Copia retrotransposons of two disjunctive Panax species: P. ginseng and P. quinquefolius
X. D. Liu A D , X. F. Zhong A D , Y. Ma A , H. J. Gong A , Y. Y. Zhao A , B. Qi A , Z. K. Yan B , X. B. Sun B and B. Liu A C EA Key Laboratory of Molecular Epigenetics of MOE, Institute of Genetics and Cytology,Northeast Normal University, Changchun 130024, China.
B Jilin Academy of Chinese Traditional Medicine, Changchun 130021, China.
C Key Laboratory of Applied Statistics of MOE, Northeast Normal University, Changchun 130024, China.
D Contributed equally to this work.
E Corresponding author. Email: baoliu6677@yahoo.com.cn
Australian Journal of Botany 56(2) 177-186 https://doi.org/10.1071/BT07030
Submitted: 20 July 2007 Accepted: 22 October 2007 Published: 19 March 2008
Abstract
Sixty highly heterogeneous reverse transcriptase (RT) gene domains, each representing a different copia retrotransposon, were isolated from Panax ginseng and P. quinquefolius, two highly valued medicinal plant species representing classical eastern Asian and eastern North American disjunctive speciation. These RT domains were classifiable into 10 distinct families. While some families contained highly degenerate elements, others were largely composed of intact ones that had been subjected to purifying selection. DNA gel-blot analysis showed that all 10 families existed in both ginseng species, although the copy number of Family 1 showed marked difference between them. All element families appeared heavily methylated in both species, but a difference in cytosine DNA-methylation patterns between the two species was also evident. Thus, the copia retrotransposons in the two ginseng species are diverse and polyphyletic in origin, yet, they all appeared antique and presumably occurred before separation of P. ginseng and P. quinquefolius, followed by genetic and epigenetic differentiation in their respective host genomes.
Acknowledgements
This study was supported by the Program for Changjiang Scholars and Innovative Research Team (PCSIRT) in University (#IRT0519), the National Natural Science Foundation of China (30430060), and the Programme of Introducing Talents of Discipline to Universities (B07017). We are grateful to two anonymous reviewers for their critical and constructive comments to improve the paper.
Alix K,
Ryder CD,
Moore J,
King GJ, Heslop-Harrison JS
(2005) The genomic organization of retrotransposons in Brassica oleracea. Plant Molecular Biology 59, 839–851.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Benabdelmouna A, Darmency H
(2003)
Copia-like retrotransposons in the genus Setaria, sequence heterogeneity, species distribution and chromosomal organization. Plant Systematics and Evolution 237, 127–136.
| Crossref | GoogleScholarGoogle Scholar |
Bennetzen JL
(1996) The contributions of retroelements to plant genome organization, function and evolution. Trends in Microbiology 4, 347–353.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brookfield JF
(2005) The ecology of the genome-mobile DNA elements and their hosts. Nature Reviews. Genetics 6, 128–136.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Capy P,
Gasperi G,
Biemont C, Bazin C
(2000) Stress and transposable elements, co-evolution or useful parasites? Heredity 85, 101–106.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chandler VL, Walbot V
(1986) DNA modification of a maize transposable element correlates with loss of activity. Proceedings of the National Academy of Sciences, USA 83, 1767–1771.
| Crossref | GoogleScholarGoogle Scholar |
Colot V, Rossignol JL
(1999) Eukaryotic DNA methylation as an evolutionary device. BioEssays 21, 402–411.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Finnegan EJ,
Genger PK,
Peacock WJ, Dennis ES
(1998) DNA methylation in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49, 223–248.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Flavell AJ,
Dunbar ER,
Anderson S,
Pearce R,
Hartley R, Kumar A
(1992a)
Ty1-copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucleic Acids Research 20, 3639–3644.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Flavell AJ,
Smith DB, Kumar A
(1992b) Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Molecular & General Genetics 231, 233–242.
Galasso I,
Harrison GE,
Pignone D,
Bres A, Heslop-Harrison JS
(1997) The distribution organization of Ty1-copia -like retrotransposable elements in the genome of Vigna unguiculata (L.) Walp. (cowpea) its relatives. Annals of Botany 80, 327–333.
| Crossref | GoogleScholarGoogle Scholar |
Gao L,
McCarthy EM,
Ganko EW, McDonald JF
(2004) Evolutionary history of Oryza sativa LTR retrotransposons: a preliminary survey of the rice genome sequences. BMC Genomics 5, 18.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Giraud T, Capy P
(1996) Somatic activity of the mariner transposable element in natural populations of Drosophila simulans. Proceedings of the Royal Society of London. Series B. Biological Sciences 263, 1481–1486.
| Crossref | GoogleScholarGoogle Scholar |
Grandbastien MA
(1992) Retroelements in higher plants. Trends in Genetics 8, 103–108.
| PubMed |
Grandbastien MA
(1998) Activation of plant retrotransposons under stress conditions. Trends in Plant Science 3, 181–187.
| Crossref | GoogleScholarGoogle Scholar |
Grandbastien MA,
Spielmann A, Caboche M
(1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337, 376–380.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hall TA
(1999) BioEdit, a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
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 Research 16, 1252–1261.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heslop-Harrison JS,
Bres A,
Taketa S,
Schmidt T,
Vershinin AV,
Alkhimova EG,
Kamm A,
Doudrick RL,
Schwarzacher T,
Katsiotis A,
Kubis S,
Kumar A,
Pearce SR,
Flavell AJ, Harrison GE
(1997) The chromosomal distributions of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica 100, 197–204.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hirochika H, Hirochika R
(1993)
Ty1-copia group retrotransposons as ubiquitous components of plant genomes. Japanese Journal of Genetics 68, 35–46.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hirochika H,
Fukuchi A, Kikuchi F
(1992) Retrotransposon families in rice. Molecular & General Genetics 233, 209–216.
| Crossref | GoogleScholarGoogle Scholar |
Ho IS, Leung FC
(2002) Isolation and characterisation of repetitive DNA sequences from Panax ginseng. Molecular Genetics and Genomics 266, 951–961.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jurka J, Smith T
(1988) A fundamental division in the Alu family of repeated sequences. Proceedings of the National Academy of Sciences, USA 85, 4775–4778.
| Crossref | GoogleScholarGoogle Scholar |
Kato M,
Miura A,
Bender J,
Jacobse SE, Kakutani T
(2003) Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Current Biology 13, 421–426.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kimura M
(1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kumar S,
Tamura K, Nei M
(2004) MEGA3, Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liu B, Wendel JF
(2000) Retrotransposon activation followed by rapid repression in introgressed rice plants. Genome 43, 874–880.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liu B,
Segal G,
Vega JM,
Feldman M, Abbo S
(1997) Isolation and characterisation of chromosome-specific sequences from a chromosome arm genomic library of common wheat. The Plant Journal 11, 959–965.
| Crossref | GoogleScholarGoogle Scholar |
Matsuoka Y, Tsunewaki K
(1996) Wheat retrotransposon families identified by reverse transcriptase domain analysis. Molecular Biology and Evolution 13, 1384–1392.
| PubMed |
McAllister BF, Werren JH
(1997) Phylogenetic analysis of a retrotransposon with implications for strong evolutionary constraints on reverse transcriptase. Molecular Biology and Evolution 14, 69–80.
| PubMed |
McClelland M,
Nelson M, Raschke E
(1994) Effect of site-specific modification on restriction endonucleases DNA modification methyltransferases. Nucleic Acids Research 22, 3640–3659.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Miller WJ, Capy P
(2004) Mobile genetic elements as natural tools for genome evolution. Methods in Molecular Biology 260, 1–20.
| PubMed |
Nei M, Gojobori T
(1986) Simple methods for estimating the numbers of synonymous non-synonymous nucleotide substitutions. Molecular Biology and Evolution 3, 418–426.
| PubMed |
Pearce SR,
Harrison G,
Li D,
Heslop-Harrison J,
Kumar A, Flavell AJ
(1996) The Ty1-copia group retrotransposons in Vicia species, copy number, sequence heterogeneity and chromosomal localization. Molecular & General Genetics 250, 305–315.
Pearce SR,
Harrison G,
Heslop-Harrison JS,
Flavell AJ, Kumar A
(1997) Characterisation and genomic organization of Ty1-copia group retrotransposons in rye (Secale cereale). Genome 40, 617–625.
| PubMed |
Pereira V
(2004) Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biology 5, R79.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Piegu B,
Guyot R,
Picault N,
Roulin A,
Saniyal A,
Kim H,
Collura K,
Brar DS,
Jackson S,
Wing RA, Panaud O
(2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Research 16, 1262–1269.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Potter S,
Truett M,
Phillips M, Maher A
(1980) Eucaryotic transposable genetic elements with inverted terminal repeats. Cell 20, 639–647.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rabinowicz PD,
Citek R,
Budiman MA,
Nunberg A,
Bedell JA,
Lakey N,
O’Shaughnessy AL,
Nascimento LU,
McCombie WR, Martienssen RA
(2005) Differential methylation of genes and repeats in land plants. Genome Research 15, 1431–1440.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ros F, Kunze R
(2001) Regulation of activator/dissociation transposition by replication DNA methylation. Genetics 157, 1723–1733.
| PubMed |
Saitou N, Nei M
(1987) The neighbor-joining method, a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
| PubMed |
San Miguel PA,
Tikhonov YK,
Jin Y,
Motchoulskaia N,
Zakharrov D,
Melake-Berhan A,
Springer P,
Edward K,
Lee M,
Avramova Z, Bennetzen J
(1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274, 765–768.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shan X,
Liu Z,
Dong Z,
Wang Y,
Chen Y,
Lin X,
Long L,
Han F,
Dong Y, Liu B
(2005) Mobilization of the active MITE transposons Ping Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Molecular Biology and Evolution 22, 976–990.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Suoniemi A,
Anamthawat-Jonsson K,
Arna T, Schulman AH
(1996) Retrotransposon BARE-1 is a major, dispersed component of the barley (Hordeum vulgare L.) genome. Plant Molecular Biology 30, 1321–1329.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tel-Zur N,
Abbo S,
Myslabodski D, Mizrahi Y
(1999) Modified CTAB procedure for DNA isolation from epiphytic cacti of the genera Hylocereus and Selenicereus (Cactaceae). Plant Molecular Biology Reporter 17, 249–254.
| Crossref | GoogleScholarGoogle Scholar |
Thompson JD,
Higgins DG, Gibson TJ
(1994) CLUSTAL W, improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vanderwiel PL,
Voytas DF, Wendel JF
(1993)
Copia-like retrotransposable element evolution in diploid polyploid cotton (Gossypium L.). Journal of Molecular Evolution 36, 429–447.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vitte C,
Panaud Q, Quesneville H
(2007) LTR retrotransposons in rice (Oryza sativa L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics art. no. 218. 8,
| Crossref |
PubMed |
Voytas DF, Ausubel FM
(1988) A copia-like transposable element family in Arabidopsis thaliana. Nature 336, 242–244.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Voytas DF,
Cummings MP,
Konieczny A,
Ausubel FM, Rodermel SR
(1992)
Copia-like retrotransposons are ubiquitous among plants. Proceedings of the National Academy of Sciences of the United States of America 89, 7124–7128.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wang S,
Zhang Q,
Maughan PJ, Saghai-Maroof MA
(1997)
Copia-like retrotransposons in rice, sequence heterogeneity, species distribution and chromosomal locations. Plant Molecular Biology 33, 1051–1058.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wang X,
Sakuma T,
Asafu-Adjaye E, Shiu GK
(1999) Determination of ginsenosides in plant extracts from Panax ginseng and Panax quinquefolius L by LC/MS/MS. Analytical Chemistry 71, 1579–1584.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wen J, Zimmer EA
(1996) Phylogeny and biogeography of Panax L. (the Ginseng genus, Araliaceae): inferences from ITS sequences of nuclear ribosomal DNA. Molecular Phylogenetics and Evolution 6, 167–177.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wessler SR
(1996) Plant retrotransposons, turned on by stress. Current Biology 6, 959–961.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wessler SR,
Bureau TE, White SE
(1996) LTR-retrotransposons MITEs, important players in the evolution of plant genome. Current Opinion in Genetics & Development 5, 814–821.
| Crossref | GoogleScholarGoogle Scholar |
White SE,
Habera LF, Wessler SR
(1994) Retrotransposons in the flanking regions of normal plant genes, a role for copia-like elements in the evolution of gene structure and expression P. Proceedings of the National Academy of Sciences, USA 91, 11792–11796.
| Crossref | GoogleScholarGoogle Scholar |
Wicker T, 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 Research 17, 1072–1081.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Xiong Y, Eickbush TH
(1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO Journal 9, 3353–3362.
| PubMed |
Yoder JA,
Walsh CP, Bestor TH
(1997) Cytosine methylation and the ecology of intragenomic parasites. Trends in Genetics 13, 335–340.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhu S,
Fushimi H,
Cai S, Komatsu K
(2003) Phylogenetic relationship in the genus Panax, inferred from chloroplast trnK gene nuclear 18S rRNA gene sequences. Planta Medica 69, 647–653.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Appendix 1.
Alignment of predicted amino acid sequences across conserved domains of Ty1-copia retrotransposons isolated from the two ginseng species, Panax ginseng and P. quinquefolius Reverse transcriptase (RT) sequences are placed according to their degree of similarity. The PCR primer regions corresponding to the conserved QMDVK and YVDDM motifs, respectively, at the amino and carboxyl ends are included. Black shading corresponds to ≥90% similarity, dark-grey shading corresponds to ≥80% similarity, and light-grey shading corresponds to ≥50% similarity. Frame shift was introduced artificially for some sequences to optimise the alignment. Dashes and asterisks refer to gaps and stop codons, respectively (available as an Accessory Publication on the web).
Appendix 2.
A diagrammatic illustration of the uniform deletion of 69 bp in all 11 members of the Family 4 ginseng copia retroelements Primers and deletion sites are indicated (available as an Accessory Publication on the web).
