Skip to main content
Log in

Identification of novel small RNAs in tomato (Solanum lycopersicum)

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

To date, the majority of plant small RNAs (sRNA) have been identified in rice, poplar and Arabidopsis. To identify novel tomato sRNAs potentially involved in tomato specific processes such as fruit development and/or ripening, we cloned 4,018 sRNAs from tomato fruit tissue at the mature green stage. From this pool of sRNAs, we detected tomato homologues of nine known miRNAs, including miR482; a poplar miRNA not conserved in Arabidopsis or rice. We identified three novel putative miRNAs with flanking sequence that could be folded into a stem-loop precursor structure and which accumulated as 19-24nt RNA. One of these putative miRNAs (Put-miRNA3) exhibited significantly higher expression in fruit compared with leaf tissues, indicating a specific role in fruit development processes. We also identified nine sRNAs that accumulated as 19–24nt RNA species in tomato but genome sequence was not available for these loci. None of the nine sRNAs or three putative miRNAs possessed a homologue in Arabidopsis that had a precursor with a predicted stem-loop structure or that accumulated as a sRNA species, suggesting that the 12 sRNAs we have identified in tomato may have a species specific role in this model fruit species.

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

Similar content being viewed by others

Abbreviations

AGO:

ARGONAaUT

BAC:

Bacterial artificial chromosome

DAP:

Days after pollination

DCL:

DICER LIKE

dsRNA:

Double stranded RNA

EST:

Expressed sequence tag

nat-siRNAs:

Natural antisense siRNAs

nt:

Nucleotide

MFE:

Minimum free energy

MiRNA:

microRNA

put-miRNA:

Putative microRNA

RISC:

RNA induced silencing complex

RDR:

RNA dependent RNA polymerase

rRNA:

Ribosomal RNA

siRNA:

Small interfering RNA

sRNA:

Small RNA

tRNA:

Transfer RNA

ta-siRNA:

Trans-acting small interfering RNA

TSD:

Tomato sequence database

References

  • Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouche N, Gasciolli V, Vaucheret H (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16:927–932

    Article  PubMed  CAS  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36:1282–1290

    Article  PubMed  CAS  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    Article  PubMed  CAS  Google Scholar 

  • Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T (2003) A uniform system for microRNA annotation. RNA 9:277–279

    Article  PubMed  CAS  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17:1658–1673

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Jan C, Rajagopalan R, Bartel DP (2006) A two-hit trigger for siRNA biogenesis in plants. Cell 127:565–577

    Article  PubMed  CAS  Google Scholar 

  • Baker CC, Sieber P, Wellmer F, Meyerowitz EM (2005) The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Curr Biol 15:303–315

    Article  PubMed  CAS  Google Scholar 

  • Bonnet E, Wuyts J, Rouze P, Van de Peer Y (2004) Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences. Bioinformatics 20:2911–2917

    Article  PubMed  CAS  Google Scholar 

  • Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291

    Article  PubMed  CAS  Google Scholar 

  • Carbone F, Pizzichini D, Giuliano G, Rosati C, Perrotta G (2005) Comparative profiling of tomato fruits and leaves evidences a complex modulation of global transcript profiles. Plant Sci 169:165–175

    Article  CAS  Google Scholar 

  • Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J Exp Bot 57:1883–1897

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cochrane G, Aldebert P, Althorpe N, Andersson M, Baker W, Baldwin A, Bates K, Bhattacharyya S, Browne P, van den Broek A, Castro M, Duggan K, Eberhardt R, Faruque N, Gamble J, Kanz C, Kulikova T, Lee C, Leinonen R, Lin Q, Lombard V, Lopez R, McHale M, McWilliam H, Mukherjee G, Nardone F, Pastor MP, Sobhany S, Stoehr P, Tzouvara K, Vaughan R, Wu D, Zhu W, Apweiler R (2006) EMBL nucleotide sequence database: developments in 2005. Nucleic Acids Res 34:D10–D15

    Article  PubMed  CAS  Google Scholar 

  • Dalmay T, Rubino L, Burgyan J, Kollar A, Russo M (1993) Functional analysis of cymbidium ringspot virus genome. Virology 194:697–704

    Article  PubMed  CAS  Google Scholar 

  • Fei Z, Tang X, Alba RM, White JA, Ronning CM, Martin GB, Tanksley SD, Giovannoni JJ (2004) Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. Plant J 40:47–59

    Article  PubMed  Google Scholar 

  • Gasciolli V, Mallory AC, Bartel DP, Vaucheret H (2005) Partially redundant functions of Arabidopsis DICERlike enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol 15:1494–1500

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:S170-S180

    Article  PubMed  CAS  Google Scholar 

  • Herr AJ (2005) Pathways through the small RNA world of plants. FEBS Lett 579:5879–5888

    Article  PubMed  CAS  Google Scholar 

  • Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31:3429–3431

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  PubMed  CAS  Google Scholar 

  • Kidner CA, Martienssen RA (2005) The developmental role of microRNA in plants. Curr Opin Plant Biol 8:38–44

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Llave C, Xie Z, Kasschau KD, Carrington JC (2002b) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    Article  CAS  Google Scholar 

  • Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005a) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203

    Article  CAS  Google Scholar 

  • Lu C, Tej SS, Luo S, Haudenschild CD, Meyers BC, Green PJ (2005b) Elucidation of the small RNA component of the transcriptome. Science 309:1567–1569

    Article  CAS  Google Scholar 

  • Lu C, Kulkarni K, Souret FF, MuthuValliappan R, Tej SS, Poethig RS, Henderson IR, Jacobsen SE, Wang W, Green PJ, Meyers BC (2006) MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res 16:1276–1288

    Article  PubMed  CAS  Google Scholar 

  • Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–52

    Article  PubMed  CAS  Google Scholar 

  • Mueller LA, Solow TH, Taylor N, Skwarecki B, Buels R, Binns J, Lin C, Wright MH, Ahrens R, Wang Y, Herbst EV, Keyder ER, Menda N, Zamir D, Tanksley SD (2005) The SOL genomics network: a comparative resource for Solanaceae biology and beyond. Plant Physiol 138:1310–1317

    Article  PubMed  CAS  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  PubMed  CAS  Google Scholar 

  • Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    Article  PubMed  CAS  Google Scholar 

  • Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNA in Arabidopsis. Genes Dev 18:2368–2379

    Article  PubMed  CAS  Google Scholar 

  • Pontes O, Fei Li C, Costa Nunes P, Haag J, Ream T, Vitins A, Jacobsen SE, Pikaard CS (2006) The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing centre. Cell 126:79–92

    Article  PubMed  CAS  Google Scholar 

  • Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425

    Article  PubMed  CAS  Google Scholar 

  • Rathjen T, Nicol C, McConkey G, Dalmay T (2006) Analysis of small RNAs in the malaria parasite and its red blood cell host. FEBS Lett 580:5185–5188

    Article  PubMed  CAS  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    Article  PubMed  CAS  Google Scholar 

  • Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M, Miller N, Mueller LA, Mundodi S, Reiser L, Tacklind J, Weems DC, Wu Y, Xu I, Yoo D, Yoon J, Zhang P (2003) The Arabidopsis information resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 31:224–228

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019

    Article  PubMed  CAS  Google Scholar 

  • Van der Hoeven R, Ronning C, Giovannoni J, Martin G, Tanksley S (2002) Deductions about the number, organization, and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencing. Plant Cell 14:1441–1456

    Article  PubMed  Google Scholar 

  • Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crete P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16:69–79

    Article  PubMed  CAS  Google Scholar 

  • Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296:343–346

    Article  PubMed  CAS  Google Scholar 

  • Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132:3657–3668

    Article  PubMed  CAS  Google Scholar 

  • Xie Z, 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:E104

    Article  PubMed  Google Scholar 

  • Xie Z, Allen E, Wilken A, Carrington JC (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:12984–12989

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa M, Peragine A, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46:243–259

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Peter Walley (Warwick-HRI, UK) for providing RNA extracted from pericarp of Ailsa Craig tomato fruits. This work was funded by the BBSRC (BB/E006981/1 and BB/E004091/1).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tamas Dalmay.

Electronic supplementary material

Below is the link to the electronic supplementary material.

425_2007_518_MOESM1_ESM.xls

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pilcher, R.L.R., Moxon, S., Pakseresht, N. et al. Identification of novel small RNAs in tomato (Solanum lycopersicum). Planta 226, 709–717 (2007). https://doi.org/10.1007/s00425-007-0518-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-007-0518-y

Keywords

Navigation