Skip to main content
Log in

ROSINA (RSI) is part of a CACTA transposable element, TamRSI, and links flower development to transposon activity

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

ROSINA (RSI) was isolated as a DNA binding factor able to bind to the CArG-box present in the promoter of the MADS-box gene DEFICIENS of Antirrhinum majus. The mosaic nature of RSI and its multi-copy presence in the A. majus genome indicated that RSI could be a part of a mobile genetic element. Here we show that RSI is a part of a CACTA transposable element system of A. majus, named TamRSI, which has evolved and is still evolving within the terminal inverted repeats (TIRs) of this CACTA transposon. Interestingly, RSI is always found in opposite orientation with respect to the transcription of a second gene present within the CACTA transposon, which encodes a putative TRANSPOSASE (TNP). This structural configuration has not yet been described for any member of the CACTA transposons superfamily. Internal deletion derivatives of the TamRSI produce aberrant RSI transcripts (RSI-ATs) that carry parts of the RSI RNA fused to parts of the TNP RNA. In addition, an intriguing seed phenotype shown by RNAi transgenic lines generated to silence RSI, relate TamRSI to epigenetic mechanisms and associate the control of flower development to transposon activity.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler JE, White J, Sikkink K, Chandler VL (2006) An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442:295–298

    Article  PubMed  CAS  Google Scholar 

  • Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, Gaasterland T, Meyer J, Tuschl T (2003) The small RNA profile during Drosophila melanogaster development. Dev Cell 5:337–350

    Article  PubMed  CAS  Google Scholar 

  • Bonas U, Sommer H, Saedler H (1984) The 17-Kb Tam-1 element of Antirrhinum majus induces a 3-bp duplication upon integration into the Chalcone Synthase gene. EMBO J 3:1015–1019

    PubMed  CAS  Google Scholar 

  • Bundock P, Hooykaas P (2005) An Arabidopsis hAT-like transposase is essential for plant development. Nature 436:282–284

    Article  PubMed  CAS  Google Scholar 

  • Bureau TE, White SE, Wessler SR (1994) Transduction of a cellular gene by a plant retroelement. Cell 77:479–480

    Article  PubMed  CAS  Google Scholar 

  • Causier B, Castillo R, Zhou JL, Ingram R, Xue YB, Schwarz-Sommer Z, Davies B (2005) Evolution in action: following function in duplicated floral homeotic genes. Curr Biol 15:1508–1512

    Article  PubMed  CAS  Google Scholar 

  • Chan SWL, Zilberman D, Xie ZX, Johansen LK, Carrington JC, Jacobsen SE (2004) RNA silencing genes control de novo DNA methylation. Science 303:1336–1336

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Carpenter R, Martin C (1986) Transposable elements generate novel spatial patterns of gene-expression in Antirrhinum majus. Cell 47:285–296

    Article  PubMed  CAS  Google Scholar 

  • Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603

    Article  PubMed  CAS  Google Scholar 

  • Fedoroff N, Schläppi M, Raina R (1995) Epigenetic regulation of the maize Spm transposon. Bioessays 14:291–297

    Article  Google Scholar 

  • Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    Article  PubMed  CAS  Google Scholar 

  • Fischer A, Baum N, Saedler H, Theissen G (1995) Chromosomal mapping of the MADS-Box multigene family in Zea mays reveals dispersed distribution of allelic genes as well as transposed copies. Nucleic Acids Res 23:1901–1911

    Article  PubMed  CAS  Google Scholar 

  • Gierl A, Lütticke S, Saedler H (1988) TnpA product encoded by the transposable element En-1 of Zea mays is a DNA binding protein. EMBO J 7:4045–4053

    PubMed  CAS  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952

    Article  PubMed  CAS  Google Scholar 

  • Hershberger RJ, Benito MI, Hardeman KJ, Warren C, Chandler VL, Walbot V (1995) Characterization of the major transcripts encoded by the regulatory MuDR transposable element of maize. Genetics 140:1087–1098

    PubMed  CAS  Google Scholar 

  • Hoen DR, Park KC, Elrouby N, Yu ZH, Mohabir N, Cowan RK, Bureau TE (2006) Transposon-mediated expansion and diversification of a family of ULP-like genes. Mol Biol Evol 23:1254–1268

    Article  PubMed  CAS  Google Scholar 

  • Hudson ME, Lisch DR, Quail PH (2003) The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J 34:453–471

    Article  PubMed  CAS  Google Scholar 

  • Jacob F, Monod J (1961) Genetic regulatory mechanisms in synthesis of proteins. J Mol Biol 3:318–356

    Article  PubMed  CAS  Google Scholar 

  • Jin YK, Bennetzen JL (1994) Integration and nonrandom mutation of a plasma-membrane proton ATPase gene fragment within the Bs1 retroelement of maize. Plant Cell 6:1177–1186

    Article  PubMed  CAS  Google Scholar 

  • Juretic N, Hoen DR, Huynh ML, Harrison PM, Bureau TE (2005) The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15:1292–1297

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov VV, Jurka J (2006) Self-synthesizing DNA transposons in eukaryotes. Proc Natl Acad Sci USA 103:4540–4545

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki S, Nitasaka E (2004) Characterization of Tpn1 family in the Japanese morning glory: En/Spm-related transposable elements capturing host genes. Plant Cell Physiol 45:933–944

    Article  PubMed  CAS  Google Scholar 

  • Ketting RF, Haverkamp THA, van Luenen H, Plasterk RHA (1999) mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell 99:133–141

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJ, Koornneef M, Kakutani T (2007) Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J 49:38–45

    Article  PubMed  CAS  Google Scholar 

  • Korneev SA, Park JH, O’Shea M (1999) Neuronal expression of neural nitric oxide synthase (nNOS) protein is suppressed by an antisense RNA transcribed from an NOS pseudogene. J Neurosci 19:7711–7720

    PubMed  CAS  Google Scholar 

  • Kunze R, Weil CF (2002) The hAT and CACTA superfamilies of plant transposon. In: Craig NL, Craigie R, Gellert M, Lambowitz (eds) Mobile DNA II ASM Press, Washington DC, pp 565–610

    Google Scholar 

  • Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476

    Article  PubMed  CAS  Google Scholar 

  • Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619

    Article  PubMed  CAS  Google Scholar 

  • Martienssen RA (2003) Maintenance of heterochromatin by RNA interference of tandem repeats. Nat Genet 35:213–214

    Article  PubMed  CAS  Google Scholar 

  • Martienssen R, Lippman Z, May B, Ronemus M, Vaughn M (2004) Transposons, tandem repeats, and the silencing of imprinted genes. Cold Spring Harb Symp Quant Biol 69:371–379

    Article  PubMed  CAS  Google Scholar 

  • Masson P, Rutherford G, Banks JA, Fedoroff N (1989) Essential large transcripts of the maize Spm transposable element are generated by alternative splicing. Cell 58:755–765

    Article  PubMed  CAS  Google Scholar 

  • Matzke M, Matzke AJ, Kooter JM (2001) RNA: guiding gene silencing. Science 293:1080–1083

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci USA 36:344–355

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1956) Controlling elements and the gene. Cold Spring Harb Symp Quant Biol 16:197–216

    Google Scholar 

  • McClintock B (1965) The control of gene action in maize. Brookhaven Symp Biol 18:162–184

    Google Scholar 

  • Mette MF, van der Winden J, Matzke M, Matzke AJM (2002) Short RNAs can identify new candidate transposable element families in Arabidopsis. Plant Physiol 130:6–9

    Article  PubMed  CAS  Google Scholar 

  • Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002

    Article  PubMed  CAS  Google Scholar 

  • Muehlbauer GJ, Bhau BS, Syed NH, Heinen S, Cho SH, Marshall D, Pateyron S, Buisine N, Chalhoub B, Flavell AJ (2006) A hAT superfamily transposase recruited by the cereal grass genome. Mol Gen Genomics 275:553–563

    Article  CAS  Google Scholar 

  • Nevers P, Saedler H (1977) Transposable Genetic Elements as Agents of Gene Instability and Chromosomal Rearrangements. Nature 268:109–115

    Article  PubMed  CAS  Google Scholar 

  • Pereira A, Cuypers H, Gierl A, Schwarz-Sommer Z, Saedler H (1986) Molecular analysis of the En/Spm transposable element system of Zea mays. EMBO J 5:835–841

    PubMed  CAS  Google Scholar 

  • Roccaro M, Li Y, Masiero S, Saedler H, Sommer H (2005) ROSINA (RSI), a novel protein with DNA-binding capacity, acts during floral organ development in Antirrhinum majus. Plant J 43:238–250

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold spring Laboratory Press, New York

    Google Scholar 

  • Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci 7:487–491

    Google Scholar 

  • Schiefelbein JW, Raboy V, Kim HY, Nelson OE (1988) Molecular characterization of Suppressor-mutator (Spm)-induced mutations at the bronze-1 locus in maize: the bz-m13 alleles. In: Nelson O (ed) Plenum Press, New York

  • Schwarz-Sommer Z, Gierl A, Klösgen RB, Wienand U, Peterson PA, Saedler H (1984) The Spm (En) transposable element controls the excision of a 2-kb DNA insert at the wx-m8 allele of Zea mays. EMBO J 3:1021–1028

    PubMed  CAS  Google Scholar 

  • Schwarz DS, Hutvagner G, Du T, Xu ZS, Aronin N, Zamore PD (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115:199–208

    Article  PubMed  CAS  Google Scholar 

  • Schwarz-Sommer Z, Silva ED, Berndtgen R, Lonnig WE Muller A, Nindl I, Stuber K, Wunder J, Saedler H, Gubitz T, Borking A, Golz JF, Ritter E, Hudson A (2003) A linkage map of an F-2 hybrid population of Antirrhinum majus and A. molle. Genetics 163:699–710

    PubMed  CAS  Google Scholar 

  • Sijen T, Plasterk RHA (2003) Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 426:310–314

    Article  PubMed  CAS  Google Scholar 

  • Sommer H, Bonas U, Saedler H (1988) Transposon-induced alterations in the promoter region affect transcription of the chalcone synthase gene of Antirrhinum majus. Mol Gen Genet 211:49–55

    Article  PubMed  CAS  Google Scholar 

  • Soppe WJJ, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef M, Peeters AJM (2000) The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 6:791–802

    Article  PubMed  CAS  Google Scholar 

  • Spielman M, Vinkenoog R, Dickinson HG, Scott RJ (2001) The epigenetic basis of gender in flowering plants and mammals. Trends Genet 17:705–711

    Article  PubMed  CAS  Google Scholar 

  • Spillane C, Baroux C, Escobar-Restrepo JM, Page DR, Laoueille S, Grossniklaus U (2004) Transposons and tandem repeats are not involved in the control of genomic imprinting at the MEDEA locus in Arabidopsis. Cold Spring Harb Symp Quant Biol 69:465–475

    Article  PubMed  CAS  Google Scholar 

  • Tabara H, Sarkissian M, Kelly WG, Fleenor J, Grishok A, Timmons L, Fire A, Mello CC (1999) The rde-1 gene, RNA interference, and transposon silencing in C elegans. Cell 99:123–132

    Article  PubMed  CAS  Google Scholar 

  • Talbert LE, Chandler VL (1988) Characterization of a highly conserved sequence related to Mutator transposable elements in maize. Mol Biol Evol 5:519–529

    PubMed  CAS  Google Scholar 

  • Tijsterman M, Ketting RF, Plasterk RHA (2002) The genetics of RNA silencing. Annu Rev Genet 36:489–519

    Article  PubMed  CAS  Google Scholar 

  • Trentmann SM, Saedler H, Gierl A (1993) The transposable element En/Spm-encoded TNPA proteins contains a DNA binding and a dimerization domain. Mol Gen Genet 238:201–208

    PubMed  CAS  Google Scholar 

  • Volpe TA, Kidner C, Hall IM, Teng G, Grewal SIS, Martienssen RA (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833–1837

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson M, Silva ED, Zachgo S, Saedler H Schwarz-Sommer Z (2000) CHORIPETALA and DESPENTEADO: general regulators during plant development and potential floral targets of FIMBRIATA-mediated degradation. Development 127:3725–3734

    PubMed  CAS  Google Scholar 

  • Xiao WY, Gehring M, Choi Y, Margossian L, Pu H, Harada JJ, Goldberg RB, Pennell RI, Fischer RL (2003) Imprinting of the MEA polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell 5:891–901

    Article  PubMed  CAS  Google Scholar 

  • Xie ZX, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:642–652

    Article  CAS  Google Scholar 

  • Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101:25–33

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Z. Schwarz-Sommer for the inbred lines investigated in this project and for the A. majus X A. molle F2 DNA samples to map some of the TamRSI copies. We also thank T. Colby, C. Micali and M. Humphry for editing the manuscript. M.R was supported by the SFB project 572; Y. L. was supported by a Max-Planck Fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mario Roccaro.

Additional information

Communicated by M.-A. Grandbastien.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Suppl. Figure 1.

The RSI sequence is conserved within the Antirrhinum family. Genomic DNA samples from different Antirrhinum species and closely related species as well as some representative plant species were digested with EcoRI endonuclease and subjected to Southern blot hybridization with the full length RSI cDNA used as a probe at low stringent conditions. Only members of the Antirrhinum family and Misopates orontium showed multiple hybridizing bands, whereas all the other species regardless of the phylogenetic distance did not. The plant species are indicated above each lane. The left black bars indicate the DNA markers with the corresponding size values (PDF 1.48 mb)

Suppl. Figure 2.

Southern blot hybridization of segregating individual F2 plants of the lines 165E and desp-1 (A and B), and of the lines 165E and desp-2 (C) to show the polymorphic fragments detected using RSI-2 and RSI-3 flanking sequences as probes. In panels A and B, the digested genomic DNAs were hybridized with the 5’ and the 3’ flanking sequences of RSI-2 (probe 1 and probe 2) respectively. Similarly, the 5’ flanking sequence of RSI-3 (probe3) was used to detect the polymorphism between 165E and desp-2 (C). The sizes of the polymorphic bands and the restriction endonucleases used are indicated. E: line 165E; d1 and d2: two alleles of despenteado (PDF 399 kb)

Suppl. Figure 3.

Schematic representation of the partial TamRSI-2 structure in the 165E line compared to desp1. The TamRSI-2 structure carries a Tam3 insertion within the TIRs as well as a Mu-like element inserted at about 350 bp to the right CACTA TIR not present in the desp1 line. A duplicated gene indicated as “Gene A” is also observed. In the opulentiflora (opu) line an instable Tam4 insertion was also detected. This structure is not complete as indicated by the two slash lines and is not drawn in scale. The two probes derived from flanking sequences and used to detect the polymorphisms shown in supplementary Figure 2 (A and B) are also indicated (PDF 180 kb)

Suppl. Figure 4.

Detection of TamRSI-3 transposition. Genomic DNA from four pools with each pool containing fifty-six 165E plants (samples 1, 2, 3 and 4) was used together with a “positive control” represented by desp-2 (sample 5; desp-2 does not carry TamRSI-3 at the investigated locus) in a nested PCR. 5 μl PCR reaction of the last primer combination (pr9/pr11) were loaded on 0.7% agarose gel and hybridised with 5’ end flaking TamRSI-3 region, as depicted. At least two strongly hybridising products were detected. A 4.0 kb band similar to the size of the desp-2 PCR product (lane 4) and a 2 kb band (lane 1), which indicates a deletion derivative of TamRSI-3. A weaker hybridising PCR product with a size bigger than 4 kb is also detected (lane 2) (PDF 591 kb)

Suppl. Figure 5.

Southern blot hybridization to detect additional deletion variants of TamRSI. A PCR amplification performed on genomic DNA from different lines yielded several products of different length. The PCR products were size-separated on two parallel agarose gels, blotted on nylon membrane and hybridized with TNP (A) and RSI (B) specific probes, respectively. Several hybridizing bands of the same size were detected. The amplified genomic fragments of 2.8 kb correspond to the TamRSI-3 copy. Note the absence of this fragment from sample 12 for both probes corresponding to desp-2 line. Plant lines: 1: 165E; 2: Sippe 50; 3: line T-53; 4: Pallida-recurens; 5: Line 91; 6: deficiens-chloranta; 7: deficiens-globifera; 8: opulentiflora; 9: pleiocotiledona; 10: graminifolia; 11: despenteado-1; 12: despenteado-2; 13: despenteado-4; 14: cycloidea-25 (PDF 840 kb)

Suppl. Figure 6.

Seed capsule of the 165E and RNAi-1b lines. The four pores necessary for seed dispersal are fully opened (black arrows) in 165E line but not in the RNAi-1b line. The same phenotype is observed in the RNAi-1a line (PDF 960 kb)

Suppl. Table 1.

List of the primers (PDF 52.6 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Roccaro, M., Li, Y., Sommer, H. et al. ROSINA (RSI) is part of a CACTA transposable element, TamRSI, and links flower development to transposon activity. Mol Genet Genomics 278, 243–254 (2007). https://doi.org/10.1007/s00438-007-0245-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-007-0245-x

Keywords

Navigation