Development and Characterisation of Irap Markers From Expressed Retrotransposon-like sequences in Pinus sylvestris L.

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Abstract

Conifer genomes are large and stably diploid, in contrast to angiosperms, which are more variable both in genome size and ploidy. Conifer genomes are characterised by multiple gene families and pseudogenes, contain large inter-gene regions and a considerable proportion of repetitive sequences. All members of plant retrotransposon orders have been identified in gymnosperm genomes, however active elements have not been described. Investigation of transposable elements in Scots pine (Pinus sylvestris L.) could offer insights into transposon-mediated reorganisation under stress conditions in complex and ancient plant genomes. Nine Pinus sylvestris specific markers were developed to hypothetical long terminal repeats (LTRs) from differentially expressed retrotransposon-like fragments after heat stress and insect damage. Genetic diversity of 150 trees from a naturally regenerated pine stand was investigated using the IRAP method. The developed markers revealed high levels of genetic diversity and were able to distinguish subpopulations growing in long-term differential environmental conditions. Somaclonal variation was also investigated using these markers and polymorphic fragments were identified between ramets of Scots pine clones growing in two different plantations, possibly indicating evidence of recent transposition events. Sequencing of the polymorphic fragments identified two groups of sequences containing LTR sequences of an unknown retrotransposon with homology to the LTRs of the Copia-17-PAb-I element.

Asif, J. M., Othman, F. Y. (2005). Characterization of fusarium wilt-resistant and fusarium wilt-susceptible somaclones of banana cultivar Rastali (Musa AAB) by random amplified polymorphic DNA and retrotransposon markers. Plant Mol. Biol. Rep., 23 (3), 241–249.

Bairu, M. W., Aremu, A. O., Staden, J. V. (2011). Somaclonal variation in plants: Causes and detection methods. Plant Growth Regul., 63, 147–173.

Baranek, M., Meszaros, M., Sochorova, J., Cechova, J., Raddova, J. (2012). Utility of retrotransposon-derived marker systems for differentiation of presumed clones of the apricot cultivar Velkopavlovická. Sci. Horticult., 143, 1–6.

Bayram, E., Yilmaz, S., Hamat-Mecbur, H., Kartal-Alacam, G., Gozukirmizi, N. (2012). Nikita retrotransposon movements in callus cultures of barley (Hordeum vulgare L.). Plant Omics Journal (POJ), 5 (3), 211–215.

Benachenhou, F., Sperber, G. O., Bongcam-Rudloff, E., Andersson, G., Boeke, J. D., Blomberg, J. (2013). Conserved structure and inferred evolutionary history of long terminal repeats (LTRs). Mobile DNA, doi: 10.1186/1759-8753-4-5.

Berg, D. E., Howe, M. H. (eds.) (1989). Mobile DNA. Washington, D.C.: American Society for Microbiology Press.

Birnboim, H. C., Doly, J. (1979). A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucl. Acids Res., 7 (6), 1513–1523.

Brandes, A., Heslop-Harrison, J. S., Kamm, A., Kubis, S., Doudrick, R. L., Schmidt, T. (1997). Comparative analysis of the chromosomal and genomic organization of Ty1-copia -like retrotransposons in pteridophytes, gymnosperms and angiosperms. Plant Mol. Biol., 33 (1), 11–21.

Campbell, B. C., LeMare, S., Piperidis, G., Godwin, I. D. (2011). IRAP, a retrotransposon-based marker system for the detection of somaclonal variation in barley. Mol. Breed., 27, 193–206.

Capy, P. (2005). Classification and nomenclature of retrotransposable elements. Cytogenet. Gen. Res., 110 (1–4), 457–461.

Capy, P., Gasperi, G., Biemont, C., Bazin, C. (2000). Stress and transposable elements: Co-evolution or useful parasites? Heredity, 85, 101–106.

Carvalho, A., Guedes-Pinto, H., Lima-Brito, J. E. (2012). Genetic diversity in old Portuguese durum wheat cultivars assessed by retrotransposon-based markers. Plant Mol. Biol. Rep., 30, 578–589.

Castro, I., D’Onofrio, C., Martín, J. P., Ortiz, J. M., De Lorenzis, G., Ferreira, V., Pinto-Carnide, O. (2012). Effectiveness of AFLPs and retrotransposon-based markers for the identification of Portuguese grapevine cultivars and clones. Mol. Biotechnol., 52 (1), 26–39.

D’Onofrio, C., De Lorenzis, G., Giordani, T., Natali, L., Cavallini, A., Scalabrelli, G. (2010). Retrotransposon-based molecular markers for grapevine species and cultivars identification. Tree Genet. Gen., 6, 451–466.

Feschotte, C., Jiang, N., Wessler, S. R. (2002). Plant transposable elements: Where genetics meets genomics. Nat. Rev. Genet., 3, 329–341.

Finnegan, D. J. (1989). Eukaryotic transposable elements and genome evolution. Trends. Genet., 5, 103–107.

Flavell, A. J., Pearce, S. R., Kumar, A. (1994). Plant transposable elements and the genome. Curr. Opin. Genet. Dev., 4, 838–844.

Friesen, N., Brandes, A., Heslop-Harrison, J. S. (2001). Diversity, origin and distribution of retrotransposons (gypsy and copia) in conifers. Mol. Biol. Evol., 18 (7), 1176–1188.

Gao, D., Chen, J., Chen, M., Meyers, B. C., Jackson, S. (2012). A highly conserved, small LTR retrotransposon that preferentially targets genes in grass genomes. PloS One, doi:10.1371/journal.pone.0032010.

Grandbastien, M. A., Lucas, H., Morel, J. B., Corinne, M. C., Vernhettes, S., Casacuberta, J. M. (1997). The expression of the tobacco Tnt1 retrotransposon is linked to plant defense responses. Genetica, 100, 241–252.

Inoue, H., Nojima, H., Okayama, H. (1990). High efficiency transformation of Escherichia coli with plasmids. Gene, 96, 23–28.

Ito, H., Gaubert, H., Bucher, E., Mirouze, M., Vaillant, I., Paszkowski, J. (2011). An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature, 472, 115–118.

Kalendar, R., Antonius, K., Smykal, P., Schulman, A.H. (2010). iPBS: A universal method for DNA fingerprinting and retrotransposon isolation. Theor. Appl. Genet., doi:10.1007/s00122-010-1398-2.

Kalendar, R., Grob, T., Regina, M., Suoniemi, A., Schulman, A. (1999). IRAP and REMAP: Two new retrotransposon-based DNA fingerprinting techniques. Theor. Appl. Genet., 98, 704–711.

Kalendar, R., Schulman, A. H. (2007). IRAP and REMAP for retrotransposon-based genotyping and fingerprinting. Nat. Protoc., 1 (5), 2478–2484.

Kamm, A., Doudric, R. L., Heslop-Harrison, J. S., Schmidt, T. (1996). The genomic and physical organization of Ty1-copia -like sequences as a component of large genomes in Pinus elliottii var. elliottii and other gymnosperms. Proc. Natl. Acad. Sci. USA, 93, 2708–2713.

Knight, C. A., Ackerly, D. D. (2002). Variation in nuclear DNA content across environmental gradients: A quantile regression analysis. Ecol. Lett., 5, 66–76.

Kohany, O., Gentles, A. J., Hankus, L., Jurka, J. (2006). Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics, doi:10.1186/1471-2105-7-474.

Kossack, D. S., Kinlaw, C. S. (1999). IFG, a gypsy -like retrotransposon in Pinus (Pinaceae), has an extensive history in pines. Plant Mol. Biol., 39, 417–426.

Kovach, A., Wegrzyn, J. L., Parra, G., Holt, C., Bruening, G. E., Loopstra, C. A., Hartigan, J., Yandell, M., Langley, C. H., Korf, I., Neale, D. B. (2010). The Pinus taeda genome is characterized by diverse and highly diverged repetitive sequences. BMC Genomics, doi: 10.1186/1471-2164-11-420.

Kumar, A., Bennetzen, J. L. (1999). Plant Retrotransposons. Annu. Rev. Genet., 33, 479–532.

Kumar, A., Hirochika, H. (2001). Applications of retrotransposons as genetic tools in plant biology. Trends Plant Sci., 6 (3), 127–134.

Kumar, A., Pearce, S. R., McLean, K., Harrison, G., Heslop-Harrison, J. S., Waugh, R., Flavell, A. J. (1997). The Ty1-copia group of retrotransposons in plants: Genomic organisation, evolution, and use as molecular markers. Genetica, 100 (1–3), 205–217.

L’Homme, Y., Seguin, A., Tremblay, F. M. (2000). Different classes of retrotransposons in coniferous spruce species. Genome, 43, 1084–1089.

Leitch, I. J., Bennett, M. D. (2004). Genome downsizing in polyploid plants. Biol. J. Linn. Soc., 82, 651–663.

Lightbourn, G. J., Jelesko, J. G., Veilleux, R. E. (2007). Retrotransposonbased markers from potato monoploids used in somatic hybridization. Genome, 50 (5), 492–501.

Mak, J., Kleiman, L. (1997). Primer tRNAs for reverse transcription. J. Virol., 71 (11), 8087–8095.

McClintock, B. (1984). The significance of responses of the genome to challenge. Science, 226, 792–801.

Mignone, F., Grillo, G., Licciulli, F., Iacono, M., Liuni, S., Kersey, P. J., Duarte, J., Saccone, C. Pesole, G. (2005). UTRdb and UTRsite: A collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucl. Acids Res., 33, D141–146.

Miguel, C., Simoes, M., Oliveira, M. M., Rocheta, M. (2008). Envelope-like retrotransposons in the plant kingdom: Evidence of their presence in Gymnosperms (Pinus pinaster). J. Mol. Evol., 67, 517–525.

Murray, B.G. (1998). Nuclear DNA amounts in gymnosperms. Ann. Bot., 82, 3–15.

Murray, B.G. (2005). When does intraspecific C-value variation become taxonomically significant? Ann. Bot., 95, 119–125.

Neumann, P., Pozárková, D., Macas, J. (2003). Highly abundant pea LTR Retrotransposon Ogre is constitutively transcribed and partially spliced. Plant. Mol. Biol., 53 (3), 399–410.

Nystedt, B., Street, N. R., Wetterbom, A., Zuccolo, A., Lin, Y. C., Scofield, D. G., Vezzi, F., Delhomme, N., Giacomello, S., Alexeyenko, A., Vicedomini, R., Sahlin, K., Sherwood, E., Elfstrand, M., Gramzow, L., Holmberg, K., Hällman, J., Keech, O., Klasson, L., Koriabine, M., Kucukoglu, M., Käller, M., Luthman, J., Lysholm, F., Niittylä, T., Olson, A., Rilakovic, N., Ritland, C., Rosselló, J.A., Sena, J., Svensson, T., Talavera-López, C., Theißen, G., Tuominen, H., Vanneste, K., Wu, Z. Q., Zhang, B., Zerbe, P., Arvestad, L., Bhalerao, R., Bohlmann, J., Bousquet, J., Garcia, G. R., Hvidsten, T. R., de Jong, P., MacKay, J., Morgante, M., Ritland, K., Sundberg, B., Thompson, S. L., Van de Peer, Y., Andersson, B., Nilsson, O., Ingvarsson, P.K., Lundeberg, J., Jansson, S. (2013). The Norway spruce genome sequence and conifer genome evolution. Nature, doi:10.1038/nature12211.

Peakall, R., Smouse, P. E. (2006). GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes, 6, 288–295.

Porebski, S., Bailey, G. L., Baum, B. R. (1997). Modification of a CTAB DNA extraction protocol for plants containing high polysaharide and polyphenol componenets. Plant Mol. Biol. Rep., 15 (1), 8–15.

Rocheta, M., Cordeiro, J., Oliveira, M., Miguel, C. (2007). PpRT1: The first complete gypsy -like retrotransposon isolated in Pinus pinaster. Planta, 225, 551–562.

Saeidi, H., Rahiminejad, M. R., Heslop-Harrison, J. S. (2008). Retroelement insertional polymorphisms, diversity and phylogeography within diploid, D-genome Aegilops tauschii (Triticeae, Poaceae) sub-taxa in Iran. Ann. Bot., 101 (6), 855–861.

Schlüter, P. M., Harris, S. A. (2006). Analysis of multilocus fingerprinting data sets containing missing data. Mol. Ecol. Notes, 6, 569–572.

Schulman, A. H. (2007). Molecular markers to assess genetic diversity. Euphytica, 158, 313–321.

Schulman, A. H., Flavell, A. J., Ellis, T. H. (2004). The application of LTR retrotransposons as molecular markers in plants. Meth. Mol. Biol., 260, 145–173.

Schulman, A. H., Flavell, A. J., Paux, E., Ellis, T. H. (2012). The application of LTR retrotransposons as molecular markers in plants. Meth. Mol. Biol., 859, 115–153.

Solovyev, V. V. (2002). Structure, properties and computer identification of eukaryotic genes. In: Bioinformatics Genomes to Drugs, Basic Technologies (59–111 pp.). Lengauer, T. (ed.). Wiley.

Solovyev, V. V., Shahmuradov, I. A. (2003). PromH: Promoters identification using orthologous genomic sequences. Nucl. Acids Res., 31 (13), 3540–3545.

Soranzo, N., Provan, J., Powell, W. (1998). Characterization of microsatellite loci in Pinus sylvestris L. Mol. Ecol., 7, 1247–1263.

Stuart-Rogers, C., Flavell, A. J. (2001). The evolution of Ty1-copia group retrotransposons in gymnosperms. Mol. Biol. Evol., 18 (2), 155–163.

Subudhi, P., Magpantay, G., Karan, R. (2013) A retrotransposon-based probe for fingerprinting and evolutionary studies in rice (Oryza sativa). Genet. Res. Crop. Evol., 60 (4), 1263–1273.

Tam, S. M., Mhiri, C., Vogelaar, A., Kerkveld, M., Pearce, S. R., Grandbastien, M. A. (2005). Comparative analyses of genetic diversities within tomato and pepper collections detected by retrotransposon-based SSAP, AFLP and SSR. Theor. Appl. Genet., 110 (5), 819–831.

Vicient, C. M., Kalendar, R., Schulman, A. H. (2005). Variability, recombination and mosaic evolution of the barley BARE-1 retrotransposon. J. Mol. Evol., 61, 275–291.

Voronova, A., Jansons, A., Ruòìis, D. (2011). Expression of retrotransposon-like sequences in Scots pine (Pinus sylvestris L.) in response to heat stress. Environ. Exper. Biol., 9, 121–127.

Wessler, S. R. (1996). Plant retrotransposons: Turned on by stress. Curr. Biol., 6 (8), 959–961.

Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J. L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., Paux, E., SanMiguel, P., Schulman, A. H. (2007) A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet., 8 (12), 973–982.

Xiong, Y., Eickbush, T. H. (1990). Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J., 9, 3353–3362.

Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., Madden, T. (2012). Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics, doi:10.1186/1471-2105-13-134.

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