Skip to main content

Advertisement

SpringerLink
Log in

The advance of tomato disease-related microRNAs

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Tomato is a model plant for studying plant–pathogen interactions. As regulatory factors, microRNAs (miRNAs) have been widely identified and play crucial roles in tomato–pathogen interactions, including host defense and pathogen counter-defense. Here, the review summarizes the discoveries and highlights of miRNAs in tomato diseases. Roles of artificial miRNAs in disease resistance are further discussed. Hence, a better understanding of the contribution of miRNAs in tomato disease will shed light on strategies in enhancing tomato–pathogen resistance.

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

Fig. 1

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  • Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Aukerman M, 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 Central  PubMed  Google Scholar 

  • Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bonnet E, He Y, Billiau K, Van de Peer Y (2010) TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26:1566–1568

    Article  CAS  PubMed  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 

  • Buscaill P, Rivas S (2014) Transcriptional control of plant defence responses. Curr Opin Plant Biol 20:35–46

    Article  CAS  PubMed  Google Scholar 

  • Cara B, Giovannoni JJ (2008) Molecular biology of ethylene during tomato fruit development and maturation. Plant Sci 175:106–113

    Article  CAS  Google Scholar 

  • Chen L, Ren YY, Zhang YY, Xu JC, Zhang ZY, Wang YW (2012) Genome-wide profiling of novel and conserved Populus microRNAs involved in pathogen stress response by deep sequencing. Planta 235:873–883

    Article  CAS  PubMed  Google Scholar 

  • Chuck G, Candela H, Hake S (2009) Big impacts by small RNAs in plant development. Curr Opin Plant Biol 12:81–86

    Article  CAS  PubMed  Google Scholar 

  • Cillo F, Mascia T, Pasciuto MM, Gallitelli D (2009) Differential effects of mild and severe cucumber mosaic virus strains in the perturbation of microRNA-regulated gene expression in tomato map to the 3′ sequence of RNA 2. Mol Plant Microbe Interact 22:1239–1249

    Article  CAS  PubMed  Google Scholar 

  • Cui JJ, Luan YS, Wang WC, Zhai JM (2014) Prediction and validation of potential pathogenic microRNAs involved in Phytophthora infestans infection. Mol Biol Rep 41:1879–1889

    Article  CAS  PubMed  Google Scholar 

  • Dai XB, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:155–159

    Article  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Saber MK, Zhang Z, Usami T, Lievens B, Subbarao KV, Thomma BPHJ (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109:5110–5115

    Article  PubMed Central  PubMed  Google Scholar 

  • de Planell-Saguer M, Rodicio MC (2011) Analytical aspects of microRNA in diagnostics: a review. Anal Chim Acta 699:134–152

    Article  PubMed  Google Scholar 

  • Diermann N, Matousek J, Junge M, Riesner D, Steger G (2010) Characterization of plant miRNAs and small RNAs derived from potato spindle tuber viroid (PSTVd) in infected tomato. Biol Chem 391:1379–1390

    Article  CAS  PubMed  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548

    Article  CAS  PubMed  Google Scholar 

  • Du Z, Chen A, Chen W, Westwood JH, Baulcombe DC, Carr JP (2014) Using a viral vector to reveal the role of microRNA159 in disease symptom induction by a severe strain of cucumber mosaic virus. Plant Physiol 164:1378–1388

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10:71–78

    Article  CAS  PubMed  Google Scholar 

  • Fahlgren N, Carrington JC (2010) miRNA target prediction in plants. Methods Mol Biol 592:51–57

    CAS  PubMed  Google Scholar 

  • Fahlgren N, Bollmann SR, Kasschau KD, Cuperus JT, Press CM, Sullivan CM, Chapman EJ, Hoyer JS, Gilbert KB, Grunwald NJ (2013) Phytophthora have distinct endogenous small RNA populations that include short interfering and microRNAs. PLoS One 8:e77181

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Feng JL, Chen JS (2013) In silico analysis the complementarity of tomato microRNA/microRNA* sequences with cucumber mosaic virus (CMV) genomic RNAs. J Nanosci Nanotechnol 13:4421–4426

    Article  CAS  PubMed  Google Scholar 

  • Feng JL, Wang K, Liu X, Chen SN, Chen JS (2009) The quantification of tomato microRNAs response to viral infection by stem-loop real-time RT-PCR. Gene 437:14–21

    Article  CAS  PubMed  Google Scholar 

  • Feng JL, Liu X, Lai LY, Chen JS (2011) Spatio-temporal expression of miRNAs in tomato tissues upon cucumber mosaic virus and tomato aspermy virus infections. Acta Biochim Biophys Sin 43:258–266

    Article  CAS  PubMed  Google Scholar 

  • Feng JL, Lai LY, Lin RH, Jin CZ, Chen JS (2012) Differential effects of cucumber mosaic virus satellite RNAs in the perturbation of microRNA-regulated gene expression in tomato. Mol Biol Rep 39:775–784

    Article  CAS  PubMed  Google Scholar 

  • Feng JL, Lin RH, Chen JS (2013a) Alteration of tomato microRNAs expression during fruit development upon cucumber mosaic virus and tomato aspermy virus infection. Mol Biol Rep 40:3713–3722

    Article  CAS  PubMed  Google Scholar 

  • Feng JL, Wang YW, Lin RH, Chen JS (2013b) Altered expression of microRNAs and target mRNAs in tomato root and stem tissues upon different viral infection. J Phytopathol 161:107–119

    Article  CAS  Google Scholar 

  • Guo HS, Ding SW (2002) A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J 21:398–407

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo HS, Xie Q, Fei JF (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to down regulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • He HY, He LF, Gu MH (2014) Role of microRNAs in aluminum stress in plants. Plant Cell Rep 33:831–836

    Article  CAS  PubMed  Google Scholar 

  • Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229:1009–1014

    Article  CAS  PubMed  Google Scholar 

  • Jin WB, Wu FL (2015) Characterization of miRNAs associated with Botrytis cinerea infection of tomato leaves. BMC Plant Biol 15:1

    Article  PubMed Central  PubMed  Google Scholar 

  • Jin WB, Wu FL, Xiao L, Liang GW, Zhen YX, Guo ZK, Guo AG (2012) Microarray-based analysis of tomato miRNA regulated by Botrytis cinerea. J Plant Growth Regul 31:38–46

    Article  CAS  Google Scholar 

  • Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    Article  CAS  PubMed  Google Scholar 

  • Lang QL, Zhou XC, Zhang XL, Drabek R, Zuo ZX, Ren YL, Li TB, Chen JS, Gao XL (2011) Microarray-based identification of tomato microRNAs and time course analysis of their response to cucumber mosaic virus infection. J Zhejiang Univ Sci B 12:116–125

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee YS, Lee DY, Cho LH, An G (2014) Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens. Rice 7:31

    Article  Google Scholar 

  • Li L, Xu JZ, Yang DY, Tan XR, Wang HF (2010) Computational approaches for microRNA studies: a review. Mamm Genome 21:1–12

    Article  CAS  PubMed  Google Scholar 

  • Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun HY, Kumar P, Baker B (2012a) MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci USA 109:1790–1795

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li J, Guo GH, Guo WW, Guo GG, Tong D, Ni ZF, Sun QX, Yao YY (2012b) miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biol 12:220

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu N, Wu S, Van Houten J, Wang Y, Ding B, Fei ZJ, Clarke TH, Reed JW, van der Knaap E (2014) Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J Exp Bot 65:2507–2520

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu YZ, Feng Z, Bian LY, Xie H, Liang JS (2011) miR398 regulation in rice of the responses to abiotic and biotic stresses depends on CSD1 and CSD2 expression. Funct Plant Biol 38(1):44–53

    Article  CAS  Google Scholar 

  • Luan YS, Wang WC, Liu P (2014) Identification and functional analysis of novel and conserved microRNAs in tomato. Mol Biol Rep 41:5385–5394

    Article  CAS  PubMed  Google Scholar 

  • Luan YS, Cui J, Zhai JM, Li J, Han L, Meng J (2015) High-throughput sequencing reveals differential expression of miRNAs in tomato inoculated with Phytophthora infestans. Planta. doi:10.1007/s00425-015-2267-7

    PubMed  Google Scholar 

  • Marone D, Russo MA, Laido G, De Leonardis AM, Mastrangelo AM (2013) Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: active guardians in host defense responses. Int J Mol Sci 14:7302–7326

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mathieu J, Yant LJ, Murdter F, Kuttner F, Schmid M (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol 7:e1000148

    Article  PubMed Central  PubMed  Google Scholar 

  • Meng J, Liu D, Sun C, Luan YS (2014a) Prediction of plant pre-microRNAs and their microRNAs in genome-scale sequences using structure-sequence features and support vector machine. BMC Bioinformatics 15:6595

    Google Scholar 

  • Meng J, Shi L, Luan YS (2014b) Plant microRNA-target interaction identification model based on the integration of prediction tools and support vector machine. PLoS One 9:e103181

    Article  PubMed Central  PubMed  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 Central  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Moustafa K, AbuQamar S, Jarrar M, Al-Rajab AJ, Tremouillaux-Guiller J (2014) MAPK cascades and major abiotic stresses. Plant Cell Rep 33:1217–1225

    Article  CAS  PubMed  Google Scholar 

  • Moxon S, Schwach F, Maclean D, Dalmay T, Studholme DJ, Moulton V (2008) A toolkit for analysing large-scale plant small RNA datasets. Bioinformatics 24:2252–2253

    Article  CAS  PubMed  Google Scholar 

  • Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci USA 106:22534–22539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guil-foyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118

    Article  CAS  PubMed  Google Scholar 

  • Naqvi AR, Choudhury NR, Haq QM, Mukherjee SK (2008) MicroRNAs as biomarkers in Tomato Leaf Curl Virus (ToLCV) disease. Nucleic Acids Symp Ser (Oxf) 52:507–508

    Article  CAS  Google Scholar 

  • Naqvi AR, Haq QM, Mukherjee SK (2010) MicroRNA profiling of tomato leaf curl new delhi virus (tolcndv) infected tomato leaves indicates that deregulation of mir159/319 and mir172 might be linked with leaf curl disease. Virol J 7:281

    Article  PubMed Central  PubMed  Google Scholar 

  • Naqvi AR, Choudhury NR, Mukherjee SK, Haq QM (2011) In silico analysis reveals that several tomato microRNA/microRNA* sequences exhibit propensity to bind to tomato leaf curl virus (ToLCV) associated genomes and most of their encoded open reading frames (ORFs). Plant Physiol Bioch 49:13–17

    Article  CAS  Google Scholar 

  • Navarro B, Pantaleo V, Gisel A, Moxon S, Dalmay T, Bisztray G, Di Serio F, Burgyán J (2009) Deep sequencing of viroid-derived small RNAs from grapevine provides new insights on the role of RNA silencing in plant–viroid interaction. PLoS One 4:e7686

    Article  PubMed Central  PubMed  Google Scholar 

  • Navarro B, Gisel A, Rodio ME, Delgado S, Flores R, Di Serio F (2012) Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide degradation of a host mRNA as predicted by RNA silencing. Plant J 70:991–1003

    Article  CAS  PubMed  Google Scholar 

  • Naya L, Paul S, Valdés-López O, Mendoza-Soto AB, Nova-Franco B, Sosa-Valencia G, Reyes JL, Hernández G (2014) Regulation of copper homeostasis and biotic interactions by microRNA 398b in common bean. PLoS One 9:e84416

    Article  PubMed Central  PubMed  Google Scholar 

  • Niu QW, Lin SS, Reyes JL, Chen KC, Wu HW, Yeh SD, Chua NH (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428

    Article  CAS  PubMed  Google Scholar 

  • Palatnik JF, Allen E, Wu XL, 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, Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 102:3691–3696

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11:745–760

    Article  CAS  PubMed  Google Scholar 

  • Qu J, Ye J, Fang RX (2007) Artificial microRNA-mediated virus resistance in plants. J Virol 81:6690–6699

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Romeis T, Piedras P, Zhang SQ, Klessig DF, Hirt H, Jones JDG (1999) Rapid Avr9- and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11(2):273–287

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ruiz-Ferrer V, Voinnet O (2007) Viral suppression of RNA silencing: 2b wins the Golden Fleece by defeating Argonaute. Bioessays 29:319–323

    Article  CAS  PubMed  Google Scholar 

  • Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sun GX, Luan YS, Cui JJ (2014) Mining and characterization of miRNAs closely associated with the pathogenicity in tomato. Hereditas (Beijing) 36:69–76

    Article  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Takagi K, Nishizawa K, Hirose A, Kurauchi T, Senda M, Masuta C, Ishimoto M (2013) Seed coat pigmentation in transgenic soybean expressing the silencing suppressor 2b gene of cucumber mosaic virus. Plant Cell Rep 32:1903–1912

    Article  CAS  PubMed  Google Scholar 

  • Tomato Genome C (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

  • Tsuda K, Katagiri F (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465

    Article  CAS  PubMed  Google Scholar 

  • Tsushima D, Adkar-Purushothama CR, Taneda A, Sano T (2015) Changes in relative expression levels of viroid-specific small RNAs and microRNAs in tomato plants infected with severe and mild symptom-inducing isolates of Potato spindle tuber viroid. J Gen Plant Pathol 81:49–62

    Article  CAS  Google Scholar 

  • Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498

    Article  PubMed  Google Scholar 

  • Vetukuri RR, Asman AKM, Tellgren-Roth C, Jahan SN, Reimegard J, Fogelqvist J, Savenkov E, Soderbom F, Avrova AO, Whisson SC, Dixelius C (2012) Evidence for small RNAs homologous to effector-encoding genes and transposable elements in the oomycete Phytophthora infestans. PLoS One 7:e51399

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vu TV, Choudhury NR, Mukherjee SK (2013) Transgenic tomato plants expressing artificial microRNAs for silencing the pre-coat and coat proteins of a begomovirus, Tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res 172:35–45

    Article  CAS  PubMed  Google Scholar 

  • Weiberg A, Wang M, Lin FM, Zhao HW, Zhang ZH, Kaloshian I, Huang HD, Jin HL (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–123

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu YJ, Du JF, Wang XL, Fang XF, Shan WX, Liang ZS (2012) Computational prediction and experimental verification of miRNAs in Panicum miliaceum L. Sci China Life Sci 55:807–817

    Article  PubMed  Google Scholar 

  • Xiao Y, Luan YS (2014) MiR482 mediates the biotic stress response of plant. Plant Physiol J 50:741–748

    CAS  Google Scholar 

  • Xie F, Frazier TP, Zhang B (2011) Identification, characterization and expression analysis of microRNAs and their targets in the potato (Solanum tuberosum). Gene 473:8–22

    Article  CAS  PubMed  Google Scholar 

  • Yi H, Richards EJ (2007) A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell 19:2929–2939

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yu N, Cai WJ, Wang S, Shan CM, Wang LJ, Chen XY (2010) Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22:2322–2335

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang YJ (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res 33:701–704

    Article  Google Scholar 

  • Zhang BH, Wang QL (2015) MicroRNA-based biotechnology for plant improvement. J Cell Physiol 230:1–15

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Yuan YR, Pei Y, Lin SS, Tuschl T, Patel DJ, Chua NH (2006) Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 20:3255–3268

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang JG, Zeng R, Chen JS, Liu X, Liao QS (2008) Identification of conserved microRNAs and their targets from Solanum lycopersicum Mill. Gene 423:1–7

    Article  CAS  PubMed  Google Scholar 

  • Zhang XH, Li HX, Zhang JH, Zhang CJ, Gong PJ, Ziaf K, Xiao FM, Ye ZB (2011a) Expression of artificial microRNAs in tomato confers efficient and stable virus resistance in a cell-autonomous manner. Transgenic Res 20:569–581

    Article  CAS  PubMed  Google Scholar 

  • Zhang XH, Zou Z, Zhang JH, Zhang YY, Han QQ, Hu TX, Xu XG, Liu H, Li HX, Ye ZB (2011b) Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Lett 585:435–439

    Article  CAS  PubMed  Google Scholar 

  • Zhang YP, Bai YH, Han J, Chen M, Kayesh E, Jiang WB, Fang JG (2013) Bioinformatics prediction of miRNAs in the Prunus persica genome with validation of their precise sequences by miR-RACE. J Plant Physiol 170:80–92

    Article  CAS  PubMed  Google Scholar 

  • Zhu QH, Helliwell CA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62:487–495

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Ding YF, Liu HL (2011) MiR398 and plant stress responses. Physiol Plantarum 143:1–9

    Article  CAS  Google Scholar 

  • Zuo JH, Wang YX, Liu HP, Ma YZ, Ju Z, Zhai BQ, Fu DQ, Zhu Y, Luo YB, Zhu BZ (2011) MicroRNAs in tomato plants. Sci China Life Sci 54:599–605

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (31272167 and 31471880).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. School of Life Science and Biotechnology, Dalian University of Technology, Dalian, China

    Weichen Wang & Yushi Luan

Authors
  1. Weichen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yushi Luan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yushi Luan.

Additional information

Communicated by N. Stewart.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, W., Luan, Y. The advance of tomato disease-related microRNAs. Plant Cell Rep 34, 1089–1097 (2015). https://doi.org/10.1007/s00299-015-1782-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-015-1782-0

Keywords

Search

Navigation