Major repeat components covering one-third of the ginseng (Panax ginseng C.A. Meyer) genome and evidence for allotetraploidy

Plant Journal

Volumn 77, Issue 6, 2014, Pages 906-916

  Choi, Hong Il ^a   Waminal, Nomar E ^a   Park, Hye Mi ^a   Kim, Nam Hoon ^a   Choi, Beom Soon ^a   Park, Minkyu ^a   Choi, Doil ^a   Lim, Yong Pyo ^b   Kwon, Soo Jin ^c   Park, Beom Seok ^c   Kim, Hyun Hee ^d   Yang, Tae Jin ^a  

^a Seoul National University   (South Korea)

^b Chungnam National University   (South Korea)

^c National Institute of Animal Science   (South Korea)

^d Sahmyook University   (South Korea)

Author keywords

allotetraploidy; genome evolution; heterochromatin; long terminal repeat retrotransposon; Panax ginseng

Indexed keywords

FISH; FLUORESCENCE MICROSCOPY;

ALLOTETRAPLOIDY; GENOME EVOLUTION; HETEROCHROMATIN; PANAX GINSENG; RETROTRANSPOSON;

GENES;

ARALIACEAE; BACTERIA (MICROORGANISMS); PANAX GINSENG;

PLANT DNA;

ALLOTETRAPLOIDY; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BIOLOGICAL MODEL; CYTOLOGY; DNA SEQUENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; GENOME EVOLUTION; GINSENG; HETEROCHROMATIN; LONG TERMINAL REPEAT; LONG TERMINAL REPEAT RETROTRANSPOSON; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PANAX; PHYLOGENY; PLANT CHROMOSOME; PLANT GENOME; RETROPOSON; TETRAPLOIDY;

ALLOTETRAPLOIDY; GENOME EVOLUTION; HETEROCHROMATIN; LONG TERMINAL REPEAT RETROTRANSPOSON; PANAX GINSENG;

AMINO ACID SEQUENCE; BASE SEQUENCE; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CHROMOSOMES, PLANT; DNA, PLANT; EVOLUTION, MOLECULAR; GENOME, PLANT; HETEROCHROMATIN; IN SITU HYBRIDIZATION, FLUORESCENCE; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PANAX; PHYLOGENY; RETROELEMENTS; SEQUENCE ANALYSIS, DNA; TERMINAL REPEAT SEQUENCES; TETRAPLOIDY;

EID: 84895921714     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12441     Document Type: Article

References (83)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J.H., Zhang, Z., Miller, W., and, Lipman, D.J., (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
2. Ammiraju, J.S., Lu, F., Sanyal, A., et al. (2008) Dynamic evolution of Oryza genomes is revealed by comparative genomic analysis of a genus-wide vertical data set. Plant Cell, 20, 3191-3209.
3. Bang, K.H., Lee, J.W., Kim, Y.C., Kim, D.H., Lee, E.H., and, Jeung, J.U., (2010) Construction of genomic DNA library of Korean ginseng (Panax ginseng C.A. MEYER) and development of sequence-tagged sites. Biol. Pharm. Bull. 33, 1579-1588.
4. Bennetzen, J.L., Ma, J., and, Devos, K.M., (2005) Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 95, 127-132.
5. Benson, G., (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573-580.
6. Charles, M., Belcram, H., Just, J., et al. (2008) Dynamics and differential proliferation of transposable elements during the evolution of the B and A genomes of wheat. Genetics, 180, 1071-1086.
7. Chen, Z.J., and, Ni, Z., (2006) Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. BioEssays, 28, 240-252.
8. Chen, S., Luo, H., Li, Y., et al. (2011) 454 EST analysis detects genes putatively involved in ginsenoside biosynthesis in Panax ginseng. Plant Cell Rep. 30, 1593-1601.
9. Choi, H.I., Kim, N.H., Kim, J.H., Choi, B.S., Ahn, I.O., Lee, J.S., and, Yang, T.J., (2011) Development of reproducible EST-derived SSR markers and assessment of genetic diversity in Panax ginseng cultivars and related species. J. Ginseng Res. 35, 399-412.
10. Choi, H.I., Kim, N.H., Lee, J., Choi, B.S., Kim, K.D., Park, J.Y., Lee, S.C., and, Yang, T.J., (2013) Evolutionary relationship of Panax ginseng and P. quinquefolius inferred from sequencing and comparative analysis of expressed sequence tags. Genet. Resour. Crop Evol. 60, 1377-1387.
11. Coon, J.T., and, Ernst, E., (2002) Panax ginseng. Drug Saf. 25, 323-344.
12. Ewing, B., and, Green, P., (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8, 186-194.
13. Ewing, B., Hillier, L., Wendl, M.C., and, Green, P., (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8, 175-185.
14. Feschotte, C., Jiang, N., and, Wessler, S.R., (2002) Plant transposable elements: where genetics meets genomics. Nat. Rev. Genet. 3, 329-341.
15. Finnegan, D.J., (1989) Eukaryotic transposable elements and genome evolution. Trends Genet. 5, 103-107.
16. Gao, X., Hou, Y., Ebina, H., Levin, H.L., and, Voytas, D.F., (2008) Chromodomains direct integration of retrotransposons to heterochromatin. Genome Res. 18, 359-369.
17. Gordon, D., Abajian, C., and, Green, P., (1998) Consed: a graphical tool for sequence finishing. Genome Res. 8, 195-202.
18. Hanson, R.E., Islam-Faridi, M.N., Crane, C.F., Zwick, M.S., Czeschin, D.G., Wendel, J.F., McKnight, T.D., Price, H.J., and, Stelly, D.M., (2000) Ty1-copia-retrotransposon behavior in a polyploid cotton. Chromosome Res. 8, 73-76.
19. Heslop-Harrison, J.S., (2000) Comparative genome organization in plants: from sequence and markers to chromatin and chromosomes. Plant Cell, 12, 617-635.
20. Ho, I.S.H., and, Leung, F.C., (2002) Isolation and characterization of repetitive DNA sequences from Panax ginseng. Mol. Genet. Genomics, 266, 951-961.
21. Hong, C.P., Lee, S.J., Park, J.Y., et al. (2004) Construction of a BAC library of Korean ginseng and initial analysis of BAC-end sequences. Mol. Genet. Genomics, 271, 709-716.
22. Jo, I.H., Bang, K.H., Kim, Y.C., et al. (2011) Rapid identification of ginseng cultivars (Panax ginseng Meyer) using novel SNP-based probes. J. Ginseng Res. 35, 504-513.
23. Kalendar, R., Vicient, C.M., Peleg, O., Anamthawat-Jonsson, K., Bolshoy, A., and, Schulman, A.H., (2004) Large retrotransposon derivatives: abundant, conserved but nonautonomous retroelements of barley and related genomes. Genetics, 166, 1437-1450.
24. Kidwell, M.G., and, Lisch, D., (1997) Transposable elements as sources of variation in animals and plants. Proc. Natl Acad. Sci. USA, 94, 7704-7711.
25. Kim, Y.J., Shim, J.S., Krishna, P.R., Kim, S.Y., In, J.G., Kim, M.K., and, Yang, D.C., (2008) Isolation and characterization of a glutaredoxin gene from Panax ginseng C. A. Meyer. Plant Mol. Biol. Rep. 26, 335-349.
26. Kim, T.D., Han, J.Y., Huh, G.H., and, Choi, Y.E., (2011) Expression and functional characterization of three squalene synthase genes associated with saponin biosynthesis in Panax ginseng. Plant Cell Physiol. 52, 125-137.
27. Kim, N.H., Choi, H.I., Ahn, I.O., and, Yang, T.J., (2012) EST-SSR marker sets for practical authentication of all nine registered ginseng cultivars in Korea. J. Ginseng Res. 36, 298-307.
28. Kim, J.H., Jung, J.Y., Choi, H.I., Kim, N.H., Park, J.Y., Lee, Y., and, Yang, T.J., (2013) Diversity and evolution of major Panax species revealed by scanning the entire chloroplast intergenic spacer sequences. Genet. Resour. Crop Evol. 60, 413-425.
29. Kimura, M., (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. J. Mol. Evol. 16, 111-120.
30. Kohany, O., Gentles, A.J., Hankus, L., and, Jurka, J., (2006) Annotation, submission and screening of repetitive elements in Repbase: Repbase Submitter and Censor. BMC Bioinformatics, 7, 474.
31. Kronmiller, B.A., and, Wise, R.P., (2009) Computational finishing of large sequence contigs reveals interspersed nested repeats and gene islands in the rf1-associated region of maize. Plant Physiol. 151, 483-495.
32. Kubis, S.E., Schmidt, T., and, Heslop-Harrison, J.S., (1998) Repetitive DNA elements as a major component of plant genomes. Ann. Bot. 82, 45-55.
33. Kumar, A., and, Bennetzen, J.L., (1999) Plant retrotransposons. Annu. Rev. Genet. 33, 479-532.
34. Lee, K.D., and, Huemer, R.P., (1971) Antitumoral activity of Panax ginseng extracts. Jpn. J. Pharmacol. 21, 299-302.
35. Lee, C., and, Wen, J., (2004) Phylogeny of Panax using chloroplast trnC-trnD intergenic region and the utility of trnC-trnD in interspecific studies of plants. Mol. Phylogenet. Evol. 31, 894-903.
36. Lim, K.B., Yang, T.J., Hwang, Y.J., et al. (2007) Characterization of the centromere and peri-centromere retrotransposons in Brassica rapa and their distribution in related Brassica species. Plant J. 49, 173-183.
37. Lloren, S.C., Futami, R., Covelli, L., et al. (2011) The Gypsy database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res. 39, D70-D74.
38. Lynch, M., and, Conery, J.S., (2000) The evolutionary fate and consequences of duplicate genes. Science, 290, 1151-1155.
39. Lysak, M.A., Koch, M.A., Beaulieu, J.M., Meister, A., and, Leitch, I.J., (2009) The dynamic ups and downs of genome size evolution in Brassicaceae. Mol. Biol. Evol. 26, 85-98.
40. Ma, J., and, Bennetzen, J.L., (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc. Natl Acad. Sci. USA, 101, 12404-12410.
41. Ma, J., Devos, K.M., and, Bennetzen, J.L., (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res. 14, 860-869.
42. Marchler-Bauer, A., Anderson, J.B., Chitsaz, F., et al. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37, D205-D210.
43. Obae, S.G., and, West, T.P., (2012) Nuclear DNA content and genome size of American ginseng. J. Med. Plants Res. 6, 4719-4723.
44. Parisod, C., Salmon, A., Zerjal, T., Tenaillon, M., Grandbastien, M.A., and, Ainouche, M., (2009) Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. New Phytol. 184, 1003-1015.
45. Park, M., Jo, S., Kwon, J.K., et al. (2011) Comparative analysis of pepper and tomato reveals euchromatin expansion of pepper genome caused by differential accumulation of Ty3/Gypsy-like elements. BMC Genomics, 12, 85.
46. Park, H.J., Kim, D.H., Park, S.J., Kim, J.M., and, Ryu, J.H., (2012a) Ginseng in traditional herbal prescriptions. J. Ginseng Res. 36, 225-241.
47. Park, M., Park, J., Kim, S., Kwon, J.K., Park, H.M., Bae, I.H., Yang, T.J., Lee, Y.H., Kang, B.C., and, Choi, D., (2012b) Evolution of the large genome in Capsicum annuum occurred through accumulation of single-type long terminal repeat retrotransposons and their derivatives. Plant J. 69, 1018-1029.
48. Sabot, F., Sourdille, P., Chantret, N., and, Bernard, M., (2006) Morgane, a new LTR retrotransposon group, and its subfamilies in wheats. Genetica, 128, 439-447.
49. Saitou, N., and, Nei, M., (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
50. Salamov, A.A., and, Solovyev, V.V., (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res. 10, 516-522.
51. Salina, E.A., Sergeeva, E.M., Adonina, I.G., Shcherban, A.B., Belcram, H., Huneau, C., and, Chalhoub, B., (2011) The impact of Ty3-gypsy group LTR retrotransposons Fatima on B-genome specificity of polyploid wheats. BMC Plant Biol. 11, 99.
52. SanMiguel, P., Tikhonov, A., Jin, Y.K., et al. (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science, 274, 765-768.
53. SanMiguel, P., Gaut, B.S., Tikhonov, A., Nakajima, Y., and, Bennetzen, J.L., (1998) The paleontology of intergene retrotransposons of maize. Nat. Genet. 20, 43-45.
54. Schnable, P.S., Ware, D., Fulton, R.S., et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science, 326, 1112-1115.
55. Schwartz, S., Zhang, Z., Frazer, K.A., Smit, A., Riemer, C., Bouck, J., Gibbs, R., Hardison, R., and, Miller, W., (2000) PipMaker-a web server for aligning two genomic DNA sequences. Genome Res. 10, 577-586.
56. Shibata, S., Tanaka, O., Ando, T., Sado, M., Tsushima, S., and, Ohsawa, T., (1966) Chemical studies on oriental plant drugs. XIV. Protopanaxadiol, a genuine sapogenin of ginseng saponins. Chem. Pharm. Bull. 14, 595-600.
57. Shirasu, K., Schulman, A.H., Lahaye, T., and, Schulze-Lefert, P., (2000) A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res. 10, 908-915.
58. Smyth, D.R., Kalitsis, P., Joseph, J.L., and, Sentry, J.W., (1989) Plant retrotransposon from Lilium henryi is related to Ty3 of yeast and the gypsy group of Drosophila. Proc. Natl Acad. Sci. USA, 86, 5015-5019.
59. Soltis, D.E., Soltis, P.S., Bennett, M.D., and, Leitch, I.J., (2003) Evolution of genome size in the angiosperms. Am. J. Bot. 90, 1596-1603.
60. Stack, S.M., (1984) Heterochromatin, the synaptonemal complex and crossing over. J. Cell Sci. 71, 159-176.
61. Sun, H., Wang, H.T., Kwon, W.S., Kim, Y.J., In, J.G., and, Yang, D.C., (2011) A simple and rapid technique for the authentication of the ginseng cultivar, Yunpoong, using an SNP marker in a large sample of ginseng leaves. Gene, 487, 75-79.
62. Suoniemi, A., Narvanto, A., and, Schulman, A.H., (1996) The BARE-1 retrotransposon is transcribed in barley from an LTR promoter active in transient assays. Plant Mol. Biol. 31, 295-306.
63. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and, Kumar, S., (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739.
64. Tansakul, P., Shibuya, M., Kushiro, T., and, Ebizuka, Y., (2006) Dammarenediol-II synthase, the first dedicated enzyme for ginsenoside biosynthesis, in Panax ginseng. FEBS Lett. 580, 5143-5149.
65. Thompson, J.D., Higgins, D.G., and, Gibson, T.J., (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
66. Vicient, C.M., Suoniemi, A., Anamthawat-Jonsson, K., Tanskanen, J., Beharav, A., Nevo, E., and, Schulman, A.H., (1999) Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell, 11, 1769-1784.
67. Vitte, C., and, Bennetzen, J.L., (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc. Natl Acad. Sci. USA, 103, 17638-17643.
68. Vitte, C., and, Panaud, O., (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons in rice Oryza sativa L. Mol. Biol. Evol. 20, 528-540.
69. Vitte, C., and, Panaud, O., (2005) LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenet. Genome Res. 110, 91-107.
70. Waminal, N.E., Park, H.M., Ryu, K.B., Kim, J.H., Yang, T.J., and, Kim, H.H., (2012) Karyotype analysis of Panax ginseng C.A. Meyer, 1843 (Araliaceae) based on rDNA loci and DAPI band distribution. Comp. Cytogenet. 6, 425-441.
71. Wen, J., (1999) Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Annu. Rev. Ecol. Syst. 30, 421-455.
72. Wen, J., Plunkett, G.M., Mitchell, A.D., and, Wagstaff, S.J., (2001) The evolution of Araliaceae: a phylogenetic analysis based on ITS sequences of nuclear ribosomal DNA. Syst. Bot. 26, 144-167.
73. Wicker, T., and, Keller, B., (2007) 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. 17, 1072-1081.
74. Wicker, T., Stein, N., Albar, L., Feuillet, C., Schlagenhauf, E., and, Keller, B., (2001) Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J. 26, 307-316.
75. Wicker, T., Zimmermann, W., Perovic, D., Paterson, A.H., Ganal, M., Graner, A., and, Stein, N., (2005) A detailed look at 7 million years of genome evolution in a 439 kb contiguous sequence at the barley Hv-eIF4E locus: recombination, rearrangements and repeats. Plant J. 41, 184-194.
76. Wicker, T., Sabot, F., Hua-Van, A., et al. (2007) A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973-982.
77. Witte, C.P., Le, Q.H., Bureau, T., and, Kumar, A., (2001) Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc. Natl Acad. Sci. USA, 98, 13778-13783.
78. Wu, B., Wang, M., Ma, Y., Yuan, L., and, Lu, S., (2012) High-throughput sequencing and characterization of the small RNA transcriptome reveal features of novel and conserved microRNAs in Panax ginseng. PLoS ONE, 7, e44385.
79. Yang, T.J., Lee, S., Chang, S.B., Yu, Y., de Jong, H., and, Wing, R.A., (2005) In-depth sequence analysis of the centromeric region of tomato chromosome 12: identification of a large CAA block and characterization of centromeric retrotransposons. Chromosoma, 114, 103-117.
80. Yang, T.J., Kwon, S.J., Choi, B.S., et al. (2007) Characterization of terminal-repeat retrotransposon in miniature (TRIM) in Brassica relatives. Theor. Appl. Genet. 114, 627-636.
81. Yi, T., Lowry, P.P., Plunkett, G.M., and, Wen, J., (2004) Chromosomal evolution in Araliaceae and close relatives. Taxon, 53, 987-1005.
82. Yun, T.K., (2001) Brief introduction of Panax ginseng C.A. Meyer. J. Korean Med. Sci. 16, S3-S5.
83. Zhao, X.P., Si, Y., Hanson, R.E., Crane, C.F., Price, H.J., Stelly, D.M., Wendel, J.F., and, Paterson, A.H., (1998) Dispersed repetitive DNA has spread to new genomes since polyploid formation in cotton. Genome Res. 8, 682.