Transposable element discovery and characterization of LTR-retrotransposon evolutionary lineages in the tropical fruit species Passiflora edulis
A significant proportion of plant genomes is consists of transposable elements (TEs), especially LTR retrotransposons (LTR-RTs) which are known to drive genome evolution. However, not much information is available on the structure and evolutionary role of TEs in the Passifloraceae family (Malpighiales order). Against this backdrop, we identified, characterized, and inferred the potential genomic impact of the TE repertoire found in the available genomic resources for Passiflora edulis, a tropical fruit species. A total of 250 different TE sequences were identified (96% Class I, and 4% Class II), corresponding to ~ 19% of the P. edulis draft genome. TEs were found preferentially in intergenic spaces (70.4%), but also overlapping genes (30.6%). LTR-RTs accounted for 181 single elements corresponding to ~ 13% of the draft genome. A phylogenetic inference of the reverse transcriptase domain of the LTR-RT revealed association of 37 elements with the Copia superfamily (Angela, Ale, Tork, and Sire) and 128 with the Gypsy (Del, Athila, Reina, CRM, and Galadriel) superfamily, and Del elements were the most frequent. Interestingly, according to insertion time analysis, the majority (95.9%) of the LTR-RTs were recently inserted into the P. edulis genome (< 2.0 Mya), and with the exception of the Athila lineage, all LTR-RTs are transcriptionally active. Moreover, functional analyses disclosed that the Angela, Del, CRM and Tork lineages are conserved in wild Passiflora species, supporting the idea of a common expansion of Copia and Gypsy superfamilies. Overall, this is the first study describing the P. edulis TE repertoire, and it also lends weight to the suggestion that LTR-RTs had a recent expansion into the analyzed gene-rich region of the P. edulis genome, possibly along WGD (Whole genome duplication) events, but are under negative selection due to their potential deleterious impact on gene regions.
KeywordsPassiflora Passion fruit Genome evolution Mobile genetic elements Reverse transcriptase
Mr. Steve Simmons for proofreading the manuscript.
Conceptualization, MLCV; Data curation, ZPC and AMV; Formal analysis, ZPC, LACS, GTR and AMV; Funding acquisition, MLCV; Investigation, ZPC; Methodology, ZPC; Resources, MCD; Supervision, MAVS, HB and MLCV; Writing – original draft, ZPC and MLCV; Writing – review & editing, MAVS and AMV.
This research was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo, Grant Number 2014/25215-2, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, scholarship awarded to ZPC) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, scholarships awarded to ZPC and GTR).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
- 11.Hernandez-Pinzon I, de Jesus E, Santiago N, Casacuberta JM (2009) The frequent transcriptional readthrough of the tobacco Tnt1 retrotransposon and its possible implications for the control of resistance genes. J Mol Evol 68:269–278. https://doi.org/10.1007/s00239-009-9204-y CrossRefPubMedGoogle Scholar
- 17.Bennetzen JL, Wang H (2014) The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol 65:505–530. https://doi.org/10.1146/annurev-arplant-050213-035811 CrossRefPubMedGoogle Scholar
- 23.Ulmer T, MacDougal JM (2004) Passiflora: passionflowers of the world. Timber Press, Portland, p 430Google Scholar
- 36.Smit A, Hubley R, Green P (2018) RepeatMasker 4.0.8Google Scholar
- 41.Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303:3997
- 47.Keane TM, Creevey CJ, Pentony MM et al (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29. https://doi.org/10.1186/1471-2148-6-29 CrossRefPubMedPubMedCentralGoogle Scholar
- 49.Rambaut A (2012) FigTree v. 1.4.0. http://tree.bio.ed.ac.uk/software/figtree/
- 58.Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498. https://doi.org/10.1093/oxfordjournals.molbev.a026248 CrossRefPubMedGoogle Scholar
- 64.Spruyt M, Buquicchio F (2004) Gene Runner for Windows. http://www.generunner.net/
- 81.Thomas J, Pritham EJ (2015) Helitrons, the eukaryotic rolling-circle transposable elements. Mob DNA III. https://doi.org/10.1128/microbiolspec.mdna3-0049-2014 CrossRefGoogle Scholar
- 94.Lynch M (2007) The origins of genome architecture, 1st edn. Sinauer Associates, SunderlandGoogle Scholar