Skip to main content
Log in

Characterization of miRNAs responsive to exogenous ethylene in grapevine berries at whole genome level

  • Original Article
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are critical regulators of various biological and metabolic processes of plants. Numerous miRNAs and their functions have been identified and analyzed in many plants. However, till now, the involvement of miRNAs in the response of grapevine berries to ethylene has not been reported yet. Here, Solexa technology was employed to deeply sequence small RNA libraries constructed from grapevine berries treated with and without ethylene. A total of 124 known and 78 novel miRNAs were identified. Among these miRNAs, 162 miRNAs were clearly responsive to ethylene, with 55 downregulated, 59 upregulated, and 14 unchanged miRNAs detected only in the control. The other 35 miRNAs responsive to ethylene were induced by ethylene and detected only in the ethylene-treated grapevine materials. Expression analysis of 27 conserved and 26 novel miRNAs revealed that 13 conserved and 18 novel ones were regulated by ethylene during the whole development of grapevine berries. High-throughput sequencing and qRT-PCR assays revealed consistent results on the expression results of ethylene-responsive miRNAs. Moreover, 90 target genes for 34 novel miRNAs were predicted, most of which were involved in responses to various stresses, especially like exogenous ethylene treatment. The identified miRNAs may be mainly involved in grapevine berry development and response to various environmental conditions.

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
Fig. 8
Fig. 9

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(14):3357–3365

    Article  CAS  PubMed  Google Scholar 

  • Akpinar B, Kantar M, Budak H (2015) Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Funct Integr Genomics. doi:10.1007/s10142-015-0453-0

    Google Scholar 

  • Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 2005 17(6):1658–1673

  • Bapat VA, Trivedi PK, Ghosh A, Sane VA, Ganapathi TR, Nath P (2010) Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnol Adv 28(1):94–107

    Article  CAS  PubMed  Google Scholar 

  • Barakat A, Wall PK, Diloreto S, Depamphilis CW, Carlson JE (2007) Conservation and divergence of microRNAs in Populus. BMC Genomics 8:481

    Article  PubMed  PubMed Central  Google Scholar 

  • Böttcher C, Burbidge CA, Boss PK, Davies C (2013) Interactions between ethylene and auxin are crucial to the control of grape (Vitis vinifera L.) berry ripening. BMC Plant Biol 13:222

    Article  PubMed  PubMed Central  Google Scholar 

  • Budak H, Akpinar BA (2015a) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genomics. doi:10.1007/s10142-015-0451-2

    Google Scholar 

  • Budak H, Bulut R, Kantar M, ALptekim B (2015a) MicroRNA nomenclature and the need for a revised naming prescription. Briefings in functional genomics. doi:10.1093/bfgp/elv026

    Google Scholar 

  • Budak H, Kantar M, Bulut R, Akpinar BA (2015b) Stress responsive miRNAs and isomiRs in cereals. Plant Sci 235:1–13

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Wang T, Zhao M, Zhang W (2011) Ethylene-responsive miRNAs in roots of Medicago truncatula identified by high-throughput sequencing at whole genome level. Plant Sci 184:14–19

    Article  PubMed  Google Scholar 

  • Chen H, Li Z, Xiong L (2012) A plant microRNA regulates the adaptation of roots to drought stress. FEBS Letters 586(12):1742-1747

  • Chen X (2005) microRNA biogenesis and function in plants. FEBS Letters 579(26):5923–5931

  • Chen X (2009) Small RNAs and their roles in plant development. AnnuRev Cell Dev Biol 25:21–44

    Article  Google Scholar 

  • Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2(2):e219

    Article  PubMed  PubMed Central  Google Scholar 

  • Han J, Fang JG, Wang C, Yin YL, Sun X, Leng XP, Song CN (2014) Grapevine microRNAs responsive to exogenous gibberellin. BMC Genomics 15:111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huq E (2006) Degradation of negative regulators: a common theme in hormone and light signaling networks? Trend Plant Sci 11(1):4–6

    Article  CAS  Google Scholar 

  • Jagadeeswaran GR, Zheng Y, Sumathipala N, Jiang HB, Arrese EI, Soulages JL, Zhang WX, 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  PubMed Central  Google Scholar 

  • Jay F, Renou JP, Voinnet O, Navarro L (2010) Biotic stress-associated microRNAs: identification, detection, regulation, and functional analysis. MethodsMol. Biol 592:183–202

    CAS  Google Scholar 

  • Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. BiochimBiophysActa 1819(2):137–148

    CAS  Google Scholar 

  • Kim J, Park JH, Lim CJ, Lim JY, Ryu JY, Lee BW, Choi JP, Kim WB, Lee HY, Choi Y, Kim D, Hur CG, Kim S, Noh YS, Shin C, Kwon SY (2012) Small RNA and transcriptome deep sequencing proffers insight into floral gene regulation in Rosa cultivars. BMC Genomics 13:657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Chen YQ (2009) Insights into the mechanism of plant development: interactions of miRNAs pathway with phytohormone response. Biochem Biophys Res Commun 384:1–5

    Article  CAS  PubMed  Google Scholar 

  • Martinez G, Forment J, Llave C, Pallas V, Gomez G (2011) High-throughput sequencing, characterization and detection of new and conserved cucumber miRNAs. PLoS One 6(5):e19523

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Mica E, Piccolo V, Delledonne M, Ferrarini A, Pezzotti M, Casati C, Fabbro CD, Valle G, Policriti A, Morgante M, Pesole G, Enrico MP, 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:11–109

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

    Article  CAS  PubMed  PubMed Central  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(6):960–976

    CAS  PubMed  Google Scholar 

  • Pei HX, Ma N, Chen JW, Zheng Y, Tian J, Li J, Zhang S, Fei ZJ, Gao JP (2013) Integrative analysis of miRNA and mRNA profiles in response to ethylene in rose petals during flower opening. PLoS One 8(5):e64290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips J, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581:3592–3597

    Article  CAS  PubMed  Google Scholar 

  • Qiu DY, Pan XP, Wilson IW, Li F, Liu M, Teng W, Zhang B (2009) High throughput sequencing technology reveals that the taxoid elicitor methyl jasmonate regulates microRNA expression in Chinese yew (Taxus chinensis). Gene 436:37–44

    Article  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. Neuroscience Lett 339(1):62–66

    Article  CAS  Google Scholar 

  • Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49(4):592–606

    Article  CAS  PubMed  Google Scholar 

  • Ruan MB, Zhao YT, Meng ZH, Wang XJ, Yang WC (2009) Conserved miRNA analysis in Gossypium hirsutum through small RNA sequencing. Genomics 94(4):263–268

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510

    Article  CAS  PubMed  Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005.) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8(4):517–527

    Article  CAS  PubMed  Google Scholar 

  • Shi R, Chiang VL (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39(4):519–525

    Article  CAS  PubMed  Google Scholar 

  • Song CN, Wang C, Zhang CQ, Korir NK, 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  PubMed Central  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  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Taylor RS, Tarver JE, Hiscock SJ, P.C. D (2014) Evolutionary history of plant microRNAs. TrendsPlantSci 19:175–182. doi:10.1016/j.tplants.2013.11.008

    CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Shangguan L, Nicholas KK, Wang X, Han J, Song C, Fang J (2011b) 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  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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 

  • Wang C, Leng XP, Zhang YY, Kayesh E, Zhang YP, Sun X, Fang JG (2014) 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

    Article  CAS  PubMed  Google Scholar 

  • Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. PlantCell 14(Suppl):S131–S151

    CAS  Google Scholar 

  • Zhao CZ, Xia H, Frazier TP, Yao YY, Bi YP, Li YP, Li AQ, Li MJ, Zhang BH, Wang XJ (2010) Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 10:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Ziliotto F, Corso M, Rizzini FM, Rasori A, Botton A, Bonghi C (2012) Grape berry ripening delay induced by a pre-véraison NAA treatment is paralleled by a shift in the expression pattern of auxin- and ethylene-related genes. BMC Plant Biol 12:185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuo J, Zhu B, Fu D, Zhu Y, Ma Y, Chi L, Ju Z, Wang Y, Zhai B, Luo Y (2012) Sculpting the maturation, softening and ethylene pathway: the influences of microRNAs on tomato fruits. BMC Genomics 13:7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported by projects funded by the Natural Science Foundation of China (NSFC) (No. 31301759), China Postdoctoral Science Foundation funded project (2013M531373), Postdoctoral Foundation of Jiangsu Province (1301116C), Special Program of China Postdoctoral Science Foundation (2014T70533), the Nanjing Agricultural University Youth Science and Technology Innovation Fund (KJ2013013), and the Fundamental Research Funds for the Central Universities of China (KYZ201411), and Jiangsu Agriculture Science and Technology Innovation Fund (JASTIF) [CX(13)5017].

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Chen Wang or Jinggui Fang.

Additional information

This article forms part of a special issue of Functional & Integrative Genomics entitled “miRNA in model and complex organisms” (Issue Editors: Hikmet Budak and Baohong Zhang).

Fanggui Zhao and Chen Wang should be considered co-first authors.

Chen Wang and Jinggui Fang are co-corresponding authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, F., Wang, C., Han, J. et al. Characterization of miRNAs responsive to exogenous ethylene in grapevine berries at whole genome level. Funct Integr Genomics 17, 213–235 (2017). https://doi.org/10.1007/s10142-016-0514-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-016-0514-z

Keywords

Navigation