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BraSto, a Stowaway MITE from Brassica: recently active copies preferentially accumulate in the gene space

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Abstract

We characterized a Brassica miniature inverted repeat transposable element (MITE) from the Stowaway superfamily, designated BraSto (Bra ssica Sto waway). BraSto copy number was assessed using real-time quantitative PCR in the two diploid species B. rapa (genome A) and B. oleracea (genome C) and the corresponding allotetraploid species B. napus (genome AC). Phylogenetic relationships among a set of 131 BraSto copies were then analyzed. BraSto appears to have been only moderately amplified in the Brassica genome and was still active recently with marks of proliferation in both diploid Brassica species, which diverged 3.75 million years ago, but also in the allotetraploid species after reuniting of the two differentiated genomes. We characterized insertion sites for low-divergence BraSto copies among the gene space of the B. rapa genome using bioinformatics approaches. For BraSto copies localized nearby or within genes, we observed frequent associations of BraSto with putative promoters and regulatory regions of genes, but exclusion from coding regions. In addition, BraSto was significantly similar to several Brassica expressed sequence tags (ESTs), including stress-induced ESTs. We also demonstrated the enrichment of BraSto sequences in binding sites for transcription factors and other regulatory elements. Our results lead to the question of a role for BraSto in the regulation of gene expression: this putative role, if further confirmed experimentally, would help to obtain a new insight into the significance of MITEs in the functional plant genome.

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Abbreviations

BrGSP:

Brassica rapa genome sequencing project

CDS:

Coding sequence

CI:

Consistency index

EBI:

European bioinformatics institute

EMBL:

European molecular biology laboratory

EMBOSS:

European molecular biology open software suite

EST:

Expressed sequence tag

GSS:

Genome survey sequence

ML:

Maximum likelihood

MITE:

Miniature inverted-repeat transposable element

NCBI:

National centre for biotechnology information

NJ:

Neighbour-joining

TAIR:

The Arabidopsis information resource

TE:

Transposable element

TIGR:

The institute for genomic research

TIR:

Terminal inverted repeat

TSD:

Target site duplication

TSS:

Transcription start site

UTR:

Untranslated region

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Acknowledgments

We are grateful to Anne-Marie Chèvre (INRA Rennes, France) for providing us with the plant material used for this study. We particularly thank Clémentine Vitte and Hadi Quesneville for their expertise in TE evolution and annotation, and Catherine Damerval and Hélène Citerne for their valuable comments on the phylogeny of BraSto. Marie-Pierre Jacquemot, Matthieu Falque and Olivier Martin are acknowledged for discussions on the qPCR approach. We thank Leigh Gebbie for English corrections. Finally, we would like to thank the handling Editor and the anonymous reviewers for helpful comments and suggestions on our manuscript. This work was partly supported by the project “Effect of polyploidy on plant genome biodiversity and evolution” funded by the French Agence Nationale de la Recherche (ANR Biodiversity programme #ANR-05-BDIV-015). VS is supported by a PhD thesis grant from the French Direction Générale de l’Enseignement et de la Recherche (DGER) via AgroParisTech and the French Centre National de la Recherche Scientifique (CNRS).

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  1. Anne Marmagne

    Present address: INRA—Institut Jean Pierre Bourgin, Nutrition Azotée des Plantes, 78026, Versailles Cedex, France

Authors and Affiliations

  1. AgroParisTech/CNRS, UMR 0320/UMR 8120 Génétique Végétale INRA/Univ. Paris-Sud/CNRS/AgroParisTech, Ferme du Moulon, 91190, Gif-sur-Yvette, France

    Véronique Sarilar

  2. CNRS, UMR 0320/UMR 8120 Génétique Végétale INRA/Univ. Paris-Sud/CNRS/AgroParisTech, Ferme du Moulon, 91190, Gif-sur-Yvette, France

    Anne Marmagne

  3. AgroParisTech, UMR 0320/UMR 8120 Génétique Végétale INRA/Univ. Paris-Sud/CNRS/AgroParisTech, Ferme du Moulon, 91190, Gif-sur-Yvette, France

    Philippe Brabant & Karine Alix

  4. INRA, UMR 0320/UMR 8120 Génétique Végétale INRA/Univ. Paris-Sud/CNRS/AgroParisTech, Ferme du Moulon, 91190, Gif-sur-Yvette, France

    Johann Joets

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Correspondence to Karine Alix.

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11103_2011_9794_MOESM3_ESM.doc

Location of the BraSto TIR-specific primers, TIRQ-2F and TIRQ-2R, used to estimate BraSto copy number in different Brassica species by real-time quantitative PCR. (DOC 32 kb)

11103_2011_9794_MOESM4_ESM.ppt

Fifty percent majority-rule consensus trees resulting from phylogenetic analyses performed on 131 BraSto sequences from Brassica, using (a) the neighbour-joining and (b) the maximum likelihood methods. The Stowaway element from Sorghum bicolor (AF488412) was used as outgroup to root the tree. Numbers associated with branches are bootstrap percentages (100 replicates). BraSto copies from B. rapa (A genome), B. oleracea (C genome) and B. napus (AC genome) are indicated in red, blue and violet, respectively. Violet circles indicate B. napus-specific clusters; the violet star indicates the B. napus-specific cluster identified by the NJ method and reported in the tree obtained with maximum parsimony (Fig. 2). (PPT 262 kb)

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Sarilar, V., Marmagne, A., Brabant, P. et al. BraSto, a Stowaway MITE from Brassica: recently active copies preferentially accumulate in the gene space. Plant Mol Biol 77, 59–75 (2011). https://doi.org/10.1007/s11103-011-9794-9

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