Skip to main content

Advertisement

Log in

MicroRNA expression profiles in conventional and micropropagated strawberry (Fragaria × ananassa Duch.) plants

  • Cell Biology and Morphogenesis
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are a class of small non-coding RNAs which play a critical role in plant growth and development. To detect strawberry miRNAs and discover the expression difference between conventional and micropropagated strawberry plants, we carried out the detection and quantification of strawberry miRNAs by microarray. The main findings were that 74 miRNAs were checked in strawberry plants and four miRNA genes displayed clear expression difference between conventional and micropropagated strawberry plants, including two up-regulated genes (miR535 and miR390) and two down-regulated genes (miR169a and miR169d). The ratios of conventionally propagated strawberry plant/micropropagated strawberry plant for miR535, miR390, miR169a and miR169d were 2.6884, 2.2673, 0.2496 and 0.3814, respectively. Quantitative reverse transcription polymerase chain reaction applied to the two up-regulated genes (miR535 and miR390) validated the microarray result. This is the first report on differential expression of miRNAs in conventional and micropropagated plants.

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

Similar content being viewed by others

Abbreviations

IBA:

Indole-3-butyric acid

RT:

Reverse transcription

PCR:

Polymerase chain reaction

RT-PCR:

Reverse transcription-polymerase chain reaction

Q-RT-PCR:

Quantitative-reverse transcription-polymerase chain reaction

cDNA:

Complementary deoxyribonucleic acid

References

  • Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131(14):3357–3365

    Article  CAS  PubMed  Google Scholar 

  • Adai A, Johnson C, Mlotshwa S, Archer-Evans S, Manocha V, Vance V, Sundaresan V (2005) Computational prediction of miRNAs in Arabidopsis thaliana. Genome Res 15:78–91

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Agostino SD, Strano S, Emiliozzi V, Zerbini V, Mottolese M, Sacchi A, Blandino G, Piaggio G (2006) Gain of function of mutant p53: the mutant p53/NF-Y protein complex reveals an aberrant transcriptional mechanism of cell cycle regulation. Cancer Cell 10:191–202

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Arazi T, Talmor-Neiman M, Stav R, Riese M, Huijser P, Baulcombe DC (2005) Cloning and characterization of micro-RNAs from moss. Plant J 43:837–848

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Bao N, Lye KW, Barton MK (2004) MicroRNA binding sites in Arabidopsis class Ш HD-ZIP mRNAs are required for methylation of the template chromosome. Dev Cell 7:653–662

    Article  CAS  PubMed  Google Scholar 

  • Barakat A, Wall K, Leebens-Mack J, Wang YJ, Carlson JE, dePamphilis CW (2007) Large-scale identification of microRNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. Plant J 51:991–1003

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  CAS  PubMed  Google Scholar 

  • Baskerville S, Bartel DP (2005) Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11:241–247

    Article  CAS  PubMed  Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharya A, Deng JM, Zhang Z, Behringer R, de Crombrugghe B, Maity SN (2003) The B subunit of the CCAAT box binding transcription factor complex (CBF/NF-Y) is essential for early mouse development and cell proliferation. Cancer Res 63:8167–8172

    CAS  PubMed  Google Scholar 

  • Billoud B, de Paepe R, Baulcombe D, Boccara M (2005) Identification of new small non-coding RNAs from tobacco and Arabidopsis. Biochimie 87:905–910

    Article  CAS  PubMed  Google Scholar 

  • Bonnet E, Wuyts J, Rouzé P, Van de Peer Y (2004) Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc Natl Acad Sci USA 101:11511–11516

    Article  CAS  PubMed  Google Scholar 

  • Boxus P (1974) The production of strawberry plants by in vitro micropropagation. J Hort Sci 49:209–210

    CAS  Google Scholar 

  • Brainerd KE, Fuchigami LH (1982) Stomatal functioning of in vitro and greenhouse apple leaves in darkness, mannitol, ABA and CO2. J Exp Bot 33:388–392

    Article  CAS  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    Article  CAS  PubMed  Google Scholar 

  • Cassells AC, Curry RF (2001) Oxidative stress and physiological, epigenetic and genetic variability in plant tissue culture: implications for micropropagators and genetic engineers. Plant Cell Tissue Organ Cult 64(2–3):145–157

    Article  CAS  Google Scholar 

  • Chang L, Zhang Z, Yang H, Li H, Dai H (2007) Detection of strawberry RNA and DNA viruses by RT-PCR using total nucleic acid as a template. J Phytopathol 155:431–436

    Article  CAS  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    Article  CAS  PubMed  Google Scholar 

  • Chen CF, Ridzon DA, Broomer AJ, Zhou ZH, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:179–187

    Article  Google Scholar 

  • Combier JP, Frugier F, de Billy F, Boualem A, EI-Yahyaoui F, Moreau S, Vernié T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2–1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20(22):3084–3088

    Article  CAS  PubMed  Google Scholar 

  • Cubas P, Coen E, Zapater JMM (2001) Ancient asymmetries in the evolution of flowers. Curr Biol 11:1050–1052

    Article  CAS  PubMed  Google Scholar 

  • Dai H, Zhang Z, Guo X (2007) Adventitious bud regeneration from leaf and cotyledon explants of Chinese hawthorn (Crataegus pinnatifida Bge. var. major N.E.Br.). In Vitro Cell Dev Biol Plant 43:2–8

    CAS  Google Scholar 

  • Dezulian T, Palatnik JF, Huson D, Weigel D (2005) Conservation and divergence of microRNA families in plants. Genome Biol 6:13

    Article  Google Scholar 

  • Eisen MB, Brown PO (1999) DNA arrays for analysis of gene expression. Methods Enzymol 303:179–205

    Article  CAS  PubMed  Google Scholar 

  • Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class Ш HD-ZIP and KANADI genes. Curr Biol 13:1768–1774

    Article  CAS  PubMed  Google Scholar 

  • Fahlgren N, Montgomery T, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16(9):939–944

    Article  CAS  PubMed  Google Scholar 

  • Floyd SK, Bowman JL (2004) Gene regulation: ancient microRNA target sequences in plants. Nature 428:485–486

    Article  CAS  PubMed  Google Scholar 

  • Garcia D, Collier SA, Byrne ME, Martienssen RA (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16:933–938

    Article  CAS  PubMed  Google Scholar 

  • Garzon R, Pichiorri F, Palumbo T, Iuliano R, Cimmino A, Aqeilan R, Volinia S, Bhatt D, Alder H, Marcucci G, Calin GA, Liu CG, Bloomfield CD, Andreeff M, Croce CM (2006) MicroRNA fingerprints during human megakaryocytopoiesis. Proc Natl Acad Sci USA 103(13):5078–5083

    Article  CAS  PubMed  Google Scholar 

  • Griffiths-Jones S (2004) The microRNA registry. Nucleic Acids Res 32:D109–D111

    Article  CAS  PubMed  Google Scholar 

  • Guo X, Gui Y, Wang Y, Zhu QH, Helliwell C, Fan L (2008) Selection and mutation on microRNA target sequences during rice evolution. BMC Genomics 9:454

    Article  PubMed  Google Scholar 

  • Jaligot E, Rival A, Beulé T, Dussert S, Verdeil JL (2000) Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis. Plant Cell Rep 19(7):684–690

    Article  CAS  Google Scholar 

  • Jemmali A, Boxus P, Dekegel D, Heule GV (1994) Occurrence of spontaneous shoot regeneration on leaf stipules in relation to hyperflowering response in micropropagated strawberry plantlets. In Vitro Cell Dev Biol 30p:192–195

    Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    Article  CAS  PubMed  Google Scholar 

  • Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MCP (2004) MicroRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88

    Article  CAS  PubMed  Google Scholar 

  • Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–188

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Jung JH, Reyes JL, Kim YS, Kim SY, Chung KS, Kim JA, Lee M, Lee Y, Kim VN, Chua NH, Park CM (2005) MicorRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J 42(1):84–94

    Article  CAS  PubMed  Google Scholar 

  • Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, Harada JJ (2003) LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15:5–18

    Article  CAS  PubMed  Google Scholar 

  • Laufs P, Peaucelle A, Morin H, Traas J (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131:4311–4322

    Article  CAS  PubMed  Google Scholar 

  • Lauter N, Kampani A, Carlson S, Goebel M, Moose SP (2005) MicroRNA 172 down-regulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci USA 102:9412–9417

    Article  CAS  PubMed  Google Scholar 

  • Lee H, Fischer RL, Goldberg RB, Harada JJ (2003) Arabidopsis LEAFY COTYLEDON1 represents a functionally specialized subunit of the CCAAT binding transcription factor. Proc Natl Acad Sci USA 100:2152–2156

    Article  CAS  PubMed  Google Scholar 

  • Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251

    Article  CAS  PubMed  Google Scholar 

  • Litwińczuk W (2004) Field performance of ‘Senga Sengana’ strawberry plants (Fragaria × ananassa Duch.) obtained by runners and in vitro through axillary and adventitious shoots. Electronic Journal of Polish Agricultural Universities, Horticulture 7(1): art–03

  • Liu B, Wendel JF (2003) Epigenetic phenomena and the evolution of plant allopolyploids. Mol Phylogenet Evol 29:365–379

    Article  CAS  PubMed  Google Scholar 

  • Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843

    Article  CAS  PubMed  Google Scholar 

  • Lotan T, Ohto M, Yee KM, West MA, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Luo MY, Tian ZG, Xu Z, Zhang L, Wang YX, Cheng J (2007) Construction and application of a microarray for profiling microRNA expression. Prog Biochem Biophys 34(1):31–41

    CAS  Google Scholar 

  • Mallory AC, Bartel DP, Bartel B (2005) MciroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375

    Article  CAS  PubMed  Google Scholar 

  • McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713

    Article  CAS  PubMed  Google Scholar 

  • McHale NA, Koning RE (2004) MicroRNA-directed cleavage of Nicotiana sylvestris PHAVLOUTA mRNA regulates the vascular cambium and structure of apical meristems. Plant Cell 16:1730–1740

    Article  CAS  PubMed  Google Scholar 

  • Mi JM, Zhang ZH, Li H, Gao XY, Du GD (2007) Blossoming and fruiting of micropropagated strawberry plants after transplantation. J Fruit Sci 24(4):472–476

    Google Scholar 

  • Millar AA, Gubler F (2005) The Arabidopsis GAMYB-Like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17:705–721

    Article  CAS  PubMed  Google Scholar 

  • Miyoshi K, Ito Y, Serizawa A, Kurata N (2003) OsHAP3 genes regulate chloroplast biogenesis in rice. Plant J 36:532–540

    Article  CAS  PubMed  Google Scholar 

  • Molnár A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447:1126–1129

    Article  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497

    Article  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  CAS  PubMed  Google Scholar 

  • Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poething RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 102(10):3691–3696

    Article  CAS  PubMed  Google Scholar 

  • Pires JC, Zhao J, Schranz EM, Leon EJ, Quijada PA, Lukens LN, Osborn TC (2004) Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol J Linn Soc Lond 82:675–688

    Article  Google Scholar 

  • Poole R, Barker G, Wilson ID, Coghill JA, Edwards KJ (2007) Measuring global gene expression in polyploidy; a cautionary note from allohexaploid wheat. Funct Integr Genomics 7:207–219

    Article  CAS  PubMed  Google Scholar 

  • Qiu CX, Xie FL, Zhu YY, Guo K, Huang SQ, Nie L, Yang ZM (2007) Computational identification of microRNAs and their targets in Gossypium hirsutum expressed sequence tags. Gene 395:49–61

    Article  CAS  PubMed  Google Scholar 

  • Rapp RA, Wendel JF (2005) Epigenetics and plant evolution. New Phytol 168:81–91

    Article  CAS  PubMed  Google Scholar 

  • Rival A, Jaligot E, Beule T, Finnegan EJ (2008) Isolation and expression analysis of genes encoding MET, CMT and DRM methyltransferases in oil palm (Elaeis guineensis Jacq.) in relation to the ‘mantled’ somaclonal variation. J Exp Bot 1–11

  • Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, Jones PA (2006) Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 9:435–443

    Article  CAS  PubMed  Google Scholar 

  • Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–470

    Article  CAS  PubMed  Google Scholar 

  • Schubert D, Clarenz O, Goodrich J (2005) Epigenetic control of plant development by Polycomb-group proteins. Curr Opin Plant Biol 8:553–561

    Article  CAS  PubMed  Google Scholar 

  • Short KC, Warburton J, Roberts AV (1987) In vitro hardening of cultured cauliflower and chrysanthemum plantlets to humidity. Acta Hortic 212:329–334

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from Rice. Plant Cell 17:1397–1411

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Zhou XF, Zheng Y, Zhang WX, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25

    Article  PubMed  Google Scholar 

  • Talmor-Neiman M, Stav R, Frank W, Voss B, Arazi T (2006a) Novel microRNAs and intermediates of microRNA biogenesis from moss. Plant J 47:25–37

    Article  CAS  PubMed  Google Scholar 

  • Talmor-Neiman M, Stav R, Klipcan L, Buxdorf K, Baulcombe DC, Arazi T (2006b) Identification of trans-acting siRNAs in moss and an RNA-dependent RNA polymerase required for their biogenesis. Plant J 48:511–521

    Article  CAS  PubMed  Google Scholar 

  • Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Gens Dev 17:49–63

    Article  CAS  Google Scholar 

  • Tang F, Hajkova P, Barton SC, Lao K, Surani MA (2006) MicroRNA expression profiling of single whole embryonic stem cells. Nucleic Acids Res 34(2):e9

    Article  PubMed  Google Scholar 

  • Thomson JM, Parker J, Perou CM, Hammond SM (2004) A custom microarray platform for analysis of microRNA gene expression. Nat Methods 1:47–53

    Article  CAS  PubMed  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    Article  CAS  PubMed  Google Scholar 

  • Tuddenham L, Wheeler G, Ntounia-Fousara S, Waters J, Hajihosseini MK, Clark I, Dalmay T (2006) The cartilage specific microRNA-140 targets histone deacetylase 4 in mouse cells. FEBS Lett 580:4214–4217

    Article  CAS  PubMed  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3:12

    Article  PubMed  Google Scholar 

  • Vaucheret H, Vazquez F, Crété P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18:1187–1197

    Article  CAS  PubMed  Google Scholar 

  • Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crété P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16(1):69–79

    Article  CAS  PubMed  Google Scholar 

  • Wang XJ, Reyes JL, Chua NH, Gaasterland T (2004) Prediction and identification of Arabidopsis thaliana microRNAs and their mRNA targets. Genome Biol 5(9):R65

    Article  PubMed  Google Scholar 

  • Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216

    Article  CAS  PubMed  Google Scholar 

  • Warpeha KM, Upadhyay S, Yeh J, Adamiak J, Hawkins SI, Lapik YR, Anderson MB, Kaufman LS (2007) The GCR1, GPA1, PRN1, NF-Y signal chain mediates both blue light and abscisic acid responses in Arabidopsis. Plant Physiol 143:1590–1600

    Article  CAS  PubMed  Google Scholar 

  • Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci USA 102:9703–9708

    Article  CAS  PubMed  Google Scholar 

  • Xie FL, Huang SQ, Guo K, Xiang AL, Zhu YY, Nie L, Yang ZM (2007) Computational identification of novel microRNAs and targets in Brassica napus. FEBS Lett 581:1464–1474

    Article  CAS  PubMed  Google Scholar 

  • Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:e15

    Article  PubMed  Google Scholar 

  • Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8:R96

    Article  PubMed  Google Scholar 

  • Yin Z, Li C, Han X, Shen F (2008) Identification of conserved microRNAs and their target genes in tomato (Lycopersicon esculentum). Gene 414:60–66

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin K (2007a) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590

    Article  CAS  PubMed  Google Scholar 

  • Zhao T, Li GL, Mi SJ, Li S, Hannon GJ, Wang XJ, Qi YJ (2007b) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21:1190–1203

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Ye ZH (2004) Amphivasal vascular bundle 1, a gain of function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stem and carpels. Plant Cell Physiol 45(4):369–385

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by National Natural Science Foundation of China (30671432) and Program for New Century Excellent Talents in University (NCET-07-0565).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhihong Zhang.

Additional information

Communicated by R. Reski.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 128 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, H., Zhang, Z., Huang, F. et al. MicroRNA expression profiles in conventional and micropropagated strawberry (Fragaria × ananassa Duch.) plants. Plant Cell Rep 28, 891–902 (2009). https://doi.org/10.1007/s00299-009-0693-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-009-0693-3

Keywords

Navigation