Transcriptionally active LTR retrotransposons in Eucalyptus genus are differentially expressed and insertionally polymorphic

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Marcon, Helena Sanches ^a   Domingues, Douglas Silva ^a   Silva, Juliana Costa ^b   Borges, Rafael Junqueira ^a   Matioli, Fábio Filippi ^a   de Mattos Fontes, Marcos Roberto ^a   Marino, Celso Luis ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b INSTITUTO AGRONÔMICO DO PARANÁ   (Brazil)

Author keywords

Comparative analysis; Dynamics; Eucalyptus genomes; Genomic distribution; LTR retrotransposons

Indexed keywords

EUCALYPTUS; EUCALYPTUS GRANDIS;

PLANT PROTEIN; RETROPOSON; TRANSCRIPTOME;

CHEMISTRY; DNA SEQUENCE; EUCALYPTUS; GENE EXPRESSION REGULATION; GENETICS; LONG TERMINAL REPEAT; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLANT GENOME; PROTEIN SECONDARY STRUCTURE; RETROPOSON;

EUCALYPTUS; GENOME, PLANT; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PHYLOGENY; PLANT PROTEINS; PROTEIN STRUCTURE, SECONDARY; RETROELEMENTS; SEQUENCE ANALYSIS, DNA; TERMINAL REPEAT SEQUENCES; TRANSCRIPTOME;

EID: 84939214411     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-015-0550-1     Document Type: Article

References (92)

1. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8:973-82.
2. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: complexity, diversity, and dynamics. Science. 2009;326:1112-5.
3. Hawkins JS, Kim HR, Nason JD, Wing RA, Wendel JF. Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res. 2006;16:1252-61.
4. Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, et al. Doubling genome size without polyploidization: Dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res. 2006;16:1262-9.
5. Vicient CM. Transcriptional activity of transposable elements in maize. BMC Genomics. 2010;11:601.
6. Domingues DS, Cruz GMK, Metcalfe CJ, Nogueira FTS, Vicentini R, Alves CS, et al. Analysis of plant LTR-retrotransposons at the fine scale family level reveals individual molecular patterns. BMC Genomics. 2012;13:137.
7. Lopes FR, Jjingo D, Da Silva CRM, Andrade AC, Marraccini P, Teixeira JB, et al. Transcriptional activity, chromosomal distribution and expression effects of transposable elements in Coffea genomes. PLoS One. 2013;8:175-91.
8. Lisch D. Epigenetic regulation of transposable elements in plants. Annu Rev Plant Physiol Plant Mol Biol. 2009;60:43-66.
9. Rocheta M, Carvalho L, Viegas W, Morais-Cecílio L. Corky, a Gypsy-like retrotransposon is differentially transcribed in Quercus suber tissues. BMC Res. 2012;5:432.
10. Myburg AA, Potts BM, Marques CM, Kirst M, Gion JM, Grattapaglia D, et al. Eucalyptus. In: Chittaranjan K, editor. Genome mapping and molecular breeding in plants. New York, NY, USA: Springer; 2007. p. 115-60.
11. Harwood C. New introductions - doing it right. In: Walker J, editor. Developing a eucalypt resource: learning from Australia and elsewhere: University of Canterbury. Christchurch, New Zealand: Wood Technology Research Centre; 2011. p. 43-54.
12. Assis, TF. Melhoramenro genético de Eucalyptus: desafios e perspectivas. 3rd Brazilian Forestry Meeting, 2014.
13. Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, et al. The genome of Eucalyptus grandis. Nature. 2014;5410:356-62.
14. Bacci Júnior M, Soares RBS, Tajara E, Ambar G, Fischer CN, Guilherme IR, et al. Identification and frequency of transposable elements in Eucalyptus. Gen Mol Biol. 2005;28:634-9.
15. Piednoël M, Carrete-Veja G, Renners S. Characterization of the LTR retrotransposon repertoire of a plant clade of six diploid and one tetraploid species. Plant J. 2013;75:699-709.
16. Yaakov B, Ben-David S, Kashkush K. Genome-wide analysis of stowaway-like MITEs in wheat reveals high sequence conservation, gene association, and genomic diversification. Plant Physiol. 2013;161:486-96.
17. Wicker T, Keller B. Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res. 2007;17:1072-81.
18. Lloréns C, Muñoz-Pomer A, Bernad L, Botella H, Moya A. Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees. Biol Direct. 2009;4:41.
19. Rossi M, Araujo PG, Van Sluys MA. Survey of transposable elements in sugarcane expressed sequence tags (ESTs). Gen Mol Biol. 2001;24:147-54.
20. Kohany O, Gentles AJ, Hankus L, Jurka J. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics. 2006;7:474.
21. Xu Z, Wang H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007;35:265-8.
22. Mccarthy EM, Mcdonald JF. LTR_STRUC: a novel search and identification program for LTR retrotransposons. Bioinformatics. 2003;19:362-7.
23. Solovyev VV. Statistical approaches in eukaryotic gene prediction. In: Balding D, Cannings C, Bishop M, editors. Handbook of statistical genetics. London.: Wiley-Interscience; 2007.
24. Du J, Tian Z, Hans CS, Laten HM, Cannon SB, Jackson SA, et al. Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J. 2010;63:584-98.
25. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-7.
26. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol. 2013;30:2725-9.
27. Söding J. Protein homology detection by HMM-HMM comparison. Bioinformatics (Oxford, England). 2005;21:951-60.
28. Wu S, Zhang Y. MUSTER: Improving protein sequence profile-profile alignments by using multiple sources of structure information. Proteins. 2008;72:547-56.
29. Fiser A, Sali A. Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol. 2003;374:461-91.
30. Lovell SC, Davis IW, Arendall WB, de Bakker PIW, Word JM, Prisant MG, et al. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins. 2003;50:437-50.
31. Wiederstein M, Sippl MJ. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007;35:407-10.
32. Hess B, Kutzner C, van der Spoel D, Lindahl E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J Chem Theor Comput. 2008;4:435-47.
33. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem. 1998;102:3586-616.
34. Berendsen HJC, Postma JPM, Gunsteren WF, Hermans J. Interaction Models for Water in Relation to Protein Hydration. In: Pullman B. Editor. The Jerusalem Symposia on Quantum Chemistry and Biochemistry. Intermolecular Forces. Springer Netherlands. 1981; p. 331-342.
35. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605-12.
36. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A. 2001;98:10037-41.
37. Olsson MHM, Søndergaard CR, Rostkowski M, Jensen JH. PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical pKa Predictions. J Chem Theor Comput. 2011;7:525-37.
38. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, et al. Circos: An information aesthetic for comparative genomics. Genome Res. 2009;19:1639-45.
39. San Miguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL. The paleontology of intergene retrotransposons of maize. Nat Genet. 1998;20:43-5.
40. Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111-20.
41. Koch MA, Haubold B, Mitchell-Olds T. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol. 2000;17:1483-98.
42. Moisy C, Schulman AH, Kalendar R, Buchmann JP, Pelsy F. The Tvv1 retrotransposon family is conserved between plant genomes separated by over 100 million years. Theor Appl Genet. 2014;127:1223-35.
43. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451-2.
44. Nascimento LC, Lepikson JN, Salazar MM, Camargo ELO, Marques WL, Gonçalves DC, et al. An integrated database of Eucalyptus spp. genome Project. BMC Proceedings. 2011;5:170.
45. Salazar MM, Nascimento LC, Camargo ELO, Gonçalves DC, Lepikson Neto J, Marques WL, et al. Xylem transcription profiles indicate potential metabolic responses for economically relevant characteristics of Eucalyptus species. BMC Genomics. 2013;14:201.
46. Ferreira ME, Grattapaglia D. Introdução ao uso de marcadores moleculares em análises genéticas. 3rd ed. Embrapa-Cenargen: Brasília; 1998.
47. Korimbocus J, Danks C, Boonham N, Barker I, Coates D. Improved detection of sugarcane leaf virus using a real-time fluorescent reverse-transcription polymerase chain reaction assay. Phytopathology. 2002;90:448-53.
48. Smýkal P. Development of an efficient retrotransposon-based fingerprinting method for rapid pea variety identification. J Appl Genet. 2006;47:221-30.
49. Kalendar R, Grob T, Regina M, Suoniemi A, Schulman AH. IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. Theor Appl Gen. 1999;98:704-11.
50. Rohlf FJ. NTSYS-pc: numerical taxonomy and multivariate analysis system. Setauket, NY: Exeter Software; 2000.
51. Fan F, Cui B, Zhang T, Ding G, Wen X. LTR-retrotransposon activation, IRAP marker development and its potential in genetic diversity assessment of masson pine (Pinus massoniana). Tree Gen Genom. 2013;10:213-22.
52. Kraitshtein Z, Yaakov B, Khasdan V, Kashkush K. Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics. 2010;186:801-12.
53. Baruch O, Kashkush K. Analysis of copy-number variation, insertional polymorphism, and methylation status of the tiniest class I (TRIM) and class II (MITE) transposable element families in various rice strains. Plant Cell Rep. 2012;31:885-93.
54. Navarathna DHMLP, Das A, Morschhäuser J, Nickerson KW, Roberts DD. Dur3 is the major urea transporter in Candida albicans and is co-regulated with the urea amidolyase Dur1,2. Microbiology. 2011;157:270-9.
55. de Michele R, Loque D, Lalonde S, Frommer WB. Ammonium and urea transporter inventory of the Selaginella and Physcomitrella genomes. Frontiers in Plant Science. 2012;3:62.
56. Rodrigues MR, Bravo JP, Sassaki FT, Severino FE, Maia IG. The tonoplast intrinsic aquaporin (TIP) subfamily of Eucalyptus grandis: Characterization of EgTIP2, a root-specific and osmotic stress-responsive gene. Plant Sci. 2013;213:106-13.
57. Cassan-Wang H, Soler M, Yu H, Camargo ELO, Carocha V, Ladouce N, et al. Reference Genes for High-Throughput Quantitative RT-PCR Analysis of Gene Expression in Organs and Tissues of Eucalyptus Grown in Various Environmental Conditions. Plant and Cell Physiol. 2012;53:2101-16.
58. Vandesompele J, Preter K, Pattyn F, Poppe B, Roy NV, Paepe AD, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:34.1-34.11.
59. Sinha DK, Smith CM. Selection of Reference Genes for Expression Analysis in Diuraphis noxia (Hemiptera: Aphididae) Fed on Resistant and Susceptible Wheat Plants. Sci Rep. 2014;4:5059.
60. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, Van Den Hoff MJB, et al. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 2009;37:1-12.
61. Livak KJ, Schmittgen TD. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-ΔΔCT Method. Methods. 2001;25:402-8.
62. Silva FAS, Azevedo CAV. Principal components analysis in the software assistat-statistical attendance. In: World Congress on Computers in Agriculture, 7. American Society of Agricultural and Biological Engineers, Reno-NV-USA. 2009.
63. Tanskanen JA, Sabot F, Vicient C, Schulman AH. Life without GAG: The BARE-2 retrotransposon as a parasite's parasite. Gene. 2007;390:166-74.
64. Ishida M, Shimojo H, Hayashi A, Kawaguchi R, Ohtani Y, Uegaki K, et al. Intrinsic nucleic acid-binding activity of Chp1 chromodomain is required for heterochromatic gene silencing. Mol Cell. 2012;47:228-41.
65. Hare S, Vos AM, Clayton RF, Thuring JW, Cummings MD, Cherepanov P. Molecular mechanisms of retroviral integrase inhibition and the evolution of viral resistance. Proc Natl Acad Sci U S A. 2010;107:20057-62.
66. Li J, Li Z, Ruan J, Xu C, Tong Y, Pan PW, et al. Structural basis for specific binding of human MPP8 chromodomain to histone H3 methylated at lysine 9. PLoS One. 2011;6, e25104.
67. Nowak E, Potrzebowski W, Konarev PV, Rausch JW, Bona MK, Svergun DI, et al. Structural analysis of monomeric retroviral reverse transcriptase in complex with an RNA/DNA hybrid. Nucleic Acids Res. 2013;41:3874-87.
68. Nowak E, Miller JT, Bona MK, Studnicka J, Szczepanowski RH, Jurkowski J, et al. Ty3 reverse transcriptase complexed with an RNA-DNA hybrid shows structural and functional asymmetry. Nature Structural Mol Biol. 2014;21:389-96.
69. Kullan ARK, van Dyk MM, Hefer CA, Jones N, Kanzler A, Myburg AA. Genetic dissection of growth, wood basic density and gene expression in interspecific backcrosses of Eucalyptus grandis and E. urophylla. BMC Genet. 2012;13:60-72.
70. Echenique V, Stamova B, Wolters P, Lazo G, Carollo V, Dubcovsky J. Frequencies of Ty1-copia and Ty3-gypsy retroelements within the Triticeae EST databases. Theor Appl Genet. 2002;104:840-4.
71. Weber B, Heitkam T, Holtgräwe D, Weisshaar B, Minoche AE, Dohm JC, et al. Highly diverse chromoviruses of Beta vulgaris are classified by chromodomains and chromosomal integration. Mobile DNA. 2013;4:8.
72. Novikova O. Chromodomains and LTR retrotransposons in plants. Commun Integ Biol. 2009;2:158-62.
73. Gao D, Jimenez-Lopez JC, Iwata A, Gill N, Jackson SA. Functional and Structural Divergence of an Unusual LTR Retrotransposon Family in Plants. PLoS One. 2012;7:e48595.
74. Abrusán G, Zhang Y, Szilágyi A. Structure prediction and analysis of DNA transposon and LINE retrotransposon proteins. J Biol Chem. 2013;288:16127-38.
75. Ma J, Bennetzen JL. Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice. Proc Natl Acad Sci. 2006;103:383-8.
76. Moisy C, Garrison KE, Meredith CP, Pelsy F. Characterization of ten novel Ty1/Copia-like retrotransposon families of the grapevine genome. BMC Genomics. 2008;9:469.
77. Xu Y, Du J. Young but not relatively old retrotransposons are preferentially located in gene-rich euchromatic regions in tomato (Solanum lycopersicum) plants. Plant J. 2014;80(4):582-591.
78. Bennetzen JL, Ma J, Devos KM. Mechanisms of recent genome size variation in flowering plants. Ann Bot. 2005;95(1):127-132.
79. Cossu RM, Buti M, Giordani T, Natali L, Cavallini A. A computational study of the dynamics of LTR retrotransposons in the Populus trichocarpa genome. Tree Gen Genomes. 2011;8:61-75.
80. Vitte C, Estep MC, Leebens-Mack J, Bennetzen JL. Young, intact and nested retrotransposons are abundant in the onion and asparagus genomes. Ann Bot. 2013. doi: 10.1093/aob/mct155.
81. Gao D, Chen J, Chen M, Meyers BC, Jackson S. A Highly Conserved, Small LTR Retrotransposon that Preferentially Targets Genes in Grass Genomes. PLoS One. 2012;7:e32010.
82. Tsukahara S, Kawabe A, Kobayashi A, Ito T, Aizu T, Shin T, et al. Centromere-targeted de novo integrations of an LTR retrotransposon of Arabidopsis lyrata. Genes Dev. 2012;26:705-13.
83. Weber B, Wenke T, Frömmel U, Schmidt T, Heitkam T. The Ty1-copia families SALIRE and Cotzilla populating the Beta vulgaris genome show remarkable differences in abundance, chromosomal distribution, and age. Chromosome Res. 2010;18:247-63.
84. Kawakami T, Strakosh SC, Zhen Y, Ungerer MC. Different scales of Ty1/Copia-like retrotransposon proliferation in the genomes of three diploid hybrid sunflower species. Heredity. 2010;104:341-50.
85. Zhao M, Ma J. Co-evolution of plant LTR-retrotransposons and their host genomes. Protein Cell. 2013;4:493-501.
86. Mandoulakani BA, Piri Y, Darvishzadeh R, Bernoosi I, Jafari M. Retroelement Insertional Polymorphism and Genetic Diversity in Medicago sativa Populations Revealed by IRAP and REMAP Markers. Plant Mol Biol Reporter. 2012;30:286-96.
87. Steane DA, Nicolle D, Sansaloni CP, Petroli CD, Carling J, Kilian A, et al. Population genetic analysis and phylogeny reconstruction in Eucalyptus (Myrtaceae) using high-throughput, genome-wide genotyping. Mol Phylogenet Evol. 2011;59:206-24.
88. Poke FS, Martin DP, Steane DA, Vaillancourt RE, Reid JB. The impact of intragenic recombination on phylogenetic reconstruction at the sectional level in Eucalyptus when using a single copy nuclear gene (cinnamoyl CoA reductase). Mol Phylogenet Evol. 2006;39:160-70.
89. Ungerer MC, Kawakami T. Transcriptional Dynamics of LTR Retrotransposons in Early Generation and Ancient Sunflower Hybrids. Genome Biol Evol. 2013;5(2):329-37.
90. Petit M, Guidat C, Daniel J, Denis E, Montoriol E, Bui QT, et al. Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytologist. 2010;186:135-47.
91. Rico-Cabanas L, Martínez-Izquierdo JA. CIRE1, a novel ranscriptionally active Ty1-copia retrotransposon from Citrus sinensis. Mol Genet Genomics. 2007;227:365-77.
92. Grandbastien MA, Audeon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa APP, et al. Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogen Genome Res. 2005;110:1-4.