Abstract
Cultivated peanut is an allotetraploid with an AB-genome. In order to learn more of the genomic structure of peanut, we characterized and studied the evolution of a retrotransposon originally isolated from a resistance gene analog (RGA)-containing bacterial artificial chromosome (BAC) clone. It is a moderate copy number Ty1-copia retrotransposon from the Bianca lineage and we named it Matita. Fluorescent in situ hybridization (FISH) experiments showed that Matita is mainly located on the distal regions of chromosome arms and is of approximately equal frequency on both A- and B-chromosomes. Its chromosome-specific hybridization pattern facilitates the identification of individual chromosomes, a useful cytogenetic tool considering that chromosomes in peanut are mostly metacentric and of similar size. Phylogenetic analysis of Matita elements, molecular dating of transposition events, and an estimation of the evolutionary divergence of the most probable A- and B-donor species suggest that Matita underwent its last major burst of transposition activity at around the same time of the A- and B-genome divergence about 3.5 million years ago. By probing BAC libraries with overgos probes for Matita, resistance gene analogues, and single- or low-copy genes, it was demonstrated that Matita is not randomly distributed in the genome but exhibits a significant tendency of being more abundant near resistance gene homologues than near single-copy genes. The described work is a further step towards broadening the knowledge on genomic and chromosomal structure of peanut and on its evolution.
This is a preview of subscription content, access via your institution.





Abbreviations
- BAC:
-
Bacterial artificial chromosome
- BES:
-
BAC end-sequences
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- EDTA:
-
Ethylenediaminetetraacetic acid
- FISH:
-
Fluorescent in situ hybridization
- FITC:
-
Fluorescein isothiocyanate
- GISH:
-
Genomic in situ hybridization
- LTR:
-
Long terminal repeat
- Mya:
-
Million years ago
- NBS:
-
Nucleotide-binding site
- NOR:
-
Nucleolar organizer region
- ORF:
-
Open reading frame
- PBS:
-
Primer binding site
- PPT:
-
Poly purine tract
- RGA:
-
Resistance gene analogue
- RT:
-
Reverse transcriptase
- SDS:
-
Sodium dodecyl sulphate
- SSC:
-
Standard saline citrate (1×SSC = 0.15 M NaCl; 0.015 M Na3-citrate)
- UTR:
-
Untranslated region
References
Alix K, Heslop-Harrison JS (2004) The diversity of retroelements in diploid and allotetraploid Brassica species. Plant Mol Biol 54:895–909
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Ameline-Torregrosa C, Wang B-B, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2008) Identification and characterization of Nucleotide-Binding Site-Leucine-Rich Repeat genes in the model plant Medicago truncatula. Plant Physiol 146:5–21
Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot (Lond) 95:127–132
Bertioli DJ, Leal-Bertioli SCM, Lion MB, Santos VL, Pappas G Jr, Cannon SB, Guimarães PM (2003) A large scale analysis of resistance gene homologues in Arachis. Mol Genet Genomics 270:34–45
Bertioli D, Moretzsohn M, Madsen LH, Sandal N, Leal-Bertioli SCM, 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 Genomics 10:45
Burow MD, Simpson CE, Starr JL, Paterson AH (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
Burow MD, Simpson CE, Faries MW, Starr JL, Paterson AH (2009) Molecular biogeographic study of recently described B- and A-genome Arachis species, also providing new insights into the origins of cultivated peanut. Genome 52:107–119
Cannon SB, Ilut D, Farmer AD, Maki SL, May GD et al (2010) Polyploidy did not predate the evolution of nodulation in all legumes. PLoS ONE 5(7):e11630
Choi HK, Mun JH, Jin Kim DJ, Zhu H, Baek JM, Mudge J, Roe B, Ellis N, Doyle J, Kiss GB, Young ND, Cook DR (2004) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci USA 101:15289–15294
Choi HK, Luckow MA, Doyle J, Cook DR (2006) Development of nuclear gene-derived molecular markers linked to legume genetic maps. Mol Genet Genomics 276:56–70
Creste S, Tulmann Neto A, Figueira A (2001) Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining. Plant Mol Biol Rep 19:299–306
Devos KM, Brown JKM, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079
Di Gaspero G, Cipriani G, Adam-Blondon AF, Testolin R (2007) Linkage maps of grapevine displaying the chromosomal locations of 420 microsatellite markers and 82 markers for R-gene candidates. Theor Appl Genet 114:1249–1263
Du J, Tian Z, Hans CS, Laten HM, Cannon SB, Jackson SA, Shoemaker RC, Ma J (2010) Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J 63:584–598
Dvorak J, Yang ZL, You FM, Luo MC (2004) Deletion polymorphism in wheat chromosome regions with contrasting recombination rates. Genetics 168:665–675
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Ewing B, Green P (1998) Base-calling of automated sequencer traces using Phred II. Error probabilities. Genome Res 8:186–194
Fávero AP, Simpson CE, Valls JFM, Vello NA (2006) Study of the evolution of cultivated peanut through crossability studies among Arachis ipaënsis, A. duranensis, and A. hypogaea. Crop Sci 46:1546–1552
Fernández A, Krapovickas A (1994) Cromosomas y evolucíon en Arachis (Leguminosae). Bonplandia 8:187–220
Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341
Foncéka D, Hodo-Abalo T, Rivallan R, Faye I, Sall MN, Ndoye O, Fávero AP, Bertioli DJ, Glaszmann JC, Courtois B, Rami JF (2009) Genetic mapping of wild introgressions into cultivated peanut: a way toward enlarging the genetic basis of a recent allotetraploid. BMC Plant Biol 9:103
Fredslund J, Madsen LH, Hougaard BK, Nielsen AM, Bertioli D, Sandal N, Stougaard J, Schauser LA (2006) A general pipeline for the development of anchor markers for comparative genomics in plants. BMC Genomics 7:207
Garber K, Bilic I, Tohme J, Bachmair A, Schweizer D, Jantsch V (1999) The Tpv2 family of retrotransposons of Phaseolus vulgaris: structure, integration characteristics, and use for phenotypic classification. Plant Mol Biol 39:797–807
Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7:1869–1885
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224
Graham MA, Marek LF, Shoemaker RC (2002) Organization, expression and evolution of a disease resistance gene cluster in soybean. Genetics 162:1961–1977
Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137
Guimarães PM, Garsmeur O, Proite K, Leal-Bertioli SCM, Seijo G, Chaine C, Bertioli DJ, D`Hont A (2008) BAC libraries construction from the ancestral diploid genomes of the allotetraploid cultivated peanut. BMC Plant Biol 8:14
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41:95–98
Hammons RO (1994) The origin and early history of the peanut. In: Smartt J (ed) The peanut crop: a scientific basis for improvement. Chapman and Hall, London, pp 24–42
Hawkins JF, Kim HR, 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
Hougaard BK, Madsen LH, Sandal N, Moretzsohn MC, Fredslund J, Schauser L, Nielsen AM, Rohde T, Sato S, Tabata S, Bertioli DJ, Stougaard J (2008) Legume anchor markers link syntenic regions between Phaseolus vulgaris, Lotus japonicus, Medicago truncatula and Arachis. Genetics 179:2299–2312
Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877
Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312
Inés LG, Fernández A (2004) Karyotypic studies in Arachis hypogaea L. varieties. Caryologia 57:353–359
Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659
Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
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
Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532
Lavia GI, Ortiz AM, Fernández A (2009) Karyotypic studies in wild germplasm of Arachis (Leguminosae). Genet Resour Crop Evol 56:755–764
Leal-Bertioli SCM, José ACFV, Alves-Freitas DMT, Moretzsohn MC, Guimarães PM, Nielen S, Vidigal B, Pereira RW, Pike J, Fávero AP, Parniske M, Varshney R, Bertioli DJ (2009) Identification of candidate genome regions controlling disease resistance in Arachis. BMC Plant Biol 9:112
Leal-Bertioli SCM, de Farias MP, Silva PIT, Guimarães PM, Brasileiro ACM, Bertioli DJ, Guerra de Araújo AC (2010) Ultrastructure of the initial interaction of Puccinia arachidis and Cercosporidium personatum with leaves of Arachis hypogaea and Arachis stenosperma. J Phytopathol 158:792–796
Ma JX, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA 101:12404–12410
Madsen LH, Collins NC, Rakwalska M, Backes G, Sandal N, Krusell L, Jensen J, Waterman EH, Jahoor A, Ayliffe M, Pryor AJ, Langridge P, Schulze-Lefert P, Stougaard J (2003) Barley disease resistance gene analogs of the NBS-LRR class: identification and mapping. Mol Genet Genomics 269:150–161
Maluszynska J, Heslop-Harrison JS (1993) Physical mapping of rDNA loci in Brassica species. Genome 36:774–781
Melayah D, Lim KY, Bonnivard E, Chalhoub B, de Borne FD, Mhiri C, Leitch AR, Grandbastien M-A (2004) Distribution of the Tnt1 retrotransposon family in the amphidiploid tobacco (Nicotiana tabacum) and its wild Nicotiana relatives. Biol J Linn Soc 82:639–649
Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130
Milla SR, Isleib TG, Stalker HT (2005) Taxonomic relationshipsamong Arachis sect. Arachis species as revealed by AFLP markers. Genome 48:1–11
Moisy C, Garrisonc KE, Meredith CP, Pelsy F (2008) Characterization of ten novel Ty1/copia-like retrotransposon families of the grapevine genome. BMC Genomics 9:469
Moretzsohn MC, Leoi L, Proite K, Guimarães PM, Leal-Bertioli SCM, Gimenes MA, Martins WS, Valls JFM, Grattapaglia D, Bertioli DJ (2005) Microsatellite based, gene-rich linkage map for the AA genome of Arachis (Fabaceae). Theor Appl Genet 111:1060–1071
Moretzsohn MC, Barbosa AVG, Alves-Freitas DMT, Teixeira C, Leal-Bertioli SCM, Guimarães PM, Pereira RW, Lopes CR, Cavallari MM, Valls JFM, 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
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Nielen S, Campos-Fonseca F, Leal-Bertioli S, Guimarães P, Seijo JG, Town C, Cook D, Arrial R, Bertioli D (2010) FIDEL—a retrovirus-like retrotransposon and its distinct evolutionary histories in the A and B-genome components of cultivated peanut. Chromosom Res 18:227–246
Ott A, Trautschold B, Sandhu D (2011) Using microsatellites to understand the physical distribution of recombination on soybean chromosomes. PLoS ONE 6:e22306
Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C, Ainouche M, Chalhoub B, Grandbastien M-A (2010) Impact of transposable elements in organization and functioning of allopolyploid genomes. New Phytol 186:37–45
Pereira V (2004) Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol 5:R79
Peterson-Burch BD, Voytas DF (2002) Genes of the Pseudoviridae (Ty1/copia retrotransposons). Mol Biol Evol 19:1832–1845
Petit M, Guidat C, Daniel J, Denis E, Montoriol E, Lim KY, Kovarik A, Leitch AR, Grandbastien M-A, Mhiri C (2010) Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytol 186:135–147
Proite K, Carneiro R, Falcão R, Gomes A, Leal-Bertioli S, Guimarães P, Bertioli D (2008) Post-infection development and histopathology of Meloidogyne arenaria race 1 on Arachis spp. Plant Pathol 57:974–980
Robledo G, Lavia GI, Seijo G (2009) Species relations among wild Arachis species with the A genome as revealed by FISH mapping of rDNA loci and heterochromatin detection. Theor Appl Genet 118:1295–1307
Ross MT, LaBrie T, McPherson J, Stanton VM (1999) Screening large-insert libraries by hybridization. Wiley, New York
Sabot F, Schulman AH (2006) Parasitism and the retrotransposon life cycle in plants: a hitchhiker’s guide to the genome. Heredity 97:381–388
Sakata K, Nagamura Y, Numa H, Antonio BA, Nagasaki H, Idonuma A, Watanabe W, Shimizu Y, Horiuchi I, Matsumoto T, Sasaki T, Higo K (2002) RiceGAAS: an automated annotation system, database for rice genome sequence. Nucleic Acids Res 30:98–102
SanMiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot (Lond) 82(Supplement A):37–44
SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45
Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large scale organization of plant chromosomes. Trends Plant Sci 3:195–199
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Myron Peto, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernethy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X-C, Shinozaki K, Nguyen H, Wing R, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacy G, Shoemker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183
Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115
Schrire BD, Lewis GP, Lavin M (2005) Biogeography of the Leguminosae. In: Lewis G, Schrire B, Mackinder B, Lock M (eds) Legumes of the world. Kew Royal Botanic Gardens, Kew, pp 21–54
Schwarzacher T, Heslop-Harrison JS (2000) Practical in situ hybridization. Springer, New York
Seijo JG, Lavia GI, Fernández A, Krapovickas A, Ducasse D, Moscone EA (2004) Physical mapping of 5S and 18S–25S rRNA genes as evidence that Arachis duranensis and A. ipaënsis are the wild diploid species involved in the origin of A. hypogaea (Leguminosae). Am J Bot 91:1294–1303
Seijo JG, 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
Shirasu K, Schulman AH, Lahaye T, Schulze-Lefert P (2000) A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res 10:908–915
Simpson CE, Starr JL, Nelson SC, Woodard KE, Smith OD (1993) Registration of TxAG6 and TxAG7 peanut germplasm. Crop Sci 33:1418
Smartt J (1990) The groundnut, Arachis hypogaea L. In: Smartt J (ed) Grain legumes: evolution and genetic resources. Cambridge University Press, Cambridge, pp 30–84
Spielmeyer W, Moullet O, Laroche A, Lagudah ES (2000) Highly recombinogenic regions at seed storage protein loci on chromosome 1DS of Aegilops tauschii, the D-genome donor of wheat. Genetics 155:361–367
Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5:233–241
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Thompson JD, Higgins DG, Gibson TJ (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
Thornton JW, DeSalle R (2000) Gene family evolution and homology: genomics meets phylogenetics. Ann Rev Genomics Hum Genet 1:41–73
Van de Peer Y (2004) Computational approaches to unveiling ancient genome duplications. Nat Rev Genet 5:752–763
Vicient CM, Suoniemi A, Anamthawat-Jonsson K et al (1999) Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11:1769–1784
Vitte C, Bennetzen JL (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci USA 103:17638–17643
Vogt VM (1997) Retroviral virions and genomes. In: Coffin J, Hughes SH, Varmus HE (eds) Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 27–70
Wang H, Liu J-S (2008) LTR retrotransposon landscape in Medicago truncatula: more rapid removal than in rice. BMC Genomics 9:382
Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191
Wawrzynski A, Ashfield T, Chen NWG, Mammadov J, Nguyen A, Podicheti R, Cannon SB, Thareau V et al (2008) Replication of nonautonomous retroelements in soybean appears to be both recent and common. Plant Physiol 148:1760–1771
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 Res 17:1072–1081
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982
Wojciechowski MF, Lavin M, Sanderson MJ (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid MatK gene resolves many well-supported subclades within the family. Am J Bot 91:1846–1862
Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362
Yüksel B, Paterson AH (2005) Construction and characterization of a peanut HindIII BAC library. Theor Appl Genet 111:630–639
Yüksel B, Estill JC, Schulze SR, Paterson AH (2005) Organization and evolution of resistance gene analogs in peanut. Mol Genet Genomics 274:248–263
Zhang XY, Wessler SR (2004) Genome-wide comparative analysis of the transposable elements in the related species Arabidopsis thaliana and Brassica oleracea. Proc Natl Acad Sci USA 101:5589–5594
Zhao XP, Si Y, Hanson RE, Crane CF, Price HJ, Stelly DM, Wendel JF, Paterson AH (1998) Dispersed repetitive DNA has spread to new genomes since polyploid formation in cotton. Genome Res 8:479–492
Acknowledgments
Stephan Nielen would like to thank the National Council for Scientific and Technological Development of Brazil (CNPq) for a post-doctoral fellowship. Bruna Vidigal is grateful for post-graduate grants from the Brazilian Ministry of Education (CAPES—Coordenação de Aperfeiçoamento de Pessoal de Nível Superior). David Bertioli would also like to thank CNPq for a productivity fellowship. We also thank the Generation Challenge Program (TLI) for supporting this work. We thank José Valls for providing Arachis germplasm.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M.-A. Grandbastien.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nielen, S., Vidigal, B.S., Leal-Bertioli, S.C.M. et al. 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 (2012). https://doi.org/10.1007/s00438-011-0656-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-011-0656-6
Keywords
- Peanut
- Arachis
- Retrotransposon
- Evolution
- Fluorescent in situ hybridization