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Korea Genome Organization (한국유전체학회)
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Transposable Elements and Genome Size Variations in Plants

  • Lee, Sung-Il (Department of Molecular Bioscience, Kangwon National University) ;
  • Kim, Nam-Soo (Department of Molecular Bioscience, Kangwon National University)
  • Received : 2014.07.18
  • Accepted : 2014.08.22
  • Published : 2014.09.30
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Abstract

Although the number of protein-coding genes is not highly variable between plant taxa, the DNA content in their genomes is highly variable, by as much as 2,056-fold from a 1C amount of 0.0648 pg to 132.5 pg. The mean 1C-value in plants is 2.4 pg, and genome size expansion/contraction is lineage-specific in plant taxonomy. Transposable element fractions in plant genomes are also variable, as low as ~3% in small genomes and as high as ~85% in large genomes, indicating that genome size is a linear function of transposable element content. Of the 2 classes of transposable elements, the dynamics of class 1 long terminal repeat (LTR) retrotransposons is a major contributor to the 1C value differences among plants. The activity of LTR retrotransposons is under the control of epigenetic suppressing mechanisms. Also, genome-purging mechanisms have been adopted to counter-balance the genome size amplification. With a wealth of information on whole-genome sequences in plant genomes, it was revealed that several genome-purging mechanisms have been employed, depending on plant taxa. Two genera, Lilium and Fritillaria, are known to have large genomes in angiosperms. There were twice times of concerted genome size evolutions in the family Liliaceae during the divergence of the current genera in Liliaceae. In addition to the LTR retrotransposons, non-LTR retrotransposons and satellite DNAs contributed to the huge genomes in the two genera by possible failure of genome counter-balancing mechanisms.

Keywords

References

  1. Bennett MD, Leitch IJ. Plant DNA C-value Database (release 6.0. December 2012). Surrey: Kew. Accessed 2014 Jul 18. Available from: http://data.kew.org/cvalues/.
  2. Bennett MD, Leitch IJ. Nuclear DNA amounts in angiosperms: targets, trends and tomorrow. Ann Bot 2011;107:467-590. https://doi.org/10.1093/aob/mcq258
  3. Michael TP, Jackson S. The first 50 plant genomes. Plant Genome 2013;6. http://dx.doi.org/10.3835/plantgenome2013.03.0001in.
  4. Doolittle WF, Sapienza C. Selfish genes, the phenotype paradigm and genome evolution. Nature 1980;284:601-603. https://doi.org/10.1038/284601a0
  5. Orgel LE, Crick FH. Selfish DNA: the ultimate parasite. Nature 1980;284:604-607. https://doi.org/10.1038/284604a0
  6. Volff JN. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 2006;28:913-922. https://doi.org/10.1002/bies.20452
  7. Feschotte C, Pritham EJ. DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 2007;41:331-368. https://doi.org/10.1146/annurev.genet.40.110405.090448
  8. Oliver KR, McComb JA, Greene WK. Transposable elements: powerful contributors to angiosperm evolution and diversity. Genome Biol Evol 2013;5:1886-1901. https://doi.org/10.1093/gbe/evt141
  9. Waring M, Britten RJ. Nucleotide sequence repetition: a rapidly reassociating fraction of mouse DNA. Science 1966;154:791-794. https://doi.org/10.1126/science.154.3750.791
  10. Britten RJ, Kohne DE. Repeated sequences in DNA: hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science 1968;161:529-540. https://doi.org/10.1126/science.161.3841.529
  11. Peterson DG, Wessler SR, Paterson AH. Efficient capture of unique sequences from eukaryotic genomes. Trends Genet 2002;18:547-550. https://doi.org/10.1016/S0168-9525(02)02764-6
  12. Yuan Y, SanMiguel PJ, Bennetzen JL. High-Cot sequence analysis of the maize genome. Plant J 2003;34:249-255. https://doi.org/10.1046/j.1365-313X.2003.01716.x
  13. Lamoureux D, Peterson DG, Li W, Fellers JP, Gill BS. The efficacy of Cot-based gene enrichment in wheat (Triticum aestivum L.). Genome 2005;48:1120-1126. https://doi.org/10.1139/g05-080
  14. Heslop-Harrison JS. Comparative genome organization in plants: from sequence and markers to chromatin and chromosomes. Plant Cell 2000;12:617-636. https://doi.org/10.1105/tpc.12.5.617
  15. Heslop-Harrison JS, Schimidt T. Plant nuclear genome composition. eLS 2012 Aug 15 [Epub]. http://dx.doi.org/10.1002/9780470015902.a0002014.pub2.
  16. Lee SI, Park KC, Son JH, Hwang YJ, Lim KB, Song YS, et al. Isolation and characterization of novel Ty1-copia-like retrotransposons from lily. Genome 2013;56:495-503. https://doi.org/10.1139/gen-2013-0088
  17. McKnight TD, Shippen DE. Plant telomere biology. Plant Cell 2004;16:794-803. https://doi.org/10.1105/tpc.160470
  18. Kaochar S, Tu BP. Gatekeepers of chromatin: small metabolites elicit big changes in gene expression. Trends Biochem Sci 2012;37:477-483. https://doi.org/10.1016/j.tibs.2012.07.008
  19. McClintock B. The association of mutants with homozygous deficiencies in Zea mays. Genetics 1941;26:542-571.
  20. McClintock B. The stability of broken ends of chromosomes in Zea mays. Genetics 1941;26:234-282.
  21. McClintock B. The fusion of broken ends of chromosomes following nuclear fusion. Proc Natl Acad Sci U S A 1942;28:458-463. https://doi.org/10.1073/pnas.28.11.458
  22. McClintock B. Mutable loci in maize. Year B Carnegie Inst Wash 1948;47:155-169.
  23. 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;8:973-982. https://doi.org/10.1038/nrg2165
  24. Wessler SR, Bureau TE, White SE. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev 1995;5:814-821. https://doi.org/10.1016/0959-437X(95)80016-X
  25. Kejnovsky E, Hawkins JS, Feschotte C. Plant transposable elements: biology and evolution. In: Plant Genome Diversity. Vol. 1 (Wendel JF, Greilhuber J, Dolezel J, Leitch IJ, eds.). Wien: Springer Verlag, 2012. pp. 17-34.
  26. Fedoroff NV. Presidential address. Transposable elements, epigenetics, and genome evolution. Science 2012;338:758-767. https://doi.org/10.1126/science.338.6108.758
  27. Finnegan DJ. Eukaryotic transposable elements and genome evolution. Trends Genet 1989;5:103-107. https://doi.org/10.1016/0168-9525(89)90039-5
  28. Michael TP. Plant genome size variation: bloating and purging DNA. Brief Funct Genomics 2014;13:308-317. https://doi.org/10.1093/bfgp/elu005
  29. Voytas DF, Boeke JD. Ty1 and Ty5 of Saccharomyces cereviceae. In: Mobile DNA II (Craig NL, Craigie R, Gellert M, Lambowitz AM, eds.). Washington, DC: ASM Press, 2002. pp. 631-662.
  30. Sandmeyer SB, Aye M, Menees T. Ty3, a position-specific, gypsy-like element in Saccharomyces cerevisiae. In: Mobile DNA II (Craig NL, Craigie R, Gellert M, Lambowitz AM, eds.). Washington, DC: ASM Press, 2002. pp. 663-683.
  31. Schulman AH, Wicker T. A field guide to transposable elements. In: Plant Transposons and Genome Dynamics in Evolution (Fedoroff NV, ed.). Oxford: Wiley Blackwell, 2013. pp. 15-40.
  32. Eickbush TH, Malik HS. Origin and evolution of retrotransposons. In: Mobile DNA II (Craig NL, Craigie R, Gellert M, Lambowitz AM, eds.). Washington, DC: ASM Press, 2002. pp. 1111-1146.
  33. Havecker ER, Gao X, Voytas DF. The diversity of LTR retrotransposons. Genome Biol 2004;5:225. https://doi.org/10.1186/gb-2004-5-6-225
  34. Levin HL. Newly identified retrotransposons of Ty3/gypsy class in fungi, plants, and vertebrates. In: Mobile DNA II (Craig NL, Craigie R, Gellert M, Lambowitz AM, eds.). Washington, DC: ASM Press, 2002. pp. 684-701.
  35. Rowold DJ, Herrera RJ. Alu elements and the human genome. Genetica 2000;108:57-72. https://doi.org/10.1023/A:1004099605261
  36. Capy P, Bazin C, Higuet D, Langin T. Dynamic and Evolution of Transposable Elements. Austin: Library of Congress, 1998.
  37. Nassif N, Penney J, Pal S, Engels WR, Gloor GB. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol Cell Biol 1994;14:1613-1625. https://doi.org/10.1128/MCB.14.3.1613
  38. Hickman AB, Perez ZN, Zhou L, Musingarimi P, Ghirlando R, Hinshaw JE, et al. Molecular architecture of a eukaryotic DNA transposase. Nat Struct Mol Biol 2005;12:715-721. https://doi.org/10.1038/nsmb970
  39. Keith JH, Schaeper CA, Fraser TS, Fraser MJ Jr. Mutational analysis of highly conserved aspartate residues essential to the catalytic core of the piggyBac transposase. BMC Mol Biol 2008;9:73. https://doi.org/10.1186/1471-2199-9-73
  40. Du C, Swigonova Z, , Messing J. Retrotranspositions in orthologous regions of closely related grass species. BMC Evol Biol 2006;6:62. https://doi.org/10.1186/1471-2148-6-62
  41. Lai J, Li Y, Messing J, Dooner HK. Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci U S A 2005;102:9068-9073. https://doi.org/10.1073/pnas.0502923102
  42. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 2005;37:997-1002. https://doi.org/10.1038/ng1615
  43. Du C, Fefelova N, Caronna J, He L, Dooner HK. The polychromatic Helitron landscape of the maize genome. Proc Natl Acad Sci U S A 2009;106:19916-19921. https://doi.org/10.1073/pnas.0904742106
  44. Jones RN. McClintock's controlling elements: the full story. Cytogenet Genome Res 2005;109:90-103. https://doi.org/10.1159/000082387
  45. Sabot F, Schulman AH. Parasitism and the retrotransposon life cycle in plants: a hitchhiker's guide to the genome. Heredity (Edinb) 2006;97:381-388. https://doi.org/10.1038/sj.hdy.6800903
  46. Manninen I, Schulman AH. BARE-1, a copia-like retroelement in barley (Hordeum vulgare L.). Plant Mol Biol 1993;22:829-846. https://doi.org/10.1007/BF00027369
  47. Tanskanen JA, Sabot F, Vicient C, Schulman AH. Life without GAG: the BARE-2 retrotransposon as a parasite's parasite. Gene 2007;390:166-174. https://doi.org/10.1016/j.gene.2006.09.009
  48. Bureau TE, Wessler SR. Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 1992;4:1283-1294. https://doi.org/10.1105/tpc.4.10.1283
  49. Bureau TE, Wessler SR. Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses. Proc Natl Acad Sci U S A 1994;91:1411-1415. https://doi.org/10.1073/pnas.91.4.1411
  50. Bureau TE, Wessler SR. Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. Plant Cell 1994;6: 907-916. https://doi.org/10.1105/tpc.6.6.907
  51. Feschotte C, Zhang X, Wessler SR. Miniature-inverted repeat transposable elements and their relationship to established DNA transposons. In: Mobile DNA II (Craig NL, Craigie R, Gellert M, Lambowitz AM, eds.). Washington, DC, ASM Press, 2002. pp. 1147-1158.
  52. Greilhuber J, Dolezel J, Lysak MA, Bennett MD. The origin, evolution and proposed stabilization of the terms 'genome size' and 'C-value' to describe nuclear DNA contents. Ann Bot 2005;95:255-260. https://doi.org/10.1093/aob/mci019
  53. Pellicer J, Fay MF, Leitch IJ. The largest eukaryotic genome of them all? Bot J Linn Soc 2010;164:10-15. https://doi.org/10.1111/j.1095-8339.2010.01072.x
  54. Corradi N, Pombert JF, Farinelli L, Didier ES, Keeling PJ. The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat Commun 2010;1:77.
  55. Hendrix B, Stewart JM. Estimation of the nuclear DNA content of Gossypium species. Ann Bot 2005;95:789-797. https://doi.org/10.1093/aob/mci078
  56. Thomas CA Jr. The genetic organization of chromosomes. Annu Rev Genet 1971;5:237-256. https://doi.org/10.1146/annurev.ge.05.120171.001321
  57. Gregory TR, Nicol JA, Tamm H, Kullman B, Kullman K, Leitch IJ, et al. Eukaryotic genome size databases. Nucleic Acids Res 2007;35:D332-D338. https://doi.org/10.1093/nar/gkl828
  58. Zedek F, Smerda J, Smarda P, Bures P. Correlated evolution of LTR retrotransposons and genome size in the genus Eleocharis. BMC Plant Biol 2010;10:265. https://doi.org/10.1186/1471-2229-10-265
  59. Proost S, Pattyn P, Gerats T, Van de Peer Y. Journey through the past: 150 million years of plant genome evolution. Plant J 2011;66:58-65. https://doi.org/10.1111/j.1365-313X.2011.04521.x
  60. El Baidouri M, Panaud O. Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biol Evol 2013;5:954-965. https://doi.org/10.1093/gbe/evt025
  61. Ibarra-Laclette E, Lyons E, Hernandez-Guzman G, Perez- Torres CA, Carretero-Paulet L, Chang TH, et al. Architecture and evolution of a minute plant genome. Nature 2013;498:94-98. https://doi.org/10.1038/nature12132
  62. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, Scofield DG, et al. The Norway spruce genome sequence and conifer genome evolution. Nature 2013;497:579-584. https://doi.org/10.1038/nature12211
  63. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: complexity, diversity, and dynamics. Science 2009;326:1112-1115. https://doi.org/10.1126/science.1178534
  64. Plasterk RH, van Luenen HG. The Tc1/mariner family of transposable elements. In: Mobile DNA II (Craig NL, Craigie R, Gellert M, Lambowitz AM, eds.). Washington, DC: ASM Press, 2002. pp. 519-532.
  65. Naito K, Cho E, Yang G, Campbell MA, Yano K, Okumoto Y, et al. Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci U S A 2006;103:17620-17625. https://doi.org/10.1073/pnas.0605421103
  66. Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, et al. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 2009;461:1130-1134. https://doi.org/10.1038/nature08479
  67. Civan P, Svec M, Hauptvogel P. On the coevolution of transposable elements and plant genomes. J Bot 2011;2011: 893546.
  68. Bennetzen JL, Kellogg EA. Do plants have a one-way ticket to genomic obesity? Plant Cell 1997;9:1509-1514. https://doi.org/10.1105/tpc.9.9.1509
  69. Knight CA, Molinari NA, Petrov DA. The large genome constraint hypothesis: evolution, ecology and phenotype. Ann Bot 2005;95:177-190. https://doi.org/10.1093/aob/mci011
  70. Wahl LM, DeHaan CS. Fixation probability favors increased fecundity over reduced generation time. Genetics 2004;168:1009-1018. https://doi.org/10.1534/genetics.104.029199
  71. Bennett MD. Variation in genomic form in plants and its ecological implications. New Phytol 1987;106:177-200.
  72. Kim YJ, Lee J, Han K. Transposable elements: no more 'junk DNA'. Genomics Inform 2012;10:226-233. https://doi.org/10.5808/GI.2012.10.4.226
  73. Dooner HK, Weil CF. Transposon and gene creation. In: Plant Transposons and Genome Dynamics in Evolution (Fedoroff NV, ed.). Ames: Wiley-Blackwell Inc., 2013. pp. 143-164.
  74. Levy AA. Transposon in plant speciation. In: Plant Transposons and Genome Dynamics in Evolution (Fedoroff NV, ed.). Ames: Wiley-Blackwell Inc., 2013. pp. 165-180.
  75. Grover CE, Wendel JF. Recent insights into mechanisms of genome size change in plants. J Bot 2010;2010:382732.
  76. Hawkins JS, Proulx SR, Rapp RA, Wendel JF. Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proc Natl Acad Sci U S A 2009;106:17811-17816. https://doi.org/10.1073/pnas.0904339106
  77. Devos KM, Brown JK, Bennetzen JL. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 2002;12:1075-1079. https://doi.org/10.1101/gr.132102
  78. Ma J, Devos KM, Bennetzen JL. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 2004;14:860-869. https://doi.org/10.1101/gr.1466204
  79. Vitte C, Panaud O, Quesneville H. LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 2007;8:218. https://doi.org/10.1186/1471-2164-8-218
  80. Kovach A, Wegrzyn JL, Parra G, Holt C, Bruening GE, Loopstra CA, et al. The Pinus taeda genome is characterized by diverse and highly diverged repetitive sequences. BMC Genomics 2010;11:420. https://doi.org/10.1186/1471-2164-11-420
  81. Chen J, Huang Q, Gao D, Wang J, Lang Y, Liu T, et al. Whole-genome sequencing of Oryza brachyantha reveals mechanisms underlying Oryza genome evolution. Nat Commun 2013;4:1595. https://doi.org/10.1038/ncomms2596
  82. Fawcett JA, Rouze P, Van de Peer Y. Higher intron loss rate in Arabidopsis thaliana than A. lyrata is consistent with stronger selection for a smaller genome. Mol Biol Evol 2012;29:849-859. https://doi.org/10.1093/molbev/msr254
  83. Hollister JD, Gaut BS. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 2009;19:1419-1428. https://doi.org/10.1101/gr.091678.109
  84. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 2011;43:476-481. https://doi.org/10.1038/ng.807
  85. Yang YF, Zhu T, Niu DK. Association of intron loss with high mutation rate in Arabidopsis: implications for genome size evolution. Genome Biol Evol 2013;5:723-733. https://doi.org/10.1093/gbe/evt043
  86. Smyth DR, Kalitsis P, Joseph JL, Sentry JW. Plant retrotransposon from Lilium henryi is related to Ty3 of yeast and the gypsy group of Drosophila. Proc Natl Acad Sci U S A 1989;86:5015-5019. https://doi.org/10.1073/pnas.86.13.5015
  87. Kato M, Miura A, Bender J, Jacobsen SE, Kakutani T. Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 2003;13:421-426. https://doi.org/10.1016/S0960-9822(03)00106-4
  88. Hollister JD, Smith LM, Guo YL, Ott F, Weigel D, Gaut BS. Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc Natl Acad Sci U S A 2011;108:2322-2327. https://doi.org/10.1073/pnas.1018222108
  89. Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 2007;8:272-285.
  90. Matzke MA, Birchler JA. RNAi-mediated pathways in the nucleus. Nat Rev Genet 2005;6:24-35. https://doi.org/10.1038/nrg1500
  91. Piegu B, Guyot R, Picault N, Roulin A, Sanyal 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;16:1262-1269. https://doi.org/10.1101/gr.5290206
  92. Leitch IJ, Beaulieu JM, Cheung K, Hanson L, Lysak MA, Fay MF. Punctuated genome size evolution in Liliaceae. J Evol Biol 2007;20:2296-2308. https://doi.org/10.1111/j.1420-9101.2007.01416.x
  93. Patterson TB, Givnish TJ. Phylogeny, concerted convergence, and phylogenetic niche conservatism in the core Liliales: insights from rbcL and ndhF sequence data. Evolution 2002;56:233-252. https://doi.org/10.1111/j.0014-3820.2002.tb01334.x
  94. Pagel M, Venditti C, Meade A. Large punctuational contribution of speciation to evolutionary divergence at the molecular level. Science 2006;314:119-121. https://doi.org/10.1126/science.1129647
  95. Givnish TJ, Pires JC, Graham SW, McPherson MA, Prince LM, Patterson TB, et al. Phylogenetic relationships of monocots based on the highly informative plastid gene ndhF: evidence for widespread concerted convergence. Aliso 2006;22:28-51. https://doi.org/10.5642/aliso.20062201.04
  96. Oliver MJ, Petrov D, Ackerly D, Falkowski P, Schofield OM. The mode and tempo of genome size evolution in eukaryotes. Genome Res 2007;17:594-601. https://doi.org/10.1101/gr.6096207
  97. Joseph JL, Sentry JW, Smyth DR. Interspecies distribution of abundant DNA sequences in Lilium. J Mol Evol 1990;30:146-154. https://doi.org/10.1007/BF02099941
  98. Smyth DR. Dispersed repeats in plant genomes. Chromosoma 1991;100:355-359. https://doi.org/10.1007/BF00337513
  99. Leeton PR, Smyth DR. An abundant LINE-like element amplified in the genome of Lilium speciosum. Mol Gen Genet 1993;237:97-104.
  100. Ambrozova K, Mandakova T, Bures P, Neumann P, Leitch IJ, Koblizkova A, et al. Diverse retrotransposon families and an AT-rich satellite DNA revealed in giant genomes of Fritillaria lilies. Ann Bot 2011;107:255-268. https://doi.org/10.1093/aob/mcq235

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  22. Hidden variation in polyploid wheat drives local adaptation vol.28, pp.9, 2018, https://doi.org/10.1101/gr.233551.117
  23. Convergent evolution of complex genomic rearrangements in two fungal meiotic drive elements vol.9, pp.1, 2018, https://doi.org/10.1038/s41467-018-06562-x
  24. In silico Phylogenetic Analysis of hAT Transposable Elements in Plants vol.9, pp.6, 2018, https://doi.org/10.3390/genes9060284
  25. Drosophila parasitoid wasps bears a distinct DNA transposon profile vol.9, pp.1, 2018, https://doi.org/10.1186/s13100-018-0127-2
  26. The Challenge of Analyzing the Sugarcane Genome vol.9, pp.1664-462X, 2018, https://doi.org/10.3389/fpls.2018.00616
  27. Retrotransposons in Betula nana, and interspecific relationships in the Betuloideae, based on inter-retrotransposon amplified polymorphism (IRAP) markers vol.40, pp.5, 2018, https://doi.org/10.1007/s13258-018-0655-7
  28. Comparative analysis of repetitive sequences among species from the potato and the tomato clades vol.123, pp.3, 2018, https://doi.org/10.1093/aob/mcy186
  29. The Evolution of Small-RNA-Mediated Silencing of an Invading Transposable Element vol.10, pp.11, 2018, https://doi.org/10.1093/gbe/evy218
  30. Shared cis-regulatory architecture identified across defense response genes is associated with broad-spectrum quantitative resistance in rice vol.9, pp.1, 2019, https://doi.org/10.1038/s41598-018-38195-x