Skip to main content
SpringerLink
Log in

Repetitive sequences in Eragrostis curvula cDNA EST libraries obtained from genotypes with different ploidy

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

Eragrostis curvula (Schrad) Nees (weeping lovegrass) represents important cultivated forage in semiarid regions, and the most useful cultivars are tetraploid and reproduce by pseudogamous diplosporous apomixis. We previously produced a series of genetically related E. curvula lines that provide a suitable system for the identification of gene(s) involved in diplosporous apomixis and ploidy, including a natural apomictic tetraploid (T), a diploid sexual line (D), and a tetraploid sexual plant (C). A collection of expressed sequence tags (ESTs) was generated from cDNA libraries obtained from panicles of the D, T, and C, and leaves of the T. The present study aimed to analyze the repetitive content of these four cDNA libraries and further identify and characterize transposable element (TE)-related ESTs. Repetitive sequences were identified through the interface RepeatMasker (RM) using the database Repbase Update and further classification of TEs was performed manually from the RM output. The different contribution of ESTs with identity to TEs among libraries was further evaluated, and such differences were validated through RT-qPCR. We found that the percentage of repetitive content in the leaf cDNA library was almost double than in inflorescence libraries, with retrotransposons contributing mostly in all libraries. The expression of TE-related ESTs was compared in cDNA samples extracted from D, T, and C leaves or inflorescences revealing that seven mRNAs containing MuDR-like DNA transposons, Gypsy-like, and Copia-like retrotransposons were differentially represented according to tissue, reproductive mode, or ploidy. The euploid series of Eragrostis curvula is a useful model to the study of epigenomic changes produced after changes in ploidy. The present work constitutes the first detailed report on repetitive sequences of Eragrostis curvula at the transcriptome level.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

C:

tetraploid sexual plant

D:

diploid sexual line

EST:

expressed sequence tag

LTR:

long terminal repeat

RM:

repeat masker

SINE:

short interspersed nuclear elements

T:

natural apomictic tetraploid plant

TE:

transposable element

References

  • Adams, K.L., Cronn, R.C., Percifield, R., Wendel, J.F.: Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. — Proc. nat. Acad. Sci. USA 100: 4649–4654, 2003.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. — Nature 408: 796–815, 2000.

    Article  Google Scholar 

  • Asker, S.E., Jerling, L.: Apomixis in Plants. — CRC Press, Boca Raton 1992.

    Google Scholar 

  • Barcaccia, G., Albertini, E.: Apomixis in plant reproduction: a novel perspective on an old dilemma. — Plant Reprod. 26; 159–179, 2013.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bedell, J.A., Korf, I., Gish, W.: MaskerAid: a performance enhancement to RepeatMasker. — Bioinformatics 16: 1040–1041, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen, J.L.: The contributions of retroelements to plant genome organization, function and evolution. — Trends Microbiol. 4: 347–353, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Blumenstiel, J.P.: Evolutionary dynamics of transposable elements in a small RNA world. — Trends Genet. 27: 23–31, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Cardone, S., Polci, P., Selva, J.P., Mecchia, M., Pessino, S., Hermann, P., Cambi, V., Voigt, P., Spangenberg, G. Echenique, V.: Novel genotypes of the subtropical grass Eragrostis curvula for the study of apomixis (diplospory). — Euphytica 151: 263–272, 2006.

    Article  CAS  Google Scholar 

  • Cervigni, G.D.L., Paniego, N., Díaz, M., Selva, J.P., Zappacosta, D., Zanazzi, D., Landerreche, I., Martelotto, L., Felitti, S., Pessino, S., Spangenberg, G., Echenique, V.; Expressed sequence tag analysis and development of gene associated markers in a near-isogenic plant system of Eragrostis curvula. — Plant mol. Biol. 67: 1–10, 2008a.

    Article  CAS  PubMed  Google Scholar 

  • Cervigni, G.D.L., Paniego, N., Pessino, S., Selva, J.P., Díaz, M., Spangenberg, G., Echenique, V.: Gene expression in diplosporous and sexual Eragrostis curvula genotypes with differing ploidy levels. — Plant. mol. Biol. 67: 11–23, 2008b.

    Article  CAS  PubMed  Google Scholar 

  • Chandler, V.L., Brendel, V.: The maize genome sequencing project. — Plant Physiol. 130: 1594–1597, 2002.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng, X., Zhang, D., Cheng, Z., Keller, B., Ling, H.Q.: A new family of Ty1-copia_like retrotransposons originated in the tomato genome by a recent horizontal transfer event. — Genetics 181: 1183–1193, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chung, T., Kim, C.S., Nguyen, H.N., Meeley, R.B., Larkins, B.A.: The maize zmsmu2 gene encodes a putative RNAsplicing factor that affects protein synthesis and RNA processing during endosperm development. — Plant Physiol. 144: 821–835, 2007.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chung, T., Wang, D., Kim, C.S., Yadegari, R., Larkins, B.A.; Plant SMU-1 and SMU-2 homologues regulate pre-mRNA splicing and multiple aspects of development. — Plant Physiol. 151: 1498–1512, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Comai, L., Tyagi, A.P., Winter, K., Holmes-Davis, R., Reynolds, S.H., Stevens,.Y, Byers, B.: Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. — Plant Cell 12: 1551–1567, 2000.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Conesa, A., Götzm, S., Garcia-Gomez, J.M., Terol, J., Talon, M., Robles, M.: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. — Bioinformatics 21: 3674–3676, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Crane, C.F.: Classification of apomictic mechanisms. — In; Savidan, Y., Carman, J.G., Dresselhaus, T. (ed.): The Flowering of Apomixis: from Mechanisms to Genetic Engineering. Pp. 24–43. CIMMYT, Mexico 2001.

    Google Scholar 

  • De Araujo, P.G., Rossi, M., De Jesus, E.M., Saccaro, N.L., Kajihara, D., Massa, R., De Felix, J.M., Drummond, R.D., Falco, M.C., Chabregas, S.M., Ulian, E.C., Menossi, M., Van Sluys, M.A.V.: Transcriptionally active transposable elements in recent hybrid sugarcane. — Plant J. 44: 707–717, 2005.

    Article  PubMed  Google Scholar 

  • Diaz, M.L., Garbus, I., Echenique, V.: Allele-specific expression of a weeping lovegrass gene from the lignin biosynthetic pathway, caffeoyl-coenzyme A 3-O-methyltransferase. — Mol. Breed. 26: 627–637, 2010.

    Article  Google Scholar 

  • Duarte Silveira, E., Alves-Ferreira, M., Arrais Guimaraes, L., Rodrigues da Silva, F., Tavares de Campos Carneiro, V.; Selection of reference genes for quantitative real-time PCR expression studies in the apomictic and sexual grass Brachiaria brizantha. — BMC Plant Biol. 9: 84, 2009.

    Article  Google Scholar 

  • Echenique, V., Stamova, B., Wolters, P., Lazo, G., Carollo, L., Dubcovsky, J.: Frequencies of Ty1- Copia and Ty3- Gypsy retroelements within the Triticeae EST databases. — Theor. appl. Genet. 104: 840–844, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Gómez, E., Schulman, A.H., Martínez-Izquierdo, J.A., Vicient, C.M.: Integrase diversity and transcription of the maize retrotransposon Grande. — Genome 49: 558–562, 2006.

    Article  PubMed  Google Scholar 

  • González, L.G., Deyholos, M.K.: Identification, characterization and distribution of transposable elements in the flax (Linum usitatissimum L.) genome. — BMC Genomics 13; 644, 2012.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hirochika, H.: Activation of tobacco retrotransposons during tissue culture. — EMBO J. 12: 2521–2528, 1993.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kashkush, K., Feldman, M., Levy A.: Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. — Genetics 160: 1651–1659, 2002.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kashkush, K., Feldman, M., Levy, A.A.: Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. — Nat. Genet. 33: 102–106, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Kidwell, M.G.: Transposable elements and the evolution of genome size in eukaryotes. — Genetica 115: 49–63, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Krom, N., Recla, J., Ramakrishna, W.: Analysis of genes associated with retrotransposons in the rice genome. — Genetica 134: 297–310, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Li, W.D., Hu, X., Liu, J.K., Jiang, G.M., Li, O., Xing, D.; Chromosome doubling can increase heat tolerance in Lonicera japonica as indicated by chlorophyll fluorescence imaging. — Biol. Plant. 55: 279–284, 2011.

    Article  CAS  Google Scholar 

  • Lisch, D.: How important are transposons for plant evolution? — Nat. Rev. Genet. 14: 49–61, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. — Methods 25: 402–408, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Lockton, S., Gaut, B.S.: The contribution of transposable elements to expressed coding sequence in Arabidopsis thaliana. — J. mol. Evol. 68: 80–89, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Ma, X.-F., Gustafson, J.P.: Genome evolution of allopolyploids; a process of cytological and genetic diploidization. Cytogenet. Genome Res. 109: 236–249, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Martelotto, L.G., Ortiz, J.P.A., Stein, J., Espinoza, F., Quarin, C.L., Pessino, S.C.: A comprehensive analysis of gene expression alterations in a newly synthesized Paspalum notatum autotetraploidy. — Plant Sci. 169: 211–220, 2005.

    Article  CAS  Google Scholar 

  • Mecchia, M.A., Ochogavía, A., Selva, J.P., Laspina, N., Felitti, S., Martelotto, L.G., Spangenberg, G., Echenique, V., Pessino, S.C.: Genome polymorphisms and gene differential expression in a ’back-andforth’ ploidy-altered series of weeping lovegrass (Eragrostis curvula). — J. Plant Physiol. 164: 1051–1061, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Meier, M., Zappacosta, D., Selva, J.P., Pessino, S., Echenique, V.: Evaluation of different methods for assessing the reproductive mode of weeping lovegrass plants, Eragrostis curvula (Schrad.) Nees. — Aust. J. Bot. 59: 253–261, 2011.

    Article  Google Scholar 

  • Messing, J., Bharti, A.K., Karlowski, W.M., Gundlach, H., Kim, H.R., Yu, Y., Wei, F., Fuks, G., Soderlund, C.A., Mayer, K.F., Wing, R.A.: Sequence composition and genome organization of maize. — Proc. nat. Acad. Sci. USA 101: 14349–14354, 2004.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mhiri, C., Morel, J.B., Vernhettes, S., Casacuberta, J.M., Lucas, H., Grandbastien, M.A.: The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. — Plant mol. Biol. 33: 257–266, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Muthukumar, B., Bennetzen, J.L.: Isolation and characterization of genomic and transcribed retrotransposon sequences from sorghum. — Mol. Genet. Genom. 271: 308–316, 2004.

    Article  CAS  Google Scholar 

  • Newcombe, R.G.: Two-sided confidence intervals for the single proportion: comparison of seven methods. — Statistics Medicine 17: 857–872, 1998

    Article  CAS  Google Scholar 

  • Nogler, G.A., Gametophytic apomixis. — In: Johri, B.M. (ed.); Embryology of Angiosperms. Pp. 475–518. Springer-Verlag, Berlin 1984.

    Chapter  Google Scholar 

  • Ochogavia, A.C., Seijo, J.G., Gonzalez, A.M., Podio, M., Duarte Silveira, E., Machado Lacerda, A.L., Tavares de Campos Carneiro, V., Ortiz, J.P., Pessino, S.C.; Characterization of retrotransposon sequences expressed in inflorescences of apomictic and sexual Paspalum notatum plants. — Sex. Plant Reprod. 24: 231–246, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Okada, T., Ito, K., Johnson, S.D., Oelkers, K., Suzuki, G., Houben, A., Mukai, Y., Koltunow, A.M.: Chromosomes carrying meiotic avoidance loci in three apomictic eudicot Hieracium subgenus Pilosella species share structural features with two monocot apomicts. — Plant Physiol. 157; 1327–1341, 2011.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oliver, K.R., McComb, J.A., Greene, W.K.: Transposable elements: powerful contributors to angiosperm evolution and diversity. — Genome Biol. Evol. 5: 1886–1901, 2013.

    Article  PubMed Central  PubMed  Google Scholar 

  • Paterson, A.H., Bowers, J.E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., Haberer, G., Hellsten, U., Mitros, T., Poliakov, A., Schmutz, J., Spannagl, M., Tang, H., Wang, X., Wicker, T., Bharti, A.K., Chapman, J., Feltus, F.A., Gowik, U., Grigoriev, I.V., Lyons, E., Maher, C.A., Martis, M., Narechania, A., Otillar, R.P., Penning, B.W., Salamov, A.A., Wang, Y., Zhang, L., Carpita, N.C., Freeling, M., Gingle, A.R., Hash, C.T., Keller, B., Klein, P., Kresovich, S., McCann, M.C., Ming, R., Peterson, D.G., Mehboob-ur-Rahman, Ware, D., Westhoff, P., Mayer, K.F., Messing, J., Rokhsar, D.S.: The Sorghum bicolor genome and the diversification of grasses. — Nature 457: 551–556, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Picault, N., Chaparro, C., Piegu, B., Stenger, W., Formey, D., Llauro, C., Descombin, J., Sabot, F., Lasserre, E., Meynard, D., Guiderdoni, E., Panaud, O.: Identification of an active LTR retrotransposon in rice. — Plant J. 58: 754–765, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Plohl, M., LuchettI, A., Mestrović, N., Mantovani, B.: Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. — Gene 409: 72–82, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Pouteau, S., Huttner, E., Grandbastien, M.A., Caboche, M.; Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. — EMBO J. 10: 1911–1918, 1991.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Project IRGSP: The map-based sequence of the rice genome. — Nature 436: 793–800, 2005.

    Article  Google Scholar 

  • Quarin, C.L., Espinoza, F., Martínez, E.J., Pessino, S.C., Bovo, O.A.: A rise of ploidy level induces the expression of apomixis in Paspalum notatum. — Sex. Plant Reprod. 13; 243–249, 2001.

    Article  Google Scholar 

  • Rabinowicz, P.D., Bennetzen, J.L.: The maize genome as a model for efficient sequence analysis of large plant genomes. — Curr. Opin. Plant Biol. 9: 146–156, 2006.

    Article  Google Scholar 

  • Ramallo, E., Kalendar, R., Schulman, A.H., Martínez-Izquierdo, J.A.: Reme1, a Copia retrotransposon in melon, is transcriptionally induced by UV light. — Plant mol. Biol. 66; 137–150, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Rebozzio R., Sartor M., Quarin C., Espinoza F.: Residual sexuality and its seasonal variation in natural apomictic Paspalum notatum. — Biol. Plant. 55: 391–395, 2011.

    Article  CAS  Google Scholar 

  • Rodriguez, M.P., Cervigni, G.D.L., Quarin, C.L. Ortiz, J.P.A.; Frequencies and variation in cytosine methylation patterns in diploid and tetraploid cytotypes of Paspalum notatum. — Biol. Plant. 56: 276–282, 2012.

    Article  CAS  Google Scholar 

  • Saze, H., Kakutani, T.: Differentiation of epigenetic modifications between transposons and genes. — Curr. Opin. Plant Biol. 14: 81–87, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Selva, J.P., Pessino, S., Meier, M., Echenique, V.: Identification of candidate genes related to polyploidy and/or apomixis in Eragrostis curvula. — Amer. J. Plant Sci. 3: 403–416, 2012.

    Article  CAS  Google Scholar 

  • Thomas, C.A., Jr.: The genetic organization of chromosomes. — Annu. Rev. Genet. 5: 237–256, 1971.

    Article  CAS  PubMed  Google Scholar 

  • Ueki, N., Nishii, I.: Idaten is a new cold-inducible transposon of Volvox carteri that can be used for tagging developmentally important genes. — Genetics 180: 1343–1353, 2008.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vicient, C.: Transcriptional activity of transposable elements in maize. — BMC Genomics 11: 601, 2010.

    Article  PubMed Central  PubMed  Google Scholar 

  • Vicient, C.M., Jääskeläinen, M.J., Kalendar, R., Schulman, A.H.: Active retrotransposons are a common feature of grass genomes. — Plant Physiol. 125: 1283–1292, 2001.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vicient, C.M., Schulman, A.H.: Copia-like retrotransposons in the rice genome: few and assorted. — Genome Lett. 1: 35–47, 2002.

    Article  CAS  Google Scholar 

  • Voigt, P., Rethman, N., Poverene, M.: Warm-Season (C4) Grasses. — American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison 2004.

    Google Scholar 

  • Wang, J., Tian, L., Madlung, A., Lee, H.S., Chen, M., Lee, J.J., Watson, B., Kagochi, T., Comai, L., Chen, Z.J.: Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. — Genetics 167: 1961–1973, 2004.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Watson, L., Dallwitz, M.J.: The Grass Genera of the World. — CAB International, Wallingford 1992.

  • Wendel, J.F.: Genome evolution in polyploids. — Plant mol. Biol 42: 225–249, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Wicker, T., Sabot F., Hua-Van, A., Bennetzen, J.L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., Paux, E., San Miguel, P., Schulman, A.H.: A unified classification system for eukaryotic transposable elements. — Nat. Rev. Genet. 8: 973–982, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Zappacosta, D.C., Ochogavía, A.C., Rodrigo, J.M., Romero, J.R., Meier, M.S., Garbus, I., Pessino S.C., Echenique, V.C.: Increased apomixis expression concurrent with genetic and epigenetic variation in a newly synthesized Eragrostis curvula polyploid. — Sci. Rep. 4: 4423, 2014.

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhou, F., Xu. Y.: RepPop: a database for repetitive elements in Populus trichocarpa. — BMC Genomics 10: 14, 2009.

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Centro de Recursos Naturales Renovables de la Zona Semiárida, CONICET, 8000, Bahía Blanca, Argentina

    J. Romero, J. P. Selva, V. Echenique & I. Garbus

  2. Departamento de Biología Bioquímica y Farmacia, Universidad Nacional del Sur, 8000, Bahía Blanca, Argentina

    J. P. Selva

  3. Facultad de Ciencias Agrarias, Universidad Nacional de Rosario, S2125ZAA, Zavalla, Argentina

    S. Pessino

  4. Departamento de Agronomía, Universidad Nacional del Sur, 8000, Bahía Blanca, Argentina

    V. Echenique

  5. Departamento de Ciencias de la Salud, Universidad Nacional del Sur, 8000, Bahía Blanca, Argentina

    I. Garbus

Authors
  1. J. Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. P. Selva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Pessino
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. Echenique
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. I. Garbus
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. Garbus.

Additional information

Acknowledgements: This work was funded by the CONICET (PIP 112-200801-01517 and PIP-112-201101-00767 to V.E), SECyT UNS (PGI 24/A168 to V.E.) and the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, PICT 2013-2029 to I.G.).

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romero, J., Selva, J.P., Pessino, S. et al. Repetitive sequences in Eragrostis curvula cDNA EST libraries obtained from genotypes with different ploidy. Biol Plant 60, 55–67 (2016). https://doi.org/10.1007/s10535-015-0569-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-015-0569-z

Additional key words

Search

Navigation