Skip to main content
Log in

LTR-TEs abundance, timing and mobility in Solanum commersonii and S. tuberosum genomes following cold-stress conditions

  • Short Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Copia/Ale is the youngest lineage in both Solanum tuberosum and S. commersonii. Within it, we identified nightshade, a new LTR element active in the cultivated potato.

Abstract

From an evolutionary perspective, long-terminal repeat retrotransposons (LTR-RT) activity during stress may be viewed as a mean by which organisms can keep up rates of genetic adaptation to changing conditions. Potato is one of the most important crop consumed worldwide, but studies on LTR-RT characterization are still lacking. Here, we assessed the abundance, insertion time and activity of LTR-RTs in both cultivated Solanum tuberosum and its cold-tolerant wild relative S. commersonii genomes. Gypsy elements were more abundant than Copia ones, suggesting that the former was somehow more successful in colonizing potato genomes. However, Copia elements, and in particular, the Ale lineage, are younger than Gypsy ones, since their insertion time was in average ~ 2 Mya. Due to the ability of LTR-RTs to be circularized by the host DNA repair mechanisms, we identified via mobilome-seq a Copia/Ale element (called nightshade, informal name used for potato family) active in S. tuberosum genome. Our analyses represent a valuable resource for comparative genomics within the Solanaceae, transposon-tagging and for the design of cultivar-specific molecular markers in potato.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Abbreviations

LTR-RTs:

Long-terminal repeat retrotransposons

TE:

Transposable element

DOC:

Depth of coverage

eccDNA:

Extrachromosomal circular DNA

References

  • Achour Z, Joets J, Leguilloux M, Sellier H, Pichon J-P, Leveugle M et al (2019) Low temperature triggers genome-wide hypermethylation of transposable elements and centromeres in maize. Biorxiv.org. https://doi.org/10.1101/573915

    Article  Google Scholar 

  • Alzohairy AM, Sabir JSM, Gyulai G, Younis RAA, Jansen RK, Bahieldin A (2014) Environmental stress activation of plant long-terminal repeat retrotransposons. Funct Plant Biol 41:557–567

    Article  CAS  Google Scholar 

  • Argout X, Salse J, Aury JM et al (2011) The genome of Theobroma cacao. Nat Genet 43:101–108

    Article  CAS  Google Scholar 

  • Aversano R, Contaldi F, Ercolano MR et al (2015) The Solanum commersonii genome sequence provides insights into adaptation to stress conditions and genome evolution of wild potato relatives. Plant Cell 27:954–968

    Article  CAS  Google Scholar 

  • Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24:1242–1255

    Article  CAS  Google Scholar 

  • Carputo D, Castaldi L, Caruso I, Aversano R, Monti L, Frusciante L (2007) Resistance to frost and tuber soft rot in near-pentaploid Solanum tuberosumS. commersonii hybrids. Breed Sci 57:145–151

    Article  Google Scholar 

  • Cho J, Benoit M, Catoni M, Drost HG, Brestovitsky A, Oosterbeek M, Paszkowski J (2019) Sensitive detection of pre-integration intermediates of long terminal repeat retrotransposons in crop plants. Nat Plants 5:26–33

    Article  CAS  Google Scholar 

  • Coil D, Jospin G, Darling AE (2015) AE A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics 31:587–589

    Article  CAS  Google Scholar 

  • De Haan S, Rodriguez F (2016) Potato origin and production. In: Singh J, Kaur L (eds) Advances in potato chemistry and technology. Elsevier, London, pp 1–32

    Google Scholar 

  • Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079. https://doi.org/10.1101/gr.132102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du D, Du X, Mattia MR, Wang Y, Yu Q, Huang M, Yu Y, Grosser JW, Gmitter FG Jr (2018) LTR retrotransposons from the Citrus x clementina genome: characterization and application. Tree Genet Genomes 14:43. https://doi.org/10.1007/s11295-018-1257-x

    Article  Google Scholar 

  • Esposito S, Aversano R, D’Amelia V, Villano C, Alioto D, Mirouze M, Carputo D (2018) Dicer-like and RNA-dependent RNA polymerase gene family identification and annotation in the cultivated Solanum tuberosum and its wild relative S. commersonii. Planta 248:729–743

    Article  CAS  Google Scholar 

  • Esposito S, Aversano R, Bradeen JM, Di Matteo A, Villano C, Carputo D (2019a) Deep-sequencing of Solanum commersonii smallRNA libraries reveals riboregulators involved in cold stress response. Plant Biol. https://doi.org/10.1111/plb.12955 (In press)

    Article  Google Scholar 

  • Esposito S, D’Amelia V, Carputo D, Aversano R (2019b) Genes involved in stress signals: the CBLs-CIPKs network in cold tolerant Solanum commersonii. Biol Plant. https://doi.org/10.32615/bp.2019.072

  • Gaiero P, Vaio M, Peters SA, Schranz ME, de Jong H, Speranza PR (2018) Comparative analysis of repetitive sequences among species from the potato and the tomato clades. Annals Bot Lond 123:521–532

    Article  Google Scholar 

  • Grandbastien MA (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3:181–187

    Article  Google Scholar 

  • Hackbusch J, Richter K, Müller J, Salamini F, Uhrig JF (2005) A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proc Natl Acad Sci USA 102:4908–4912

    Article  CAS  Google Scholar 

  • Jaillon O, Aury JM, Benjamin N (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  Google Scholar 

  • Jiang N, Visa S, Wu S, Van Der Knaap E (2012) Rider transposon insertion and phenotypic change in tomato. In: Grandbastien MA, Casacuberta JM (eds) Plant Transposable Elements, Topics in Current Genetics, Heidelberg. Springer-Verlag, Berlin, pp 297–312

  • Lanciano S, Carpentier MC, Llauro C, Jobet E, Robakowska-Hyzorek D, Lasserre E, Ghesquière A, Panaud O, Mirouze M (2017) Sequencing the extrachromosomal circular mobilome reveals retrotransposon activity in plants. PLoS Genet 13:e1006630

    Article  Google Scholar 

  • Leisner CP, Hamilton JP, Crisovan E, Manrique-Carpintero NC, Marand AP, Newton L, Pham GM, Jiang J, Douches DS, Jansky SH, Buell CR (2018) Genome sequence of M6, a diploid inbred clone of the high glycoalkaloid-producing tuber-bearing potato species Solanum chacoense, reveals residual heterozygosity. Plant J 94:562–570

    Article  CAS  Google Scholar 

  • Ma JX, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869

    Article  CAS  Google Scholar 

  • Novák P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform 11:378

    Article  Google Scholar 

  • Paz RC, Kozaczek ME, Rosli HG, Andino NP, Sánchez-Puerta MV (2017) Diversity, distribution and dynamics of full-length Copia and Gypsy LTR retroelements in Solanum lycopersicum. Genetica 145:417–430

    Article  CAS  Google Scholar 

  • Piegu B, Guyot R, Picault N, Roulin A, Sanyal A, Kim H, 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

    Article  CAS  Google Scholar 

  • Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195

    Article  Google Scholar 

  • Potter SC, Luciani A, Eddy SR, Park YM, Lopez R, Finn RD (2018) HMMER web server: 2018 update. Nucleic Acids Res 46:W200–W204

    Article  CAS  Google Scholar 

  • Qiu F, Ungerer MC (2018) Genomic abundance and transcriptional activity of diverse gypsy and copia long terminal repeat retrotransposons in three wild sunflower species. BMC Plant Biol 18:6

    Article  Google Scholar 

  • SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45

    Article  CAS  Google Scholar 

  • Strand D, Mcdonald JF (1985) Copia is transcriptionally responsive to environmental stress. Nucl Acids Res 13:4401–4410

    Article  CAS  Google Scholar 

  • Tittel-Elmer M, Bucher E, Broger L, Mathieu O, Paszkowski J, Vaillant I (2010) Stress-induced activation of heterochromatic transcription. PLoS Genet 6:e1001175. https://doi.org/10.1371/journal.pgen.1001175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van der Knaap E, Chakrabarti M, Hsuan Chu Y, Clevenger JP, Illa-Berenguer E, Huang Z, Keyhaninejad N, Mu Q, Sun L, Wang Y, Wu S (2014) What lies beyond the eye: the molecular mechanisms regulating tomato fruit weight and shape. Front Plant Sci 5:227

    PubMed  PubMed Central  Google Scholar 

  • Vicient CM, Suoniemi A, Anamthawat-Jónsson K, Tanskanen J, Beharav A, Nevo E, Schulman AH (1999) Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11:1769–1784

    Article  CAS  Google Scholar 

  • Vitte C, Panaud O, Quesneville H (2007) LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genom 8:218

    Article  Google Scholar 

  • Wang Y, Tang X, Cheng Z, Mueller L, Giovannoni J, Tanksley SD (2006) Euchromatin and pericentromeric heterochromatin: comparative composition in the tomato genome. Genetics 172:2529–2540

    Article  CAS  Google Scholar 

  • Wicker T, Gundlach H, Spannagl M, Uauy C, Borrill P, Ramírez-González RH, Oliveira RD, IWGS C, Mayer KFX, Paux E, Choulet F (2018) Impact of transposable elements on genome structure and evolution in bread wheat. Genome Biol 19:103

    Article  Google Scholar 

Download references

Acknowledgements

This work was carried out within the project “Development of potato genetic resources for sustainable agriculture” (PORES) funded by the University of Naples Federico II (Project ID: E76J17000010001). We are grateful to Mr. Raffaele Garramone for his technical assistance. No conflict of interest declared.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Domenico Carputo or Riccardo Aversano.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Esposito, S., Barteri, F., Casacuberta, J. et al. LTR-TEs abundance, timing and mobility in Solanum commersonii and S. tuberosum genomes following cold-stress conditions . Planta 250, 1781–1787 (2019). https://doi.org/10.1007/s00425-019-03283-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-019-03283-3

Keywords

Navigation