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Transposable Elements in Spruce

  • Giovanni Marturano
  • Camilla Canovi
  • Federico Rossi
  • Andrea ZuccoloEmail author
Chapter
  • 134 Downloads
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

Transposable elements (TEs), along with other repetitive sequences, were dismissed for a long time as junk DNA. Over the years, much evidence accumulated, clarifying how TEs are instead major components of host genomes and have a substantial role in shaping genome structure, functioning, and evolution. In plants, TEs were mostly studied in important model and crop species, in particular, Arabidopsis, rice, and maize. The studies focusing on TEs in gymnosperms lagged behind for different reasons, last but not least, the enormous genome sizes for most species belonging to this group. Recently, the decrease in sequencing cost and advances in assembly algorithms allowed whole-genome sequencing of conifers such as Norway spruce, white spruce, and loblolly pine (Nystedt et al. 2013, Birol et al. 2013, Neale et al. 2014). The availability of such genomic data enabled a more comprehensive and insightful study of TEs starting to depict patterns quite different from the ones already described for angiosperms. In this chapter, we present and discuss the available and newly generated data regarding Norway spruce TEs comparing evidence gathered from genomic and transcriptomic analyses with analogous data of other conifers, crops, and model species, pointing out similarities and differences.

Keywords

Transposable elements Long terminal repeat retrotransposons Genome size Unequal recombination Methylation 

References

  1. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796–815Google Scholar
  2. Ausin I, Feng S, Yu C, Liu W, Kuo HY et al (2016) DNA methylome of the 20-gigabase Norway spruce genome. Proc Natl Acad Sci USA 113(50):E8106–E8113PubMedGoogle Scholar
  3. Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A et al (2009) Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet 5(11):e1000732PubMedPubMedCentralGoogle Scholar
  4. Birol I, Raymond A, Jackman SD, Pleasance S, Coope R et al (2013) Assembling the 20 Gb white spruce (Picea glauca) genome from whole-genome shotgun sequencing data. Bioinformatics 29(12):1492–1497Google Scholar
  5. Brookfield JF (2005) The ecology of the genome-mobile DNA elements and their hosts. Nature Rev. Genet 6(2):128–136PubMedGoogle Scholar
  6. Bouillé M, Bousquet J (2005) Trans-species shared polymorphisms at orthologous gene loci among distant species in the conifer Picea (Pinaceae): implications for the long-term maintenance of genetic diversity in trees. Am J Bot 92:63–73PubMedGoogle Scholar
  7. Bundock P, Hooykaas P (2005) An Arabidopsis hAT-like transposase is essential for plant development. Nature 436(7048):282–284PubMedGoogle Scholar
  8. Charlesworth B, Borthwick H, Bartolome C, Pignatelli P (2004) Estimates of the genomic mutation rate for detrimental alleles in Drosophila melanogaster. Genetics 167(2):815–826PubMedPubMedCentralGoogle Scholar
  9. Chénais B, Caruso A, Hiard S, Casse N (2012) The impact of transposable elements on eukaryotic genomes: From genome size increase to genetic adaptation to stressful environments. Gene 509(1):7–15PubMedGoogle Scholar
  10. Colomé-Tatché M, Cortijo S, Wardenaar R, Morgado L, Lahouze B et al (2012) Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc Natl Acad Sci USA 109(40):16240–16245PubMedGoogle Scholar
  11. Cossu RM, Casola C, Giacomello S, Vidalis A, Scofield DG, Zuccolo A (2017) LTR retrotransposons show low levels of unequal recombination and high rates of intraelement gene conversion in large plant genomes. Genome Biol Evol 9(12):3449–3462PubMedPubMedCentralGoogle Scholar
  12. Cowan RK, Hoen DR, Schoen DJ, Bureau TE (2005) MUSTANG is a novel family of domesticated transposase genes found in diverse angiosperms. Mol Biol Evol 22(10):2084–2089PubMedGoogle Scholar
  13. Dawkins R (1976) The selfish gene. Oxford University Press, New York, p 2Google Scholar
  14. Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12(7):1075–1079PubMedPubMedCentralGoogle Scholar
  15. De Souza FS, Franchini LF, Rubinstein M (2013) Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong? Mol Biol Evol 30(6):1239–1251PubMedPubMedCentralGoogle Scholar
  16. Dubcovsky J, Ramakrishna W, SanMiguel PJ, Busso CS, Yan L et al (2001) Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes. Plant Physiol 125(3):1342–1353PubMedPubMedCentralGoogle Scholar
  17. El Baidouri M, Panaud O (2013) Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biol Evol 5(5):954–965PubMedPubMedCentralGoogle Scholar
  18. Fedoroff NV (1998) Discoveries in plant biology (Kung S-D, Yang S-F (eds), vol. 1. World Scientific, Singapore, pp 89–104Google Scholar
  19. Fedoroff NV (2012). Presidential address. Transposable elements, epigenetics, and genome evolution. Science 338(6108):758–767Google Scholar
  20. Finnegan DJ (1989) Eukaryotic transposable elements and genome evolution. Trends Genet 5:103–107PubMedGoogle Scholar
  21. Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA 99(14):9573–9578PubMedGoogle Scholar
  22. Gaut BS, Ross-Ibarra J (2008) Selection on major components of angiosperm genomes. Science 320(5875):484–486PubMedGoogle Scholar
  23. Greilhuber J, Borsch T, Müller K, Worberg A, Porembski S, Barthlott (2006) Smallest angiosperm genomes found in Lentibulariaceae, with chromosomes of bacterial size. Plant Biol 8(6):770–777PubMedGoogle Scholar
  24. Grzebelus D (2018) The functional impact of transposable elements on the diversity of plant genomes. Diversity 10(2):18Google Scholar
  25. Guan R, Zhao Y, Zhang H, Fan G, Liu X, Zhou W, Shi C, Wang J, Liu W, Liang X, Fu Y, Ma K, Zhao L, Zhang F, Lu Z, Lee SM, Xu X, Wang J, Yang H, Fu C, Ge S, Chen W (2016) Draft genome of the living fossil Ginkgo biloba. Gigascience. 5(1):49PubMedPubMedCentralGoogle Scholar
  26. Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF (2006) Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res 16(10):1252–1261PubMedPubMedCentralGoogle Scholar
  27. Hudson ME, Lisch DR, Quail PH (2003) The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J 34(4):453–471PubMedGoogle Scholar
  28. Joly-Lopez Z, Bureau TE (2018) Exaptation of transposable element coding sequences. Curr Opin Genet Dev 49:34–42PubMedGoogle Scholar
  29. Kolosha VO, Martin SL (2003) High-affinity, non-sequence-specific RNA binding by the open reading frame 1 (ORF1) protein from long interspersed nuclear element 1 (LINE-1). J Biol Chem 278(10):8112–8117PubMedGoogle Scholar
  30. Leslie AB, Beaulieu JM, Rai HS, Crane PR, Donoghue MJ et al (2012) Hemisphere-scale differences in conifer evolutionary dynamics. Proc Natl Acad Sci USA 109(40):16217–16221PubMedGoogle Scholar
  31. Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66PubMedGoogle Scholar
  32. Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14(1):49–61PubMedGoogle Scholar
  33. Liu R, Bennetzen JL (2008) Enchilada redux: how complete is your genome sequence? New Phytol 179(2):249–250PubMedGoogle Scholar
  34. Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14(5):860–869PubMedPubMedCentralGoogle Scholar
  35. Ma JX, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA 101:12404–12410PubMedGoogle Scholar
  36. Magbanua ZV, Ozkan S, Bartlett BD, Chouvarine P, Saski CA et al (2011) Adventures in the enormous: A 1.8 million clone BAC library for the 21.7 Gb genome of loblolly pine. PLoS One 6(1):e16214Google Scholar
  37. Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN, RossEIbarra J, Springer NM (2015) Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genet 11(1):e1004915PubMedPubMedCentralGoogle Scholar
  38. Martin SL, Cruceanu M, Branciforte D, Li PWL, Kwok SC et al (2005) LINE-1 retrotransposition requires the nucleic acid chaperone activity of the ORF1 protein. J Mol Biol 348(3):549–561PubMedGoogle Scholar
  39. McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801PubMedGoogle Scholar
  40. Mirouze M, Lieberman-Lazarovich M, Aversano R, Bucher E, Nicolet J et al (2012) Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc Natl Acad Sci USA 109(15):5880–5885PubMedGoogle Scholar
  41. Morse AM, Peterson DG, Islam-Faridi MN, Smith KE, Magbanua Z et al (2009) Evolution of genome size and complexity inPinus. PLoS ONE 4(2):e4332PubMedPubMedCentralGoogle Scholar
  42. Murray BG, Leitch IJ, Bennett MD (2004) Gymnosperm DNA C-values Database. www.kew.org/cvalues
  43. Neale DB, Wegrzyn JL, Stevens KA, Zimin AV, Puiu D et al (2014) Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biol 15(3):R59PubMedPubMedCentralGoogle Scholar
  44. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC et al (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497(7451):579PubMedGoogle Scholar
  45. Ohno S (1972) So much “junk” DNA in our genome. Brookhaven Symp Biol 23:366–370PubMedGoogle Scholar
  46. Orgel LE, Crick FH (1980) Selfish DNA: the ultimate parasite. Nature 284(5757):604–607PubMedGoogle Scholar
  47. Pellicer J, Fay MF, Leitch IJ (2010) The largest eukaryotic genome of them all? Bot J Linnean Soc 164(1):10–15Google Scholar
  48. Piegu B, Guyot R, Picault N, Roulin A, Saniyal A et al (2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16(10):1262–1269PubMedPubMedCentralGoogle Scholar
  49. Richard GF, Kerrest A, Dujon B (2008) Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiol Mol Biol Rev 72(4):686–727PubMedPubMedCentralGoogle Scholar
  50. Rosbash M, Ford PJ, Bishop JO (1974) Analysis of the C-value paradox by molecular hybridization. Proc Natl Acad Sci USA 71(9):3746–3750PubMedGoogle Scholar
  51. SanMiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82(suppl_1):37–44Google Scholar
  52. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D et al (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274(5288):765–768PubMedGoogle Scholar
  53. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F-S, Pasternak S et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115PubMedGoogle Scholar
  54. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8(4):272–285PubMedGoogle Scholar
  55. Smit AFA, Hubley R, Green P (2015) RepeatMasker Open-4.0. http://www.repeatmasker.org. Accessed 10 Sept 2016
  56. Stevens KA, Wegrzyn J, Zimin A, Puiu D, Crepeau M et al (2016) Sequence of the sugar pine megagenome. Genetics 204(4):1613–1626PubMedPubMedCentralGoogle Scholar
  57. Thomas CA Jr (1971) The genetic organization of chromosomes. Annu Rev Genet 5:237–256PubMedGoogle Scholar
  58. Vicient CM, Suoniemi A, Anamthawat-Jónsson K, Tanskanen J, Beharav A et al (1999) Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11(9):1769–1784PubMedPubMedCentralGoogle Scholar
  59. Vitte C, Panaud O (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retro-transposons in rice Oryza sativa L. Mol Biol Evol 20(4):528–540PubMedGoogle Scholar
  60. Wallberg A, Glémin S, Webster MT (2015) Extreme recombination frequencies shape genome variation and evolution in the honeybee, Apis mellifera. PLoS Genet 11(4):e1005189PubMedPubMedCentralGoogle Scholar
  61. Wegrzyn JL, Liechty JD, Stevens KA, Wu LS, Loopstra C et al (2014) Unique features of the loblolly pine (Pinus taeda L.) megagenome revealed through sequence annotation. Genetics 196(3):891–909Google Scholar
  62. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982PubMedGoogle Scholar
  63. Yao JL, Dong YH, Morris BA (2001) Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc Nati Acad Sci USA 98(3):1306–1311Google Scholar
  64. Yelina NE, Lambing C, Hardcastle TJ, Zhao X, Santos B et al (2015) DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis. Gene Dev 29(20):2183–2202PubMedGoogle Scholar
  65. Zuccolo A, Scofield DG, De Paoli E, Morgante M (2015) The Ty1-copia LTR retroelement family PARTC is highly conserved in conifers over 200MY of evolution. Gene 568(1):89–99PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Giovanni Marturano
    • 1
  • Camilla Canovi
    • 2
  • Federico Rossi
    • 3
  • Andrea Zuccolo
    • 1
    Email author
  1. 1.Institute of Life Sciences, Scuola Superiore Sant’AnnaPisaItaly
  2. 2.Dipartimento di Scienze Agrarie, Alimentari e Agro-Ambientali, Università di PisaPisaItaly
  3. 3.Medical and Molecular Genetics DepartmentKing’s CollegeLondonUK

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