oxfordjournals.molbev.a026164

[43]   F. Bushman, “Lateral DNA Transfer: Mechanisms and Consequences,” Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 2002.

[44]   S. Schaack, C. Gilbert and C. Feschotte, “Promiscuous DNA: Horizontal Transfer of Transposable Elements and Why It Matters for Eukaryotic Evolution,” Trends in Ecology and Evolution, Vol. 25, No. 9, 2010, pp. 537-546. doi:10.1016/j.tree.2010.06.001

[45]   M. A. Grandbastien, A. Spielmann and M. Caboche, “Tnt1, a Mobile Retroviral-Like Transposable Element of Tobacco Isolated by Plant Cell Genetics,” Nature, Vol. 337, No. 6205, 1989, pp. 376-380.doi:10.1038/337376a0

[46]   A. Konieczny, D. F. Voytas, M. P. Cummings and F. M. Ausubel, “A Superfamily of Arabidopsis thaliana Retrotransposons,” Genetics, Vol. 127, No. 4, 1991, pp. 801- 809.

[47]   J. Pozueta-Romero, G. Houlné, and R. Schantz, “Identification of a Short Interspersed Repetitive Element in Partially Spliced Transcripts of the Bell Pepper (Capsicum annuum) PAPGene: New Evolutionary and Regulatory Aspects on Plant tRNA-Related SINEs,” Gene, Vol. 214, No. 1-2, 1998, pp. 51-58. doi:10.1016/S0378-1119(98)00217-0

[48]   F. Martin-Laurent, D. van Tuinen, E. Dumas-Gaudot, V. Gianinazzi-Pearson, S. Gianinazzi and P. Franken, “Differential Display Analysis of RNA Accumulation in Arbuscular Mycorrhiza of Pea and Isolation of a Novel Symbiosis-Regulated Plant Gene,” Molecular and General Genetics, Vol. 256, No. 1, 1997, pp. 37-44. doi:10.1007/s004380050543

[49]   D. Kordis and F. Gubensek, “Unusual Horizontal Transfer of a Long Interspersed Nuclear Element between Distant Vertebrate Classes,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 95, No. 18, 1998, pp. 10704-10709. doi:10.1073/pnas.95.18.10704

[50]   A. Morton Walsh, R. D. Kortschak, M. G. Gardner, T. Bertozzi and D. L. Adelson, “Widespread Horizontal Transfer of Retrotransposons,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 110, No. 3, 2013, pp. 1012-1016. doi:10.1073/pnas.1205856110

[51]   A. Roulin, B. Piegu, P. M. Fortune, et al., “Whole Genome Surveys of Rice, Maize and Sorghum Reveal Multiple Horizontal Transfers of the LTR-Retrotransposon Route 66 in Poaceae,” BMC Evolutionary Biology, Vol. 9, 2009, Article 58. doi:10.1186/1471-2148-9-58

[52]   K. R. Oliver and W. K. Greene, “Transposable Elements: Powerful Facilitators of Evolution,” BioEssays, Vol. 31, No. 7, 2009, pp. 703-714. doi:10.1002/bies.200800219

[53]   J. C. Silva, E. L. Loreto and J. B. Clark, “Factors That Affect the Horizontal Transfer of Transposable Elements,” Current Issues in Molecular Biology, Vol. 6, No. 1, 2004, pp. 57-71.

[54]   M. G. Kidwell, “Lateral Transfer in Natural Populations of Eukaryotes,” Annual Review of Genetics, Vol. 27, 1993, pp. 235-256. doi:10.1146/annurev.genet.27.1.235

[55]   P. J. Keeling and J. D. Palmer, “Horizontal Gene Transfer in Eukaryotic Evolution,” Nature Reviews Genetics, Vol. 9, No. 8, 2008, pp. 605-618. doi:10.1038/nrg2386

[56]   M. Yoshiyama, Z. Tu, Y. Kainoh, H. Honda, T. Shono and K. Kimura, “Possible Horizontal Transfer of a Transposable Element from Host to Parasitoid,” Molecular Biology and Evolution, Vol. 18, No. 10, 2001, pp. 1952- 1958. doi:10.1093/oxfordjournals.molbev.a003735

[57]   C. Gilbert, S. Schaack, J. K. Pace, P. J. Brindley and C. Feschotte, “A Role for Host-Parasite Interactions in the Horizontal Transfer of Transposons across Phyla,” Nature, Vol. 464, No. 7293, 2010, pp. 1347-1350. doi:10.1038/nature08939