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Transcriptome-wide analysis of dynamic variations in regulation modes of grapevine microRNAs on their target genes during grapevine development

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Abstract

MicroRNAs (miRNAs) play critical regulatory roles mainly through cleaving their target mRNAs or repressing gene translation during plant development. Grapevines are among the most economically important fruit crops with available whole genome sequences. Studies on grapevine miRNAs (Vv-miRNAs) are also widely available. However, studies on the regulation mode of Vv-miRNAs on their target mRNAs during grapevine development have not been studied well, especially at the transcriptome-wide level. Here, six small RNA and mRNA libraries from various grapevine tissues were constructed for Illumina and Degradome sequencing. Subsequently, we systematically analyzed the spatiotemporal variations in the regulation of the target genes of regulation of Vv-miRNAs. In total, 242 known and 132 novel Vv-miRNAs and 193 target mRNAs were identified, including 103 target mRNAs for known and 90 target mRNAs for novel miRNAs, were validated in one or more of the tissues examined. More than 50 % of novel miRNAs were expressed exclusively in the flowers and berries, where they cleaved their target genes in a tissue-specific manner, especially, the breadth of their cleavage sites in flower tissues. Moreover, six novel miRNAs in berries responded to exogenous gibberellin and/or ethylene under a quantitative real time RT-PCR analysis, which confirmed their regulatory functions during berry development. Up to 93.6 % of the known miRNAs were highly conserved in various tissues, where their expression levels exhibited dynamic variations during grapevine development. Significantly, some Vv-miRNA families had one key member that acted as the main regulator of their target genes during grapevine development.

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References

  • Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18:758–762

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Addo-Quaye C, Miller W, Axtell MJ (2009) CleaveL and A pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 25:130–131

    Article  CAS  PubMed  Google Scholar 

  • Allen RS, Li JY, Alonso-Peral MM, White RG, Gubler F, Millar AA (2010) MicroR159 regulation of most conserved targets in Arabidopsis has negligible phenotypic effects. Silence 1:18

    Article  PubMed Central  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 co-expression with neighboring miRNAs and host genes. RNA 11:241–247

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Wang C, Fang JG, Yang G, Yu HP, Song CN (2011) Cloning, subcellular localization and expression analysis of SPL9 and SPL10 genes from grapevine. Acta Horticulturae Sinica 38(2):240–250 (in Chinese)

    CAS  Google Scholar 

  • Carra A, Mica E, Gambino G, Pindo M, Moser C, Pè ME, Schubert A (2009) Cloning and characterization of small non-coding RNAs from grapevine. Plant J 59:750–763

    Article  CAS  PubMed  Google Scholar 

  • Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338

    Article  CAS  PubMed  Google Scholar 

  • Fahlgren N, Howell MD, Kasschau KD et al (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2:e219

    Article  PubMed Central  PubMed  Google Scholar 

  • Jagadeeswaran GR, Zheng Y, Sumathipala N, Jiang HB, Arrese EL, Soulages JL, Zhang W, Sunkar R (2010) Deep sequencing of small RNA libraries reveals dynamic regulation of conserved and novel microRNAs and microRNA-stars during silkworm development. BMC Genomics 11:52

    Article  PubMed Central  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Fabbro CD, Alaux M, Gaspero GD, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Clainche IL, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave PèG, Valle FME, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quétier F, Wincker P, French-Italian public consortium for grapevine genome characterization (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  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 

  • Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217

    Article  CAS  PubMed  Google Scholar 

  • Lazzari B, Caprera A, Cestaro A, Merelli I, DelCorvol M, Fontana P, Milanesi L, Velasco R, Stella A (2009) Ontology-oriented retrieval of putative microRNAs in Vitis vinifera via GrapeMiRNA: a web database of de novo predicted grape microRNAs. BMC Plant Biol 9:82

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee Y, Jeon K, Lee JT, Kim S, Kim VN (2002) MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 21:4663–4670

    Article  CAS  PubMed  Google Scholar 

  • Leung AKL, Sharp PA (2010) MicroRNA functions in stress responses. Mol Cell 40(2):205–215

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lu YD, Gan QH, Chi XY, Qin S (2008) Identification and characteristization of microRNAs and their targets in grapevine (Vitis Vinifera). Agric Sci China 7(8):929–943

    Article  CAS  Google Scholar 

  • Mallory AC, Vaucheret H (2004) MicroRNAs: something important between the genes. Curr Opin Plant Biol 7:120–125

    Article  CAS  PubMed  Google Scholar 

  • Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-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 Central  PubMed  Google Scholar 

  • Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao XF, Carrington JC, Chen XM, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi YJ, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20:3186–3190

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mica E, Piccolo V, Delledonne M, Ferrarini A, Pezzotti M, Casati C, Del Fabbro C, Valle G, Policriti A, Morgante M, Pesole G, Enrico Pè M, Horner DS (2010) Correction: high-throughput approaches reveal splicing of primary microRNA transcripts and tissue specific expression of mature microRNAs in Vitis vinifera. BMC Genomics 11:9

    Article  Google Scholar 

  • Moxon S, Jing R, Szittya G, Schwach F, Pilcher RL, Moulton V, Dalmay T (2008a) Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res 18:1602–1609

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62:960–976

    CAS  PubMed  Google Scholar 

  • Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66

    Article  CAS  PubMed  Google Scholar 

  • Song CN, Wang C, Zhang CQ, Nicholas KK, Yu HP, Ma ZQ, Fang JG (2010) Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genomics 11:431

    Article  PubMed Central  PubMed  Google Scholar 

  • Sun X, Nicholas KK, Han J, Leng XP, Fang JG (2012) Characterization of grapevine microR164 and its target genes. Mol Biol Rep 39(10):9463–9472

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Szittya G, Moxon S, Santos DM, Jing R, Fevereiro MP, Moulton V, Dalmay T (2008) High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 9:593

    Article  PubMed Central  PubMed  Google Scholar 

  • Thomson DW, Bracken CP, Goodal GJ (2011) Experimental strategies for microRNA target identification. Nucleic Acids Res 39(16):6845–6853

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, FitzGerald LM, Vezzulli S, Reid J, Malacame G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Cyzerski R, Moretto M, Gutin N, Stefanin M, Chen Y, Segala C, Kavenport C, Demattè L, Mraz A, Battilana J, Stormo K, Costa F, Tao QZ, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepolele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Ven de Peer Y, Salamini F, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2:e1326

    Article  PubMed Central  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:R65

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang C, Shangguan LF, Nicholas KK, Wang XC, Han J, Song CN, Fang JG (2011a) Characterization of microRNAs identified in a table grapevine cultivar with validation of computationally predicated grapevine miRNAs by miR-RACE. PLoS ONE 6(7):e21259

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang C, Wang XC, Nicholas KK, Song CN, Zhang CQ, Li XY, Han J, Fang JG (2011b) Deep sequencing of grapevine flower and berry short RNA library for discovery of novel microRNAs and validation of precise sequences of grapevine microRNAs deposited in miRBase. Physiol Plant 143:64–81

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Han J, Liu C, Nicholas K, Kayesh E, Shangguan LF, Li XY, Fang JG (2012) Identification of microRNAs from Amur grapes (Vitis amurensis Rupr.) by deep sequencing and analysis of microRNA variations with bioinformatics. BMC Genomics 13:122

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang C, Han J, Nicholas KK, Wang XC, Liu H, Li XY, Leng XP, Fang JG (2013) The characterization of target mRNAs for table grapevines miRNAs with an integrated strategy of modified RLM RACE, PPM RACE and qRT-PCRs of cleavage products. J Plant Physiol 170(10):943–957

    Article  CAS  PubMed  Google Scholar 

  • Wilson DN, Chung H, Elliott RC, Bremer E, George D, Koh S (2005) Microarray analysis of postictal transcriptional regulation of neuropeptides. J Mol Neurosci 25:285–298

    Article  CAS  PubMed  Google Scholar 

  • Xie FL, Frazier TP, Zhang BH (2011) Identification, characterization and expression analysis of MicroRNAs and their targets in the potato (Solanum tuberosum). Gene 473:8–22. doi:10.1016/j.gene.2010.09.007

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and the Graduate innovative training project in Jiangsu Province CXZZ11_0665 and CXZZ12_0284.

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The authors declare that they have no conflict of interests.

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Correspondence to Jinggui Fang.

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Wang, C., Leng, X., Zhang, Y. et al. Transcriptome-wide analysis of dynamic variations in regulation modes of grapevine microRNAs on their target genes during grapevine development. Plant Mol Biol 84, 269–285 (2014). https://doi.org/10.1007/s11103-013-0132-2

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  • DOI: https://doi.org/10.1007/s11103-013-0132-2

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