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.
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References
Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131(14):3357–3365
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
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
Barakat A, Wall PK, Diloreto S, Depamphilis CW, Carlson JE (2007) Conservation and divergence of microRNAs in Populus. BMC Genomics 8:481
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
Budak H, Akpinar BA (2015a) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genomics. doi:10.1007/s10142-015-0451-2
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
Budak H, Kantar M, Bulut R, Akpinar BA (2015b) Stress responsive miRNAs and isomiRs in cereals. Plant Sci 235:1–13
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
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
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
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
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
Huq E (2006) Degradation of negative regulators: a common theme in hormone and light signaling networks? Trend Plant Sci 11(1):4–6
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
Jay F, Renou JP, Voinnet O, Navarro L (2010) Biotic stress-associated microRNAs: identification, detection, regulation, and functional analysis. MethodsMol. Biol 592:183–202
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
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
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
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
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
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
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
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
Phillips J, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581:3592–3597
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
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
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
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
Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510
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
Shi R, Chiang VL (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39(4):519–525
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
Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411
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
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
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
Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687
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
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
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
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
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
Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. PlantCell 14(Suppl):S131–S151
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
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
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
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].
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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.
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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
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DOI: https://doi.org/10.1007/s10142-016-0514-z