Abstract
The completion of the genome assembly for the economically important coffee plant Coffea canephora (Rubiaceae) has allowed the use of bioinformatic tools to identify and characterize a diverse array of transposable elements (TEs), which can be used in evolutionary studies of the genus. An overview of the copy number and location within the C. canephora genome of four TEs is presented. These are tested for their use as molecular markers to unravel the evolutionary history of the Millotii Complex, a group of six wild coffee (Coffea) species native to Madagascar. Two TEs from the Gypsy superfamily successfully recovered some species boundaries and geographic structure among samples, whereas a TE from the Copia superfamily did not. Notably, species occurring in evergreen moist forests of eastern and southeastern Madagascar were divergent with respect to species in other habitats and regions. Our results suggest that the peak of transpositional activity of the Gypsy and Copia TEs occurred, respectively, before and after the speciation events of the tested Madagascan species. We conclude that the utilization of active TEs has considerable potential to unravel the evolutionary history and delimitation of closely related Coffea species. However, the selection of TE needs to be experimentally tested, since each element has its own evolutionary history. Different TEs with similar copy number in a given species can render different dendrograms; thus copy number is not a good selection criterion to attain phylogenetic resolution.
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Andrianasolo DN, Davis AP, Razafinarivo NJ, Hamon S, Rakotomalala JJ, Sabatier SA (2013) High genetic diversity of in situ and ex situ populations of Madagascan coffee species: further implications for the management of coffee genetic resources. Tree Genet Genomes 9:1295–1312
Batzer MA, Deininger PL (2002) Alu repeats and human genomic diversity. Nat Rev Genet 3:370–379
Briggs JC (2003) The biogeographic and tectonic history of India. J Biogeogr 30:381–388
Capy P, Gasperi G, Biémont C, Bazin C (2001) Stress and transposable elements: co-evolution or useful parasites? Heredity 85:101–106
Casacuberta E, González J (2013) The impact of transposable elements in environmental adaptation. Mol Ecol 22:1503–1517
Charrier A (1978) Le structure génétiques des caféiers spontanés de la région malgache (Mascarocoffea). Leurs relations avec les caféiers d’origine africaine (Eucoffea). Dissertation, Université Paris-Sud Orsay
Chevalier A (1947) Les caféiers du globe. III Systématique des caféiers et faux caféiers. Maladies et insectes nuisibles. Lechevalier P, Paris
Davis AP, Govaerts R, Bridson DM, Stoffelen P (2006) An annotated taxonomic conspectus of the genus Coffea (Rubiaceae). Bot J Lin Soc 152:465–512
Davis AP, Tosh J, Ruch N, Fay M (2011) Growing coffee: Psilanthus (Rubiaceae) subsumed on the basis of molecular and morphological data; implications for the size, morphology, distribution and evolutionary history of Coffea. Bot J Lin Soc 167:357–377
DeBarry JD, Liu R, Bennetzen JL (2008) Discovery and assembly of repeat family pseudomolecules from sparse genomic sequence data using the Assisted Automated Assembler of Repeat Families (AAARF) algorithm. BMC Bioinf. doi:10.1186/1471-2105-9-235
Denoeud F, Carretero-Paulet L, Dereeper A et al (2014) The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345:1181–1184
Dereeper A, Guyot R, Tranchant-Dubreuil C, Anthony F, Argout X, de Bellis F, Combes MC, Gavory F, de Kochko A, Kudrna D, Leroy T, Poulain J, Rondeau M, Song X, Wing R, Lashermes P (2013) BAC-end sequences analysis provides first insights into coffee (Coffea canephora P.) genome composition and evolution. Plant Mol Biol 83:177–189
Dodsworth S, Chase MW, Kelly LJ, Leitch IJ, Macas J, Novák P, Piednoël M, Weiss-Schneeweiss H, Leitch AR (2015) Genomic repeat abundances contain phylogenetic signal. Syst Biol 64:112–126
Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341
Hamon P, Duroy PO, Dubreuil-Tranchant C, Mafra D’Almeida Costa P, Durret C, Razafinarivo NJ, Couturon E, Hamon S, de Kochko A, Poncet V, Guyot R (2011) Two-novel Ty1-copia retrotransposons isolated from coffee trees can effectively reveal evolutionary relationships in the Coffea genus (Rubiaceae). Mol Genet Genomics 285:447–460
Hedrick PW (2000) Genetics of populations, 2nd edn. Jones and Bartlett, Boston
Jing R, Vershinin A, Grzebyta J, Shaw P, Smykal P, Marshall D, Ambrose MA, Noel Ellis TH, Flavell AJ (2010) The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis. BMC Evol Biol. doi:10.1186/1471-2148-10-44
Joshi SP, Gupta VS, Aggarwal RK, Ranjekar PK, Brar DS (2000) Genetic diversity and phylogenetic relationship as revealed by inter simple sequence repeat (ISSR) polymorphism in the genus Oryza. Theor Appl Genet 100:1311–1320
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467
Kalendar R, Schulman AH (2006) IRAP and REMAP for retrotransposon-based genotyping and fingerprinting. Nat Protoc 1:2478–2484
Kalendar R, Grob T, Regina M, Suoniemi A, Schulman AH (1999) IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. Theor Appl Genet 98:704–711
Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH (2000) Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc Natl Acad Sci USA 97:6603–6607
Konovalov FA, Goncharov NP, Goryunova S, Shaturova A, Proshlyakova T, Kudryavtsev A (2010) Molecular markers based on LTR retrotransposons BARE-1 and Jeli uncover different strata of evolutionary relationships in diploid wheats. Mol Genet Genomics 283:551–563
Maguire TL, Peakall R, Saenger P (2002) Comparative analysis of genetic diversity in the mangrove species Avicennia marina (Forsk.) Vierh. (Avicenniaceae) detected by AFLPs and SSRs. Theor Appl Genet 104:388–398
Maurin O, Davis AP, Chester M, Mvungi EF, Jaufeerally-Fakim Y, Fay MF (2007) Towards a phylogeny for Coffea (Rubiaceae): identifying well-supported lineages based on nuclear and plastid DNA sequences. Ann Bot Lond 100:1565–1583
Nowak MD, Davis AP, Yoder AD (2012) Sequence data from new plastid and nuclear COSII regions resolves early diverging lineages in Coffea (Rubiaceae). Syst Bot 37:995–1005
Peakall R, Smouse PE (2006) GeneAlEx 6: genetic analysis in Excel, population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim A, 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 Res 16:1262–1269
Razafinarivo NJ, Rakotomalala JJ, Brown SC, Bourge M, Hamon S, de Kochko A, Poncet V, Dubreuil-Tranchant C, Couturon E, Guyot R, Hamon P (2012) Geographical gradients in the genome size variation of wild coffee trees (Coffea) native to Africa and Indian Ocean islands. Tree Genet Genomes 8:1345–1358
Razafinarivo NJ, Guyot R, Davis AP, Couturon E, Hamon S, Crouzillat D, Rigoreau M, Dubreuil-Tranchant C, Poncet V, De Kochko A, Rakotomalala JJ, Hamon P (2013) Genetic structure and diversity of coffee (Coffea) across Africa and the Indian Ocean islands revealed using microsatellites. Ann Bot 111:229–248
Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16:276–277
Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945
Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864
Schulman AH, Flavell AJ, Noel Ellis TH (2004) The application of LTR retrotransposons as molecular markers in plants. In: Miller WJ, Capy P (eds) Methods in molecular biology, vol 260., Mobile genetic elementsHumana Press Inc, Totowa, pp 145–173
Scotese CR (2000) PALEOMAP project: earth history (paleogeographic maps). Dept. Geol., Univ. Texas, Arlington
Smykal P, Bacova-Kerteszova N, Kalendar R, Corander J, Schulman AH, Pavelek M (2011) Genetic diversity of cultivated flax (Linum usitatissimum L.) germplasm assessed by retrotransposon-based markers. Theor Appl Genet 122:1385–1397
Sonnhammer EL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:GC1–GC10
Untergrasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucl Acid Res 40:e115
Vences M, Wollenberg KC, Vieites DR, Lees DC (2009) Madagascar as a model region of species diversification. Trends Ecol Evol 24:456–465
Vitte C, Panaud O (2005) LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenet Genome Res 110:91–107
Vukich M, Schulman AH, Giordani T, Natali L, Kalendar R, Cavallini A (2009) Genetic variability in sunflower (Helianthus annus L.) and in the Helianthus genus as assessed by retrotransposon-based molecular markers. Theor Appl Genet 119:1027–1038
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
Yoder AD, Heckman KL (2006) Mouse lemur phylogeography revises a model of ecogeographic constraint in Madagascar. In: Lehman SM, Fleagle JG (eds) Primate biogeography. Springer, New York, pp 255–268
Yoder AD, Nowak MD (2006) Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annu Rev Ecol Evol Syst 37:405–431
Acknowledgments
We are grateful to the Plate-forme de Séquençage LabEx CeMEB of the Université de Montpellier for DNA fragment analysis. Clémence Hatt helped with laboratory work and Emily Fitzgerrald with raw data reading.
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This study was funded by the Marie Curie Intra-European Fellowship Program (Grant Number PIEF-GA-2009-251702 to JR).
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Communicated by S. Hohmann.
Data deposition: KM489129, KM489130, KM489131, KM489132, PRJNA242989.
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Roncal, J., Guyot, R., Hamon, P. et al. Active transposable elements recover species boundaries and geographic structure in Madagascan coffee species. Mol Genet Genomics 291, 155–168 (2016). https://doi.org/10.1007/s00438-015-1098-3
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DOI: https://doi.org/10.1007/s00438-015-1098-3