Contrasting evolutionary trajectories of multiple retrotransposons following independent allopolyploidy in wild wheats

New Phytologist

Volumn 202, Issue 3, 2014, Pages 975-985

  Senerchia, Natacha ^a   Felber, François ^a,b   Parisod, Christian ^a  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^b Musée et Jardins Botaniques Cantonaux   (Switzerland)

Author keywords

Aegilops; Genome evolution; Genome shock; Pivotal differential genome evolution; Sequence specific amplified polymorphism (SSAP); Transposable elements (TEs)

Indexed keywords

GENOME; POLYMORPHISM; POLYPLOIDY; WHEAT; WILD POPULATION;

AEGILOPS; TRITICUM AESTIVUM;

RETROPOSON;

DIPLOIDY; GENE LOCUS; GENETIC VARIABILITY; GENETICS; LONG TERMINAL REPEAT; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PLANT GENOME; POLYPLOIDY; RETROPOSON; SPECIES DIFFERENCE; WHEAT;

BASE SEQUENCE; DIPLOIDY; EVOLUTION, MOLECULAR; GENETIC LOCI; GENETIC VARIATION; GENOME, PLANT; POLYPLOIDY; RETROELEMENTS; SPECIES SPECIFICITY; TERMINAL REPEAT SEQUENCES; TRITICUM;

EID: 84898024392     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12731     Document Type: Article

References (77)

1. Badaeva ED, Amosova AV, Muravenko OV, Samatadze TE, Chikida NN, Zelenin AV, Friebe B, Gill BS. 2002. Genome differentiation in Aegilops. 3. Evolution of the D-genome cluster. Plant Systematics and Evolution 231: 163-190.
2. Badaeva ED, Amosova AV, Samatdze TE, Zoshchuk SA, Shostak NG, Chikida NN, Zelenin AV, Raupp WJ, Friebe B, Gill BS. 2004. Genome differentiation in Aegilops. 4. Evolution of the U-genome cluster. Plant Systematics and Evolution 246: 45-76.
3. Badaeva ED, Dedkova OS, Gay G, Pukhalskyi VA, Zelenin AV, Bernard S, Bernard M. 2007. Chromosomal rearrangements in wheat: their types and distribution. Genome 50: 907-926.
4. Baum BR, Edwards T, Mamuti M, Johnson DA. 2012. Phylogenetic relationships among the polyploid and diploid Aegilops species inferred from the nuclear 5S rDNA sequences (Poaceae: Triticeae). Genome 55: 177-193.
5. Bennetzen JL, Kellogg EA. 1997. Do plants have a one-way ticket to genomic obesity? Plant Cell 9: 1509-1514.
6. Bento M, Gustafson JP, Viegas W, Silva M. 2011. Size matters in Triticeae polyploids: larger genomes have higher remodeling. Genome 54: 175-183.
7. Bonchev G, Parisod C. 2013. Transposable elements and microevolutionary changes in natural populations. Molecular Ecology Resources 13: 765-775.
8. Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P. 2004. How to track and assess genotyping errors in population genetics studies. Molecular Ecology 13: 3261-3273.
9. Bourc'his D, Voinnet O. 2010. A small-RNA perspective on gametogenesis, fertilization, and early zygotic development. Science 330: 617-622.
10. Brenchley R, Spannagl M, Pfeifer M, Barker GLA, D'Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D et al. 2012. Analysis of the breadwheat genome using whole-genome shotgun sequencing. Nature 491: 705-710.
11. Cervera MT, Ruiz-Garcia L, Martinez-Zapater JM. 2003. Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers. Molecular Genetics and Genomics 268: 832-833.
12. Comai L. 2000. Genetic and epigenetic interactions in allopolyploid plants. Plant Molecular Biology 43: 387-399.
13. Comai L, Madlung A, Josefsson C, Tyagi A. 2003. Do the different parental 'heteromes' cause genomic shock in newly formed allopolyploids? Philosophical Transactions of the Royal Society B 358: 1149-1155.
14. Devos KM, Brown JKM, Bennetzen JL. 2002. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Research 12: 1075-1079.
15. Doyle J, Flagel L, Paterson A, Rapp R, Soltis D. 2008. Evolutionary genetics of genome merger and doubling in plants. Annual Review of Genetics 42: 443-461.
16. Doyle JJ, Egan AN. 2010. Dating the origins of polyploidy events. New Phytologist 186: 73-85.
17. Eilam T, Anikster Y, Millet E, Manisterski J, Feldman M. 2008. Nuclear DNA amount and genome downsizing in natural and synthetic allopolyploids of the genera Aegilops and Triticum. Genome 51: 616-627.
18. Eilam T, Anikster Y, Millet E, Manisterski J, Sag-Assif O, Feldman M. 2007. Genome size and genome evolution in diploid Triticeae species. Genome 50: 1029-1037.
19. El Baidouri M, Panaud O. 2013. Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biology and Evolution 5: 954-965.
20. Esnault C, Palavesam A, Pilitt K, O'Brochta DA. 2011. Intrinsic characteristics of neighboring DNA modulate transposable element activity in Drosophila melanogaster. Genetics 187: 319-331.
21. Fedoroff NV. 2012. Transposable elements, epigenetics, and genome evolution. Science 338: 758-767.
22. Feldman M. 1965a. Further evidence for natural hybridization between tetraploid species of Aegilops Section Pleionathera. Evolution 19: 162-174.
23. Feldman M. 1965b. Fertility of interspecific F1 hybrids and hybrid derivatives involving tetraploid species of Aegilops Section Pleionathera. Evolution 19: 556-562.
24. Feldman M. 1965c. Chromosome pairing between differential genomes in hybrids of tetraploid Aegilops species. Evolution 19: 563-568.
25. Feldman M, Levy AA. 2012. Genome evolution due to allopolyploidization in wheat. Genetics 192: 763-774.
26. Feldman M, Levy AA, Fahima T, Korol A. 2012. Genomic asymmetry in allopolyploid plants: wheat as a model. Journal of Experimental Botany 63: 5045-5059.
27. Ha M, Lu J, Tian L, Ramachandran V, Kasschau K. 2009. Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proceedings of the National Academy of Sciences, USA 106: 17835-17840.
28. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-113.
29. Jurka J, Bao W, Kojima K. 2011. Families of transposable elements, population structure and the origin of species. Biology Direct 6: 44.
30. Kashkush K, Feldman M, Levy AA. 2003. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nature Genetics 33: 102-106.
31. Kejnovsky E, Leitch IJ, Leitch AR. 2009. Contrasting evolutionary dynamics between angiosperm and mammalian genomes. Trends in Ecology and Evolution 24: 572-582.
32. Kilian B, Mammen K, Millet E, Sharma R, Graner A, Salamini F, Hammer K, Özkan H. 2011. Aegilops. In: Kole C, ed. Wild crop relatives: genomic and breeding resources, cereals. Berlin, Heidelberg, Germany: Springer-Verlag, 1-17.
33. Kimber G, Sallee PJ, Feiner MM. 1988. The interspecific and evolutionary relationships in Triticum ovatum. Genome 30: 218-221.
34. Kraitshtein Z, Yaakov B, Khasdan V, Kashkush K. 2010. Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186: 801-812.
35. Kumar A, Bennetzen JL. 1999. Plant retrotransposons. Annual Review of Genetics 33: 479-532.
36. Le Rouzic A, Dupas S, Capy P. 2007. Genome ecosystem and transposable elements species. Gene 390: 214-220.
37. Leitch IJ, Bennett MD. 2004. Genome downsizing in polyploid plants. Biological Journal of the Linnean Society 82: 651-663.
38. Leitch IJ, Hanson L, Lim KY, Kovarik A, Chase MW, Clarkson JJ, Leitch AR. 2008. The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Annals of Botany 101: 805-814.
39. Levy AA. 2013. Transposons in plant speciation. In: Fedoroff NV, ed. Plant transposons and genome dynamics in evolution. Ames, IA, USA: John Wiley and Sons Ltd., 165-176.
40. Li WL, Zhang P, Fellers JP, Friebe B, Gill BS. 2004. Sequence composition, organization, and evolution of the core Triticeae genome. Plant Journal 40: 500-511.
41. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
42. Liu B, Wendel JF. 2003. Epigenetic phenomena and the evolution of plant allopolyploids. Molecular Phylogenetics and Evolution 29: 365-379.
43. Lynch M, Conery JS. 2003. The origins of genome complexity. Science 302: 1401-1404.
44. Ma JX, Bennetzen JL. 2004. Rapid recent growth and divergence of rice nuclear genomes. Proceedings of the National Academy of Sciences, USA 101: 12404-12410.
45. Ma JX, Devos KM, Bennetzen JL. 2004. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Research 14: 860-869.
46. Ma XF, Gustafson JP. 2005. Genome evolution of allopolyploids: a process of cytological and genetic diploidization. Cytogenetics and Genome Research 109: 236-249.
47. McClintock B. 1984. The significance of responses of the genome to challenge. Science 226: 792-801.
48. Meimberg H, Rice K, Milan N, Njoku C, McKay J. 2009. Multiple origins promote the ecological amplitude of allopolyploid Aegilops (Poaceae). American Journal of Botany 96: 1262-1273.
49. Murat F, Van de Peer Y, Salse J. 2012. Decoding plant and animal genome plasticity from differential paleo-evolutionary patterns and processes. Genome Biology and Evolution 4: 917-928.
50. 2 from generalized linear mixed-effects models. Method in Ecology and Evolution 4: 133-142.
51. Ozkan H, Tuna M, Arumuganathan K. 2003. Nonadditive changes in genome size during allopolyploidization in the wheat (Aegilops-Triticum) group. Journal of Heredity 94: 260-264.
52. Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C, Ainouche M, Chalhoub B, Grandbastien MA. 2009. Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. New Phytologist 184: 1003-1015.
53. Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C, Ainouche M, Chalhoub B, Grandbastien M-A. 2010. Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytologist 186: 37-45.
54. Parisod C, Christin P-A. 2008. Genome-wide association to fine-scale ecological heterogeneity within a continuous population of Biscutella laevigata (Brassicaceae). New Phytologist 178: 436-447.
55. Parisod C, Mhiri C, Lim KY, Clarkson JJ, Chase MW, Leitch AR, Grandbastien M-A. 2012. Differential dynamics of transposable elements during long-term diploidization of Nicotiana section Repandae (Solanaceae) allopolyploid genomes. PLoS ONE 7: e50352.
56. Parisod C, Senerchia N. 2012. Responses of transposable elements to polyploidy. In: Grandbastien M-A, Casacuberta JM, eds. Plant transposable elements. Berlin, Heidelberg, Germany: Springer-Verlag, 147-148.
57. Petit M, Guidat C, Daniel J, Denis E, Montoriol E, Bui QT, Lim KY, Kovarik A, Leitch AR, Grandbastien MA et al. 2010. Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytologist 186: 135-147.
58. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology 132: 365-386.
59. Sabot F, Schulman AH. 2009. Genomics of transposable elements in the Triticeae. In: Muehlbauer GJ, Feuille C, eds. Genetics and genomics of the Triticeae. New York, NY, USA: Springer-Verlag, 387-405.
60. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL. 1998. The paleontology of intergene retrotransposons of maize. Nature Genetics 20: 43-45.
61. Sarilar V, Palacios PM, Rousselet A, Ridel C, Falque M, Eber F, Chevre A-M, Joets J, Brabant P, Alix K. 2013. Allopolyploidy has a moderate impact on restructuring at three contrasting transposable element insertion sites in resynthesized Brassica napus allotetraploids. New Phytologist 198: 593-604.
62. Senerchia N, Wicker T, Felber F, Parisod C. 2013. Evolutionary dynamics of retrotransposons assessed by next generation sequencing in wild relatives of wheat. Genome Biology and Evolution 5: 1010-1020.
63. van Slageren MW. 1994. Wild wheats: a monograph of Aegilops L. and Amblyopyrum (Jaub & Spach) Eig (Poaceae). Wageningen Agricultural University Papers 97.
64. Soltis DE, Soltis PS. 1999. Polyploidy: recurrent formation and genome evolution. Trends in Ecology & Evolution 14: 348-352.
65. Tayalé A, Parisod C. 2013. Natural pathways to polyploidy in plants and consequences for genome reorganization. Cytogenetic and Genome Research 140: 79-96.
66. Tenaillon M, Hollister J, Gaut B. 2010. A triptych of the evolution of plant transposable elements. Trends in Plant Science 15: 471-478.
67. Vekemans X 2002. AFLP-SURV version 1.0. Distributed by the author. Belgium: Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles.
68. Vicient CM, Suoniemi A, Anamthawat-Jonsson K, Tanskanen J, Beharav A, Nevo E, Schulman AH. 1999. Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11: 1769-1784.
69. Vitte C, Panaud O. 2005. LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenetics and Genome Research 110: 91-107.
70. Wang JB, Wang C, Shi SH, Zhong Y. 2000. Evolution of parental ITS regions of nuclear rDNA in allopolyploid Aegilops (Poaceae) species. Hereditas 133: 1-7.
71. Wang Q, Dooner HK. 2006. Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proceedings of the National Academy of Sciences, USA 103: 17644-17649.
72. Wicker T. 2013. So many repeats and so little time: how to classify transposable elements. In: Grandbastien M-A, Casacuberta JM, eds. Plant transposable elements. Berlin, Heidelberg, Germany: Springer-Verlag, 1-15.
73. Wicker T, Buell CR. 2009. Gene and repetitive sequence annotation in the Triticeae. In: Muehlbauer GJ, Feuillet C, eds. Genetics and genomics of the Triticeae. New York, NY, USA: Springer-Verlag, 407-425.
74. Wicker T, Sabot F, Van Hua A, Bennetzen J, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O et al. 2007. A unified classification system for eukaryotic transposable elements. Nature Reviews Genetics 8: 973-982.
75. Yaakov B, Kashkush K. 2011. Massive alterations of the methylation patterns around DNA transposons in the first four generations of a newly formed wheat allohexaploid. Genome 54: 42-49.
76. Yaakov B, Meyer K, Ben-David S, Kashkush K. 2013. Copy number variation of transposable elements in Triticum-Aegilops genus suggests evolutionary and revolutionary dynamics following allopolyploidization. Plant Cell Reports 32: 1615-1624.
77. Zohary D, Feldman M. 1962. Hybridization between amphidiploids and evolution of polyploids in wheat (Aegilops-Triticum) group. Evolution 16: 44-61.