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Transposable element discovery and characterization of LTR-retrotransposon evolutionary lineages in the tropical fruit species Passiflora edulis

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Abstract

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.

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Acknowledgements

Mr. Steve Simmons for proofreading the manuscript.

Funding

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).

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Authors and Affiliations

  1. Departamento de Genética, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, 13418-900, Brazil

    Zirlane Portugal da Costa, Luiz Augusto Cauz-Santos & Maria Lucia Carneiro Vieira

  2. Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, 05508-090, Brazil

    Geovani Tolfo Ragagnin & Marie-Anne Van Sluys

  3. Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, 13083-862, Brazil

    Marcelo Carnier Dornelas

  4. Institut National de la Recherche Agronomique (INRA), Centre National de Ressources Génomique Végétales, Castanet-Tolosan, 31326, France

    Hélène Berges

  5. Departamento de Tecnologia, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista, Jaboticabal, 14884-900, Brazil

    Alessandro de Mello Varani

Authors
  1. Zirlane Portugal da Costa
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  2. Luiz Augusto Cauz-Santos
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  3. Geovani Tolfo Ragagnin
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  4. Marie-Anne Van Sluys
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  5. Marcelo Carnier Dornelas
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  6. Hélène Berges
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  7. Alessandro de Mello Varani
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  8. Maria Lucia Carneiro Vieira
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Contributions

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.

Corresponding author

Correspondence to Maria Lucia Carneiro Vieira.

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Electronic supplementary material

Below is the link to the electronic supplementary material.

11033_2019_5047_MOESM1_ESM.pdf

Electronic supplementary material 1—Schematic representation of domains found in 11 DIRS elements from Passiflora edulis. Domain abbreviations and color-coding: GAG = gag (red); MET = methyltransferase (light blue); PROT = protease (green); RT = reverse transcriptase (blue); RH = ribonuclease H (yellow); INT = integrase (purple). Numbers on the right are element lengths (in bp). (PDF 46 kb)

11033_2019_5047_MOESM2_ESM.pdf

Electronic supplementary material 3—Phylogenetic tree of Copia lineages inferred from the complete amino acid sequence of the GAG domain. Maximum Likelihood analysis was based on the WAG+F model. The bootstrap values for each lineage node are indicated in bold type. Sequences from the Gypsy database are indicated by an asterisk. Names and colored lines indicate lineages. The CRM lineage from the Gypsy superfamily was used as the outgroup to produce a rooted tree. (PDF 68 kb)

11033_2019_5047_MOESM3_ESM.pdf

Electronic supplementary material 4—Phylogenetic tree of Gypsy lineages inferred from the complete amino acid sequence of the GAG domain. Maximum Likelihood analysis was based on the JTT model. The bootstrap values for each lineage node are indicated in bold type. Sequences from the Gypsy database are indicated by an asterisk. Names and colored lines indicate lineages. The Sire lineage from the Copia superfamily was used as the outgroup to produce a rooted tree. (PDF 373 kb)

11033_2019_5047_MOESM4_ESM.pdf

Electronic supplementary material 5—Number of complete and incomplete copies of LTR-RTs in nine lineages of the Copia and Gypsy superfamilies. (PDF 54 kb)

11033_2019_5047_MOESM5_ESM.pdf

Electronic supplementary material 6—Whole genome duplication analysis, based on the distribution of synonymous substitutions per synonymous site for pairwise paralogs (dS), showing at least two WGD events that the P. edulis genome has undergone. (PDF 12 kb)

Electronic supplementary material 7 (FASTA 1823 kb)

Electronic supplementary material 8 (DOCX 13 kb)

Electronic supplementary material 9 (XLSX 54 kb)

Electronic supplementary material 10 (DOCX 14 kb)

Electronic supplementary material 2 (XLSX 23 kb)

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da Costa, Z.P., Cauz-Santos, L.A., Ragagnin, G.T. et al. Transposable element discovery and characterization of LTR-retrotransposon evolutionary lineages in the tropical fruit species Passiflora edulis. Mol Biol Rep 46, 6117–6133 (2019). https://doi.org/10.1007/s11033-019-05047-4

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