Identification of miRNAs involved in fruit ripening in Cavendish bananas by deep sequencing

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Bi, Fangcheng ^a,b,c   Meng, Xiangchun ^a,b,c   Ma, Chao ^d   Yi, Ganjun ^a,b,c  

^a INSTITUTE OF ANIMAL SCIENCE   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^c Key Laboratory of Tropical and Subtropical Fruit Tree Researches   (China)

^d VOLCANI CENTER   (Israel)

Author keywords

Fruit ripening; High throughput sequencing; MiRNA; Musa acuminate

Indexed keywords

1 METHYLCYCLOPROPENE; BETA GALACTOSIDASE; BETA GLUCOSIDASE; ETHYLENE; MICRORNA; PROPYLENE; TRANSCRIPTION FACTOR; TRANSFER RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; PLANT RNA; TRANSCRIPTOME;

APETALA2 GENE; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DEEP SEQUENCING; DOWN REGULATION; EIN3 GENE; FRUIT RIPENING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE TARGETING; HIGH THROUGHPUT SEQUENCING; MUSA AAA GROUP; NONHUMAN; PLANT GENE; PREDICTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPL GENE; UPREGULATION; FRUIT; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MUSA; PLANT GENOME;

FRUIT; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; MUSA; RNA, PLANT; TRANSCRIPTOME;

EID: 84994410212     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1995-1     Document Type: Article

References (76)

1. Giovannoni JJ. Genetic regulation of fruit development and ripening. Plant Cell. 2004;16(Suppl):S170-80
2. Seymour GB, Ostergaard L, Chapman NH, Knapp S, Martin C. Fruit development and ripening. Annu Rev Plant Biol. 2013;64:219-41
3. Gao C, Ju Z, Cao D, Zhai B, Qin G, Zhu H, et al. MicroRNA profiling analysis throughout tomato fruit development and ripening reveals potential regulatory role of RIN on microRNAs accumulation. Plant Biotechnol J. 2015;13(3):370-82
4. Bapata VA, Trivedib PK, Ghoshc A, Ganapathic VASTR, Nath P. Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnol Adv. 2010;28(1):94-107
5. Clendennen S, Kipp P, May G, AK K. The role of ethylene in banana fruit ripening. In: Biology and biotechnology of the plant hormone ethylene. Dordrecht: Kluwer Academic Publishers; 1997. p. 141-8
6. Liu X, Shiomi S, Nakatsuka A, Kubo Y, Nakamura R, Inaba A. Characterization of ethylene biosynthesis associated with ripening in banana fruit. Plant Physiol. 1999;121(4):1257-66
7. Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H. The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene. J Exp Bot. 2010;61(5):1523-35
8. Mbeguie-A-Mbeguie D, Hubert O, Fils-Lycaon B, Chillet M, Baurens FC. EIN3-like gene expression during fruit ripening of Cavendish banana (Musa acuminata cv. Grande naine). Physiol Plant. 2008;133(2):435-48
9. Roy Choudhury S, Roy S, Nag A, Singh SK, Sengupta DN. Characterization of an AGAMOUS-like MADS box protein, a probable constituent of flowering and fruit ripening regulatory system in banana. PLoS One. 2012;7(9):e44361
10. Shan W, Kuang JF, Chen L, Xie H, Peng HH, Xiao YY, et al. Molecular characterization of banana NAC transcription factors and their interactions with ethylene signalling component EIL during fruit ripening. J Exp Bot. 2012;63(14):5171-87
11. Xiao YY, Chen JY, Kuang JF, Shan W, Xie H, Jiang YM, et al. Banana ethylene response factors are involved in fruit ripening through their interactions with ethylene biosynthesis genes. J Exp Bot. 2013;64(8):2499-510
12. Ba LJ, Shan W, Xiao YY, Chen JY, Lu WJ, Kuang JF. A ripening-induced transcription factor MaBSD1 interacts with promoters of MaEXP1/2 from banana fruit. Plant Cell Rep. 2014;33(11):1913-20
13. Ba L-J, Shan W, Kuang J-F, Feng B-H, Xiao Y-Y, Lu W-J, et al. The Banana MaLBD (LATERAL ORGAN BOUNDARIES DOMAIN) Transcription Factors Regulate EXPANSIN Expression and Are Involved in Fruit Ripening. Plant Mol Biol Rep. 2014;32(6):1103-13
14. Cuperus JT, Fahlgren N, Carrington JC. Evolution and functional diversification of MIRNA genes. Plant Cell. 2011;23(2):431-42
15. Debat HJ, Ducasse DA. Plant microRNAs: recent advances and future challenges. Plant Mol Biol Rep. 2014;32(6):1257-69
16. Moxon S, Jing R, Szittya G, Schwach F, Rusholme Pilcher RL, Moulton V, et al. Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res. 2008;18(10):1602-9
17. Zuo J, Zhu B, Fu D, Zhu Y, Ma Y, Chi L, et al. Sculpting the maturation, softening and ethylene pathway: the influences of microRNAs on tomato fruits. BMC Genomics. 2012;13:7
18. Zhang X, Zou Z, Zhang J, Zhang Y, Han Q, Hu T, et al. Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Lett. 2011;585(2):435-9
19. Gao Z, Shi T, Luo X, Zhang Z, Zhuang W, Wang L. High-throughput sequencing of small RNAs and analysis of differentially expressed microRNAs associated with pistil development in Japanese apricot. BMC Genomics. 2012;13:371
20. Zhu QH, Helliwell CA. Regulation of flowering time and floral patterning by miR172. J Exp Bot. 2011;62(2):487-95
21. Silva GFF, Silva EM, Azevedo MS, Guivin MAC, Ramiro DA, Figueiredo CR, et al. microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development. Plant J. 2014;78(4):604-18
22. Liu Y, Wang L, Chen D, Wu X, Huang D, Chen L, et al. Genome-wide comparison of microRNAs and their targeted transcripts among leaf, flower and fruit of sweet orange. BMC Genomics. 2014;15:695
23. Chen W, Kong J, Lai T, Manning K, Wu C, Wang Y, et al. Tuning LeSPL-CNR expression by SlymiR157 affects tomato fruit ripening. Sci Rep. 2015;5:7852
24. Wu J, Wang D, Liu Y, Wang L, Qiao X, Zhang S. Identification of miRNAs involved in pear fruit development and quality. BMC Genomics. 2014;15:953
25. Aukerman MJ, Sakai H. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell. 2003;15(11):2730-41
26. Chen X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science. 2004;303(5666):2022-5
27. Karlova R, van Haarst JC, Maliepaard C, van de Geest H, Bovy AG, Lammers M, et al. Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis. J Exp Bot. 2013;64(7):1863-78
28. D'Hont A, Denoeud F, Aury JM, Baurens FC, Carreel F, Garsmeur O, et al. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature. 2012;488(7410):213-7
29. Chai J, Feng R, Shi H, Ren M, Zhang Y, Wang J. Bioinformatic identification and expression analysis of banana MicroRNAs and their targets. PLoS One. 2015;10(4):e0123083
30. Wen JZ, Liao JY, Zheng LL, Xu H, Yang JH, Guan DG, et al. A contig-based strategy for the genome-wide discovery of microRNAs without complete genome resources. PLoS One. 2014;9(2):e88179
31. Reid MS, Staby GL. A Brief History of 1-Methylcyclopropene. Hortscience. 2008;43(1):83-5
32. Tonutti P, Bonghi C, Ramina A. Modulating effects of ethylene and ethylene inhibitors in the control of fruit ripening. In: Ramina A, Chang C, Giovannoni J, Klee H, Perata P, Woltering E, editors. Advances in Plant Ethylene Research: Proceedings of the 7th International Symposium on the Plant Hormone Ethylene. Dordrecht, The Netherlands: online: Springer; 2007. p. 407-15
33. Eyles RP, Williams PH, Ohms SJ, Weiller GF, Ogilvie HA, Djordjevic MA, et al. microRNA profiling of root tissues and root forming explant cultures in Medicago truncatula. Planta. 2013;238(1):91-105
34. Kong X, Zhang M, Xu X, Li X, Li C, Ding Z. System analysis of microRNAs in the development and aluminium stress responses of the maize root system. Plant Biotechnol J. 2014;12(8):1108-21
35. Lakhotia N, Joshi G, Bhardwaj AR, Katiyar-Agarwal S, Agarwal M, Jagannath A, et al. Identification and characterization of miRNAome in root, stem, leaf and tuber developmental stages of potato (Solanum tuberosum L.) by high-throughput sequencing. BMC Plant Biol. 2014;14:6
36. Song C, Wang C, Zhang C, Korir NK, Yu H, Ma Z, et al. Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genomics. 2010;11:431
37. Kou SJ, Wu XM, Liu Z, Liu YL, Xu Q, Guo WW. Selection and validation of suitable reference genes for miRNA expression normalization by quantitative RT-PCR in citrus somatic embryogenic and adult tissues. Plant Cell Rep. 2012;31(12):2151-63
38. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 2006;20(24):3407-25
39. Morin RD, Aksay G, Dolgosheina E, Ebhardt HA, Magrini V, Mardis ER, et al. Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res. 2008;18(4):571-84
40. Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, et al. Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol. 2007;8(6):R96
41. Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, et al. Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J. 2010;62(6):960-76
42. Qiu D, Pan X, Wilson IW, Li F, Liu M, Teng W, et al. High throughput sequencing technology reveals that the taxoid elicitor methyl jasmonate regulates microRNA expression in Chinese yew (Taxus chinensis). Gene. 2009;436(1-2):37-44
43. Thiebaut F, Grativol C, Tanurdzic M, Carnavale-Bottino M, Vieira T, Motta MR, et al. Differential sRNA regulation in leaves and roots of sugarcane under water depletion. PLoS One. 2014;9(4):e93822
44. Liu HW, Luo LX, Liang CQ, Jiang N, Liu PF, Li JQ. High-throughput sequencing identifies novel and conserved cucumber (Cucumis sativus L.) microRNAs in response to cucumber green mottle mosaic virus infection. PLoS One. 2015;10(6):e0129002
45. Zhao CZ, Xia H, Frazier TP, Yao YY, Bi YP, Li AQ, et al. Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol. 2010;10:3
46. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, et al. Criteria for annotation of plant MicroRNAs. Plant Cell. 2008;20(12):3186-90
47. Yu R, Wang Y, Xu L, Zhu X, Zhang W, Wang R, et al. Transcriptome profiling of root microRNAs reveals novel insights into taproot thickening in radish (Raphanus sativus L.). BMC Plant Biol. 2015;15(1):30
48. Bonnet E, Wuyts J, Fau Rouze P, Fau RP, Van de Peer Y, Van de Peer Y. Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences. Bioinformatics. 2004;20(17):2911-7
49. Wang JW, Czech B, Weigel D. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell. 2009;138(4):738-49
50. Gandikota M, Birkenbihl RP, Hohmann S, Cardon GH, Saedler H, Huijser P. The miRNA156/157 recognition element in the 3' UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J. 2007;49(4):683-93
51. Aharoni A, De Vos CH, Wein M, Sun Z, Greco R, Kroon A, et al. The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J. 2001;28(3):319-32
52. Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R, et al. GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J. 2006;47(3):427-44
53. Sorin C, Declerck M, Christ A, Blein T, Ma L, Lelandais-Briere C, et al. A miR169 isoform regulates specific NF-YA targets and root architecture in Arabidopsis. New Phytol. 2014;202(4):1197-211
54. Guo HS, Xie Q, Fei JF, Chua NH. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for arabidopsis lateral root development. Plant Cell. 2005;17(5):1376-86
55. Gutierrez L, Bussell J, Pacurar D, Schwambach J, Pacurar M, Bellini C. Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell. 2009;10:3119-32
56. Kumar R, Sharma AK. Ethylene perception and signaling in ripening fruit. In: Nath P, Bouzayen M, Pech JC, Mattoo AK, editors. Fruit ripening: physiology, signalling and genomics. Croydon: CABI; 2014. p. 193-201
57. Wang Y, Wang W, Cai J, Zhang Y, Qin G, Tian S. Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening. Genome Biol. 2014;15(12):548
58. Kevany BM, Tieman DM, Taylor MG, Cin VD, Klee HJ. Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J. 2007;51(3):458-67
59. Skottke KR, Yoon GM, Kieber JJ, DeLong A. Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genet. 2011;7(4):e1001370
60. Carey AT, Smith DL, Harrison E, Bird CR, Gross KC, Seymour GB, et al. Down-regulation of a ripening-related beta-galactosidase gene (TBG1) in transgenic tomato fruits. J Exp Bot. 2001;52(357):663-8
61. Mazzuca S, Spadafora A, Innocenti AM. Cell and tissue localization of β-glucosidase during the ripening of olive fruit (Olea europaea) by in situ activity assay. Plant Sci. 2006;171(6):726-33
62. J-H S, Dong Y-H, C-L L, Shen Y-Y. Transcription and enzymatic analysis of beta-glucosidase VvBG1 in grape berry ripening. Plant Growth Regul. 2014;75(1):67-73
63. Hobert O. Gene regulation by transcription factors and microRNAs. Science. 2008;319(5871):1785-6
64. Cherian S, Figueroa CR, Nair H. 'Movers and shakers' in the regulation of fruit ripening: a cross-dissection of climacteric versus non-climacteric fruit. J Exp Bot. 2014;65(17):4705-22
65. Tieman DM, Ciardi JA, Taylor MG, Klee HJ. Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. Plant J. 2001;26(1):47-58
66. Yokotani N, Nakano R, Imanishi S, Nagata M, Inaba A, Kubo Y. Ripeningassociated ethylene biosynthesis in tomato fruit is autocatalytically and developmentally regulated. J Exp Bot. 2009;60(12):3433-42
67. Kawashima CG, Matthewman CA, Huang S, Lee BR, Yoshimoto N, Koprivova A, et al. Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J. 2011;66(5):863-76
68. Wan CY, Wilkins TA. A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem. 1994;223(1):7-12
69. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25
70. Wen M, Shen Y, Shi S, Tang T. miREvo: an integrative microRNA evolutionary analysis platform for next-generation sequencing experiments. BMC Bioinformatics. 2012;13:140
71. Friedlander MR, Mackowiak SD, Li N, Chen W, Rajewsky N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res. 2012;40(1):37-52
72. Wang L, Feng Z, Wang X, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics. 2010;26(1):136-8
73. Storey JD. The positive false discovery rate: a Bayesian interpretation and the q-value. Ann Statist. 2003;31:2013-35
74. Wu HJ, Ma YK, Chen T, Wang M, Wang XJ. PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Res. 2012;40(W1):W22-8
75. Chen L, Zhong HY, Kuang JF, Li JG, Lu WJ, Chen JY. Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta. 2011;234(2):377-90
76. Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP. Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods. 2007;3:12