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First insight into divergence, representation and chromosome distribution of reverse transcriptase fragments from L1 retrotransposons in peanut and wild relative species

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Abstract

Peanut is an allotetraploid (2n = 2x = 40, AABB) of recent origin. Arachis duranensis and A. ipaënsis, the most probable diploid ancestors of the cultigen, and several other wild diploid species with different genomes (A, B, D, F and K) are used in peanut breeding programs. However, the genomic relationships and the evolutionary pathways of genome differentiation of these species are poorly understood. We performed a sequence-based phylogenetic analysis of the L1 reverse transcriptase and estimated its representation and chromosome distribution in species of five genomes and three karyotype groups with the aim of contributing to the knowledge of the genomic structure and evolution of peanut and wild diploid relatives. All the isolated rt fragments were found to belong to plant L1 lineage and were named ALI. The best supported phylogenetic groups were not concordant with the genomes or karyotype groups. The copy number of ALI sequences was higher than the expected one for plants and directly related to genome size. FISH experiments revealed that ALI is mainly located on the euchromatin of interstitial and distal regions of most chromosome arms. Divergence of ALI sequences would have occurred before the differentiation of the genomes and karyotype groups of Arachis. The representation and chromosome distribution of ALI in peanut was almost additive of those of the parental species suggesting that the spontaneous hybridization of the two parental species of peanut followed by chromosome doubling would not have induced a significant burst of ALI transposition.

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Abbreviations

LINEs:

Long interspersed nuclear elements

rt :

Reverse transcriptase

GSS:

Genomic survey sequences

ESTs:

Expressed sequence tags

FISH:

Fluorescent in situ hybridization

LTR:

Long terminal repeats

SINEs:

Short interspersed nuclear elements

NJ:

Neighbor joining

GISH:

Genome in situ hybridization

ORFs:

Open reading frames

PCR:

Polymerase chain reaction

dNTPs:

Deoxynucleotide triphosphates

CSPD:

Disodium 3-(4-methoxyspiro {1,2-dioxetane-3,2′-(5′-chloro)tricyclo [3.3.1.13,7]decan}-4-yl)phenyl phosphate

DAPI:

4,6-Diamidino-2-phenylindole

TE:

Transposable element

References

  • Alix K, Heslop-Harrison JS (2004) The diversity of retroelements in diploid and allotetraploid Brassica species. Plant Mol Biol 54:895–909

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers E, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bertioli DJ, Moretzsohn MC, Madsen LH, Sandal N, Leal-Bertioli SC, Guimarães PM, Hougaard BK, Fredslund J, Schauser L, Nielsen AM, Sato S, Tabata S, Cannon SB, Stougaard J (2009) An analysis of synteny of Arachis with Lotus and Medicago sheds new light on the structure, stability and evolution of legume genomes. BMC Genome 10:45

    Article  Google Scholar 

  • Bertioli DJ, Vidigal B, Nielen S, Ratnaparkhe MB, Lee T-H, Leal-Bertioli SCM, Kim C, Guimarães PM, Seijo G, Schwarzacher T, Paterson AH, Heslop-Harrison P, Araujo ACG (2013) The repetitive component of the A genome of peanut (Arachis hypogaea) and its role in remodelling intergenic sequence space since its evolutionary divergence from the B genome. Ann Bot 112:545–559

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Burow MD, Simpson CE, Starr JL, Paterson A (2001) Transmission genetics of chromatin from a synthetic amphidiploid to cultivated peanut (Arachis hypogaea L.): broadening the gene pool of a monophyletic polyploid species. Genetics 159:823–837

    CAS  PubMed Central  PubMed  Google Scholar 

  • Devos KM, Brown JKM, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Di Rienzo JA, Casanoves F, Balzarini MG, González L, Tablada M, Robledo CW (2013) InfoStat version 2014. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar/

  • Doležel J, Bartos J (2005) Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot 95:99–110

    Article  PubMed Central  PubMed  Google Scholar 

  • Doolittle RF, Feng DF, Johnson MS, McClure MA (1989) Origins and evolutionary relationships of retroviruses. Quart Rev Biol 64:1–30

    Article  CAS  PubMed  Google Scholar 

  • Fernández A, Krapovickas A (1994) Cromosomas y evolución en Arachis (Leguminosae). Bonplandia 8:188–220

    Google Scholar 

  • Flavell AJ (1995) Retroelements, reverse transcriptase and evolution. Comp Biochem Physiol B Biochem Mol Biol 110:3–15

    Article  CAS  PubMed  Google Scholar 

  • Grabiele M, Chalup L, Robledo G, Seijo G (2012) Genetic and geographic origin of domesticated peanut as evidenced by 5S rDNA and chloroplast DNA sequences. Plant Syst Evol 298:1151–1165

    Article  Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic linkage Maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: map** strategy and RAPD markers. Genetics 137:1121–1137

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gregory MP, Gregory WC (1979) Exotic germoplasm of Arachis L. interspecific hybrids. J Hered 70:185–193

    Google Scholar 

  • Hammons RO (1994) The origin and history of the groundnut. In: Smartt J (ed) The groundnut crop: a scientific basis for improvement. Chapman & Hall, London, pp 24–39

    Chapter  Google Scholar 

  • Han JS (2010) Non-long terminal repeat (non-LTR) retrotransposons: mechanisms, recent developments, and unanswered questions. Mobile DNA 1:15

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 Res 16:1252–1261

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heitkam T, Schmidt T (2009) BNR-a LINE family from Beta vulgaris-contains a RRM domain in open reading frame 1 and defines a L1 sub-clade present in diverse plant genomes. Plant J 59:872–882

    Article  CAS  PubMed  Google Scholar 

  • Husted L (1936) Cytological studies on the peanut Arachis. II. Chromosome number, morphology and behavior, and their application to the problem of the origin of the cultivated forms. Cytologia 7:396–423

    Article  Google Scholar 

  • Ichimura S, Mita K, Sugaya K (1997) A major non-LTR retrotransposon of Bombyx mori, L1Bm. J Mol Evol 45:253–264

    Article  CAS  PubMed  Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kochert G, Stalker HT, Gimenes M, Galgaro L, Lopes CR, Moore K (1996) RFLP and cytogenetic evidence on the origin and evolution of allotetraploid domesticated peanut, Arachis hypogaea (Leguminosae). Am J Bot 83:1282–1291

    Article  CAS  Google Scholar 

  • Krapovickas A, Gregory W (1994) Taxonomía del género Arachis (Leguminosae). Bonplandia 8:1–186

    Google Scholar 

  • Kubis SE, Heslop-Harrison JS, Desel C, Schmidt T (1998) The genomic organization of non-LTR retrotransposons (LINEs) from three Beta species and five other angiosperms. Plant Mol Biol 36:821–831

    Article  CAS  PubMed  Google Scholar 

  • Kubo Y, Okazaki S, Anzai T, Fujiwara H (2001) Structural and phylogenetic analysis of TRAS, telomeric repeat-specific non-LTR retrotransposon families in Lepidopteran insects. Mol Biol Evol 18:848–857

    Article  CAS  PubMed  Google Scholar 

  • Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532

    Article  CAS  PubMed  Google Scholar 

  • Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921

    Article  CAS  PubMed  Google Scholar 

  • Leeton PR, Smyth DR (1993) An abundant LINE-like element amplified in the genome of Lilium speciosum. Mol Gen Genet 237:97–104

    CAS  PubMed  Google Scholar 

  • Lim KY, Kovarik A, Matyasek R, Chase MW, Clarkson JJ, Grandbastien MA, Leitch AR (2007) Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol 175:756–763

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Wendel JF (2000) Retroelement activation followed by rapid repression in interspecific hybrid plants. Genome 43:874–880

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Madlung A, Tyagi AP, Watson B, Jiang H, Kagochi T, Doerge RW, Martienssen R, Comai L (2005) Genomic changes in synthetic Arabidopsis polyploids. Plant J 41:221–230

    Article  CAS  PubMed  Google Scholar 

  • Malik HS, Burke WD, Eickbush TH (1999) The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol 16:793–805

    Article  CAS  PubMed  Google Scholar 

  • Martin SL, Bushman FD (2001) Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol Cell Biol 2:467–475

    Article  CAS  Google Scholar 

  • Meyers BC, Tingey SV, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11:1660–1676

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moretzhon MC, Gouvea EG, Inglis PW, Leal-Bertioli SCM, Valls JFM, Bertioli DJ (2013) A study of the relationships of cultivated peanut (Arachis hypogaea) and its most closely related wild species using intron sequences and microsatellite markers. Ann Bot 111:113–126

    Article  Google Scholar 

  • Moretzsohn MC, Barbosa AV, Alves-Freitas DM, Teixeira C, Leal-Bertioli SC, Guimarães PM, Pereira RW, Lopes CR, Cavallari MM, Valls JF, Bertioli DJ, Gimenes MA (2009) A linkage map for the B-genome of Arachis (Fabaceae) and its synteny to the A-genome. BMC Plant Biol 9:40

    Article  PubMed Central  PubMed  Google Scholar 

  • Moscone E, Matzke M, Matzke A (1996) The use of combined FISH/GISH in conjunction with DAPI counterstaining to identify chromosomes containing transgene inserts in amphidiploid tobacco. Chromosoma 105:231–236

    Article  CAS  Google Scholar 

  • Nielen S, Campos-Fonseca F, Leal-Bertioli S, Guimaraes P, Seijo G, Town C, Arrial R, Bertioli D (2009) FIDEL—a retrovirus-like retrotransposon and its distinct evolutionary histories in the A- and B-genome components of cultivated peanut. Chromosome Res 18:227–246

    Article  Google Scholar 

  • Nielen S, Vidigal B, Leal-Bertioli S, Ratnaparkhe M, Paterson A, Garsmeur O, D’Hont A, Guimarães P, Bertioli D (2011) Matita, a new retroelement from peanut: characterization and evolutionary context in the light of the Arachis A–B genome divergence. Mol Genet Genomics 287:21–38

    Article  PubMed  Google Scholar 

  • Noma K, Ohtsubo E, Ohtsubo H (1999) Non-LTR retrotransposons (LINEs) as ubiquitous components of plant genomes. Mol Gen Genet 261:71–79

    Article  CAS  PubMed  Google Scholar 

  • Ohshima K, Hamada M, Terai Y, Okada N (1996) The 3′-ends of tRNA-derived short interspersed repetitive elements are derived from the 3′-ends of long interspersed repetitive elements. Mol Cell Biol 16:3756–3764

    CAS  PubMed Central  PubMed  Google Scholar 

  • Petrov DA (2002) Mutational equilibrium model of genome size evolution. Theor Popul Biol 61:531–543

    Article  PubMed  Google Scholar 

  • Robledo G, Seijo JG (2008) Characterization of Arachis D genome using physical map** of heterochromatic regions and rDNA loci by FISH. Genet Mol Biol 31:717–724

    Article  CAS  Google Scholar 

  • Robledo G, Seijo G (2010) Species relationships among the wild B genome of Arachis species (section Arachis) based on FISH map** of rDNA loci and heterochromatin detection: a new proposal for genome arrangement. Theor Appl Genet 121:1033–1046

    Article  PubMed  Google Scholar 

  • Robledo G, Lavia GI, Seijo G (2009) Species relations among wild Arachis species with the A genome as revealed by FISH map** of rDNA loci and heterochromatin detection. Theor Appl Genet 118:1295–1307

    Article  CAS  PubMed  Google Scholar 

  • Rossi M, Gonçalves Araujo P, Van Sluys MA (2001) Survey of transposable elements in sugarcane expressed sequence tags (ESTs). Genet Mol Biol 24:147–154

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sakamoto K, Ohmido N, Fukui K, Kamada H, Satoh S (2000) Site-specific accumulation of a LINE-like retrotransposon in a sex chromosome of the dioecious plant Cannabis sativa. Plant Mol Biol 44:723–732

    Article  CAS  PubMed  Google Scholar 

  • Schmidt T (1999) LINEs, SINEs and repetitive DNA: non-LTR retrotransposons in plant genomes. Plant Mol Biol 40:903–910

    Article  CAS  PubMed  Google Scholar 

  • Schön I, Arkhipova IR (2006) Two families of non-LTR retrotransposons, Syrinx and Daphne, from the Darwinulid ostracod, Darwinula stevensoni. Gene 371:296–307

    Article  PubMed  Google Scholar 

  • Schwarzacher T, Ambros P, Schweizer D (1980) Application of Giemsa banding to orchid karyotype analysis. Plant Syst Evol 134:293–297

    Article  Google Scholar 

  • Schwarz-Sommer Z, Leclercq L, Göbel E, Saedler H (1987) Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J 6:3873–3880

    CAS  PubMed Central  PubMed  Google Scholar 

  • Seijo G, Lavia GI, Fernández A, Krapovickas A, Ducasse D, Moscone EA (2004) Physical map** of 5S and 18S-25S rRNA genes evidences that Arachis duranensis and A. ipaënsis are the wild diploid species involved in the origin of A. hypogaea (Leguminosae). Am J Bot 91:2293–2303

    Article  Google Scholar 

  • Seijo G, Lavia GI, Fernández A, Krapovickas A, Ducasse D, Bertioli DJ, Moscone EA (2007) Genomic relationships between the cultivated peanut (Arachis hypogaea-Leguminosae) and its close relatives revealed by double GISH. Am J Bot 94:1963–1971

    Article  PubMed  Google Scholar 

  • Shirasawa K, Bertioli D, Varshney R, Moretzsohn M, Leal-Bertioli S, Thudi M, Pandey M, Rami J, Foncéka D, Gowda M, Qin H, Guo B, Hong Y, Liang X, Hirakawa H, Tabata S, Isobe S (2013) Integrated consensus map of cultivated peanut and wild relatives reveals structures of the A and B genomes of Arachis and divergence of the legume genomes. DNA Res 20:173–184

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Silvestri MC, Ortiz AM, Lavia GI (2014) rDNA loci and heterochromatin positions support a distinct genome type for ‘x = 9 species’ of section Arachis (Arachis, Leguminosae). Plant Syst Evol. doi:10.1007/s00606-014-1092-y

    Google Scholar 

  • Simpson CE, Krapovickas A, Valls JFM (2001) History of Arachis including evidence of A. hypogaea L. progenitors. Peanut Sci 28:78–80

    Article  Google Scholar 

  • Smartt J, Gregory WC, Gregory MP (1978) The genomes of Arachis hypogaea. 1. Cytogenetic studies of putative genome donors. Euphytica 27:665–675

    Article  Google Scholar 

  • Smyshlyaev G, Voigt F, Blinov A, Barabas O, Novikova O (2013) Acquisition of an Archaea-like ribonuclease H domain by plant L1 retrotransposons supports modular evolution. Proc Natl Acad Sci USA 110:20140–20145

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stalker HT (1991) A new species-section Arachis of peanuts with D genome. Am J Bot 78:630–637

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vaio M, Mazzella C, Porro V, Speranza P, López-Carro B, Estramil E, Folle GA (2007) Nuclear DNA content in allopolyploid species and synthetic hybrids in the grass genus Paspalum. Plant Syst Evol 265:109–121

    Article  CAS  Google Scholar 

  • Valls JFM, Simpson CE (2005) New species of Arachis (Leguminosae) from Brazil, Paraguay and Bolivia. Bonplandia 14:35–63

    Google Scholar 

  • Vershinin AV, Druka A, Alkhimova AG, Kleinhofs A, Heslop-Harrison JS (2002) LINEs and gypsy-like retrotransposons in Hordeum species. Plant Mol Biol 49:1–14

    Article  CAS  PubMed  Google Scholar 

  • Wenke T, Döbel T, Sörensen TR, Junghans H, Weisshaar B, Schmidt T (2011) Targeted identification of short interspersed nuclear element families shows their widespread existence and extreme heterogeneity in plant genomes. Plant Cell 23:3117–3128

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wessler SR (2006) Transposable elements and the evolution of eukaryotic genomes. Proc Natl Acad Sci USA 103:17600–17601

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wicker T, Yahiaoui N, Guyot R, Schlagenhauf E, Liu ZD, Dubcovsky J, Keller B (2003) Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat. Plant Cell 15:1186–1197

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • **ong Y, Eickbush TH (1988) Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol Biol Evol 5:675–690

    CAS  PubMed  Google Scholar 

  • **ong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zupunski V, Gubensek F, Kordis D (2001) Evolutionary dynamics and evolutionary history in the RTE clade of non-LTR retrotransposons. Mol Biol Evol 18:1849–1863

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work is part of S. Samoluk Doctoral Thesis that will be presented in the Facultad de Ciencias Agrarias, Universidad Nacional de Rosario (Santa Fe, Argentina). It was supported by the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), Argentina, Project PICT 2007-1356 and PICT 2012-1875, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina, Project PIP No 11220090100613 and Universidad Nacional del Nordeste, PI No 189. S. Samoluk, M. Podio and L. Chalup received fellowships from CONICET. G. Robledo, S. Pessino, J.P.A. Ortiz and J. G. Seijo are research staff members of CONICET. We would like to thank INTA Manfredi Station, Córdoba, Argentina and the Texas Agriculture Experimental Station, Stephenville, Texas, for providing seeds of some accessions.

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Correspondence to Sergio Sebastián Samoluk.

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10709_2015_9820_MOESM1_ESM.pdf

Alignments of deduced amino acid rt sequences used for construction of NJ trees of ALI elements and LINEs from other species. Arabidopsis thaliana Ta11-1 (L47193), Beta vulgaris BvL2 (FM993987), Zea mays Cin4 (Y00086), Hordeum vulgare BLIN (AJ270056), Cannabis sativa LINE-CS (AB013908), Rattus norvegicus L1 rat (U83119), Homo sapiens L1 hs (U93574), Drosophila melanogaster I (M14954), Drosophila melanogaster Jockey (M22874), Gallus gallus CR1 (U88211). The symbols “-, ? and *” indicates gaps, incomplete codons and stop codons, respectively. (PDF 140 kb)

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Samoluk, S.S., Robledo, G., Podio, M. et al. First insight into divergence, representation and chromosome distribution of reverse transcriptase fragments from L1 retrotransposons in peanut and wild relative species. Genetica 143, 113–125 (2015). https://doi.org/10.1007/s10709-015-9820-y

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