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Matita, a New Retroelement from Peanut: Characterization and Evolutionary Context in the Light of the Arachis A–B Genome Divergence

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Matita, a New Retroelement from Peanut: Characterization and Evolutionary Context in the Light of the Arachis A–B Genome Divergence Mol Genet Genomics (2012) 287:21–38 DOI 10.1007/s00438-011-0656-6 ORIGINAL PAPER Matita, a new retroelement from peanut: characterization and evolutionary context in the light of the Arachis A–B genome divergence Stephan Nielen • Bruna S. Vidigal • Soraya C. M. Leal-Bertioli • Milind Ratnaparkhe • Andrew H. Paterson • Olivier Garsmeur • Ange´lique D’Hont • Patricia M. Guimara˜es • David J. Bertioli Received: 10 June 2011 / Accepted: 20 October 2011 / Published online: 27 November 2011 Ó Springer-Verlag 2011 Abstract Cultivated peanut is an allotetraploid with an experiments showed that Matita is mainly located on the AB-genome. In order to learn more of the genomic struc- distal regions of chromosome arms and is of approximately ture of peanut, we characterized and studied the evolution equal frequency on both A- and B-chromosomes. Its of a retrotransposon originally isolated from a resistance chromosome-specific hybridization pattern facilitates the gene analog (RGA)-containing bacterial artificial chromo- identification of individual chromosomes, a useful cyto- some (BAC) clone. It is a moderate copy number Ty1- genetic tool considering that chromosomes in peanut are copia retrotransposon from the Bianca lineage and we mostly metacentric and of similar size. Phylogenetic named it Matita. Fluorescent in situ hybridization (FISH) analysis of Matita elements, molecular dating of transpo- sition events, and an estimation of the evolutionary diver- Communicated by M.-A. Grandbastien. gence of the most probable A- and B-donor species suggest that Matita underwent its last major burst of transposition Electronic supplementary material The online version of this activity at around the same time of the A- and B-genome article (doi:10.1007/s00438-011-0656-6) contains supplementary divergence about 3.5 million years ago. By probing BAC material, which is available to authorized users. libraries with overgos probes for Matita, resistance gene S. Nielen Á S. C. M. Leal-Bertioli Á P. M. Guimara˜es analogues, and single- or low-copy genes, it was demon- Embrapa Recursos Gene´ticos e Biotecnologia, strated that Matita is not randomly distributed in the gen- 70770-917 Brası´lia, DF, Brazil ome but exhibits a significant tendency of being more Present Address: abundant near resistance gene homologues than near sin- S. Nielen (&) gle-copy genes. The described work is a further step Plant Breeding and Genetics Section, Joint FAO/IAEA Division towards broadening the knowledge on genomic and chro- of Nuclear Techniques in Food and Agriculture, mosomal structure of peanut and on its evolution. International Atomic Energy Agency, Vienna, Austria e-mail: [email protected] Keywords Peanut Á Arachis Á Retrotransposon Á B. S. Vidigal Á D. J. Bertioli Evolution Á Fluorescent in situ hybridization Universidade de Brası´lia, Campus Universita´rio, 70910-900 Brası´lia, DF, Brazil Abbreviations B. S. Vidigal Á D. J. Bertioli BAC Bacterial artificial chromosome Universidade Cato´lica de Brası´lia, Campus II, SGAN 916, BES BAC end-sequences 70790-160 Brası´lia, DF, Brazil DAPI 40,6-Diamidino-2-phenylindole M. Ratnaparkhe Á A. H. Paterson EDTA Ethylenediaminetetraacetic acid Plant Genome Mapping Laboratory, The University of Georgia, FISH Fluorescent in situ hybridization Athens 30605, USA FITC Fluorescein isothiocyanate GISH Genomic in situ hybridization O. Garsmeur Á A. D’Hont Centre de Coope´ration International en Recherche Agronomique LTR Long terminal repeat pour le Developpement (CIRAD), Montpellier, France Mya Million years ago 123 22 Mol Genet Genomics (2012) 287:21–38 NBS Nucleotide-binding site different types of SAT chromosomes and the small chro- NOR Nucleolar organizer region mosome pair A9 as a characteristic feature of the A-gen- ORF Open reading frame ome component. The use of DAPI (40-6-diamidino-2- PBS Primer binding site phenylindole) for chromosome staining revealed distinct PPT Poly purine tract heterochromatic bands of A-genome chromosomes with RGA Resistance gene analogue the most prominent band in the pair A9 and absent or RT Reverse transcriptase considerably weaker bands in the B-genome (Seijo et al. SDS Sodium dodecyl sulphate 2004). Using molecular cytogenetics with rDNA sequences SSC Standard saline citrate (19SSC = 0.15 M NaCl; as probes in FISH, the latter authors substantially contrib- 0.015 M Na3-citrate) uted to the identification of the most probable ancestors of UTR Untranslated region peanut. From genetic maps, it is apparent that the order of molecular markers (which are derived predominantly from low-copy DNA) in the A- and B-genomes is mostly co- Introduction linear with only a few major rearrangements (Burow et al. 2001; Moretzsohn et al. 2009). Furthermore, comparative Cultivated peanut (Arachis hypogaea) is tetraploid with an mapping has shown that there is detectable gene synteny AB-genome (2n = 4x = 40) of recent origin, arising from between Arachis and Lotus, Medicago and Phaseolus, hybridization of two wild species and spontaneous chro- legumes that are separated from peanut by an estimated mosome duplication. Comparisons of the karyotypes of divergence time of 55 million years ago (Mya) (Hougaard diploid wild species with A. hypogaea, together with et al. 2008; Bertioli et al. 2009; Wojciechowski et al. 2004; molecular data and phylogeographic considerations, Cannon et al. 2010). This emphasises the slow evolution of suggests that A. duranensis (A-genome) and A. ipae¨nsis gene order and suggests that much of the gene space of the (B-genome) (both 2n = 2x = 20) are the extant species A- and B-genome components is likely to be highly most closely related to the ancestors of cultivated peanut similar. (Kochert et al. 1996; Seijo et al. 2004, 2007; Burow et al. However, in most plants it is repetitive DNA and not 2009). Homoeolgous A- and B-chromosomes rarely pair genes that occupy most of the genome and determine large- during meiosis (Smartt 1990), thus the peanut genome can scale structure of the chromosomes (Schmidt and Heslop- be characterized as being genetically diploid. Harrison 1998). In contrast to the surprising degree of Cultivated peanut has a very limited DNA diversity conservation observed for genes, whole genome in situ (Kochert et al. 1996; Milla et al. 2005). Therefore, wild hybridization suggests that the repetitive genome fractions species are an attractive source of new alleles, traits, and of the A- and B-genomes, and indeed of different species of higher DNA polymorphism which facilitates genetic map wild peanut in general, are substantially diverged (Seijo construction (Simpson et al. 1993; Moretzsohn et al. 2005; et al. 2007). The retroelement FIDEL provides one exam- Leal-Bertioli et al. 2009; Fonce´ka et al. 2009). Cytogenetic ple of a family of repetitive sequences with considerable markers allowing the following of individual chromosomes quantitative and sequence-related divergence between the in hybrids derived from cultivated 9 wild crosses, as well component genomes (Nielen et al. 2010). In allopolyploid as to detect genome/chromosomal rearrangements would species further importance is attached to the repetitive be of great value. For studies based only on cultivated DNA as a dynamic part of the genome. The genomic shock peanut, a lack of available tools for genetic mapping and a resulting from unification of different genomes in one lack of knowledge of the genome in general are major nucleus can initiate reactivation of transposable elements obstacles. A whole genome sequence would be a major with potential consequences for genome structure and gene step to overcome these difficulties. The design of expression (Zhao et al. 1998; Kashkush et al. 2002, 2003; sequencing and assembly strategies, however, require a Petit et al. 2010). more thorough understanding of the repeat structure of the As part of the repetitive DNA, transposable elements peanut genome, which also would contribute to under- and in particular long terminal repeat (LTR) retrotranspo- standing the genetic behaviour and biology of the peanut sons contribute a substantial fraction of genomes, making genome in general. as much as 80% of the genome in plants such as in maize Due to small chromosome sizes and metacentric and (SanMiguel and Bennetzen 1998). LTR elements can be sub-metacentric morphologies karyotype analysis in peanut divided into two superfamilies, the Ty1-copia retrotrans- is challenging. Comprehensive studies of karyotypes in posons (pseudoviridae), and the Ty3-gypsy retrotranspsons Arachis based on classical cytogenetics have been made by (metaviridae) (Xiong and Eickbush 1990), which differ in Ferna´ndez and Krapovickas (1994), who described their reverse transcriptases, and in their structure. In the 123 Mol Genet Genomics (2012) 287:21–38 23 Ty1-copia elements the integrase gene antecedes the (GenBank accession no. AY157808; Bertioli et al. 2003). reverse transcriptase gene and in the Ty3-gypsy elements it A marker derived from this resistance gene analogue maps is located after the RNaseH gene (Kumar and Bennetzen close to a QTL for resistance against late leaf spot 1999). The lifecycle of retrotransposons is complex (Cercosporidium personatum Berk. & M.A. Curtis) in a (reviewed by Sabot and Schulman 2006) and a number of mapping population between the two wild A-genome regulatory measures can interfere between initiation of species A. duranensis and A. stenosperma (Moretzsohn transcription and successful integration of a new complete et al. 2005; Leal-Bertioli et al. 2009). (A. stenosperma is copy (Feschotte et al. 2002). Many retrotransposon copies resistant against rust, late leaf spot, and root knot nema- found in the genome exhibit insertions, deletions, and todes, all important pests of cultivated peanut; Leal-Bertioli frameshifts and thus, are not functional (Kumar and Ben- et al. 2010; Proite et al. 2008). The selected BAC clone netzen 1999, and herein mentioned references). Moreover, AD25F09 was subcloned using two shotgun strategies: solo LTRs are generated by illegitimate intraelement cloning of restriction fragments after HindIII, or BamHI recombination, which counteracts retrotransposon-driven digestion into pBlueScript SK-minus vector and shearing genome expansion (Shirasu et al.
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