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Cold stress responsive microRNAs and their targets in Musa balbisiana |
Jingyi WANG1,Juhua LIU1,Caihong JIA1,Hongxia MIAO1,Jianbin ZHANG1,Zhuo WANG1,Biyu XU1( ),Zhiqiang JIN1,2() |
1. Key Laboratory of Biology and Genetic Resources of Tropical Crops, Ministry of Agriculture/Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China
2. Key Laboratory of Genetic Improvement of Bananas, Haikou Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Haikou 570101, China |
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Abstract Cold stress is an environmental factor affecting plant development and production. Recently, microRNAs (miRNAs) have been found to be involved in several plant processes such as growth regulation and stress responses. Although miRNAs and their targets have been identified in several banana species, their participation during cold accumulation in banana remains unknown. In this study, two small RNA libraries were generated from micropropagated plantlets of Musa balbisiana grown at normal and low temperature (5°C). A total of 69 known miRNAs and 32 putative novel miRNAs were detected in the libraries by Solexa sequencing. Sixty-four cold-inducible miRNAs were identified through differentially expressed miRNAs analysis. Among 43 miRNAs belonging to 26 conserved miRNA families with altered expression, 18 were upregulated and 25 downregulated under cold stress. Of 21 putative novel miRNAs with altered expression, four were downregulated and 17 upregulated. Furthermore, eight miRNAs were validated by stem-loop qRT-PCR and their dynamic differential expression was analyzed. In addition, 393 target genes of 58 identified cold-responsive miRNAs were predicted and categorized by function. These results provide important information for further characterization and functional analysis of cold-responsive miRNAs in banana.
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| Keywords
cold stress
microRNA
Musa balbisiana
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Corresponding Author(s):
Biyu XU,Zhiqiang JIN
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Just Accepted Date: 14 December 2016
Online First Date: 04 January 2017
Issue Date: 22 January 2017
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|
| 1 |
Bartel D P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2): 281–297
https://doi.org/10.1016/S0092-8674(04)00045-5
|
| 2 |
Park M Y, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig R S. Nuclear processing and export of microRNAs in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(10): 3691–3696
https://doi.org/10.1073/pnas.0405570102
|
| 3 |
Papp I, Mette M F, Aufsatz W, Daxinger L, Schauer S E, Ray A, van der Winden J, Matzke M, Matzke A J. Evidence for nuclear processing plant microRNA and short interfering precursors. Plant Physiology, 2003, 132(3): 1382–1390
https://doi.org/10.1104/pp.103.021980
|
| 4 |
Valencia-Sanchez M A, Liu J D, Hannon G J, Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes & Development, 2006, 20(5): 515–524
https://doi.org/10.1101/gad.1399806
|
| 5 |
Dong Q H, Han J, Yu H P, Wang C, Zhao M Z, Liu H, Ge A J, Fang J G. Computational identification of microRNAs in strawberry expressed sequence tags and validation of their precise sequences by miR-RACE. Journal of Heredity, 2012, 103(2): 268–277
https://doi.org/10.1093/jhered/esr127
|
| 6 |
Sunkar R, Li Y F, Jagadeeswaran G. Functions of microRNAs in plant stress responses. Trends in Plant Science, 2012, 17(4): 196–203
https://doi.org/10.1016/j.tplants.2012.01.010
|
| 7 |
Sunkar R, Zhu J K. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 2004, 16(8): 2001–2019
https://doi.org/10.1105/tpc.104.022830
|
| 8 |
Zhou X, Wang G, Sutoh K, Zhu J K, Zhang W. Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochimica et Biophysica Acta, 2008, 1779(11): 780–788
https://doi.org/10.1016/j.bbagrm.2008.04.005
|
| 9 |
Liu H H, Tian X, Li Y J, Wu C A, Zheng C C. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA , 2008, 14(5): 836–843
https://doi.org/10.1261/rna.895308
|
| 10 |
Lu S, Sun Y H, Chiang V L. Stress-responsive microRNAs in Populus. Plant Journal, 2008, 55(1): 131–151
https://doi.org/10.1111/j.1365-313X.2008.03497.x
|
| 11 |
Zhang J, Xu Y, Huan Q, Chong K. Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress responses. BMC Genomics, 2009, 10(1): 449–465
https://doi.org/10.1186/1471-2164-10-449
|
| 12 |
Lv D K, Bai X, Li Y, Ding X D, Ge Y, Cai H, Ji W, Wu N, Zhu Y M. Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene, 2010, 459(1–2): 39–47
https://doi.org/10.1016/j.gene.2010.03.011
|
| 13 |
Tang Z, Zhang L, Xu C, Yuan S, Zhang F, Zheng Y, Zhao C. Uncovering small RNA-mediated responses to cold stress in a wheat thermosensitive genic male-sterile line by deep sequencing. Plant Physiology, 2012, 159(2): 721–738
https://doi.org/10.1104/pp.112.196048
|
| 14 |
Thiebaut F, Rojas C A, Almeida K L, Grativol C, Domiciano G C, Lamb C R, De Almeida Engler J, Hemerly A S, Ferreira P C G, De Almeida Engler J, Hemerly A S, Ferreira P C. Regulation of miR319 during cold stress in sugarcane. Plant, Cell & Environment, 2012, 35(3): 502–512
https://doi.org/10.1111/j.1365-3040.2011.02430.x
|
| 15 |
D’Hont A, Denoeud F, Aury J M, Baurens F C, Carreel F, Garsmeur O, Noel B, Bocs S, Droc G, Rouard M, Da Silva C, Jabbari K, Cardi C, Poulain J, Souquet M, Labadie K, Jourda C, Lengellé J, Rodier-Goud M, Alberti A, Bernard M, Correa M, Ayyampalayam S, Mckain M R, Leebens-Mack J, Burgess D, Freeling M, Mbéguié-A-Mbéguié D, Chabannes M, Wicker T, Panaud O, Barbosa J, Hribova E, Heslop-Harrison P, Habas R, Rivallan R, Francois P, Poiron C, Kilian A, Burthia D, Jenny C, Bakry F, Brown S, Guignon V, Kema G, Dita M, Waalwijk C, Joseph S, Dievart A, Jaillon O, Leclercq J, Argout X, Lyons E, Almeida A, Jeridi M, Dolezel J, Roux N, Risterucci A M, Weissenbach J, Ruiz M, Glaszmann J C, Quétier F, Yahiaoui N, Wincker P. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature, 2012, 488(710): 213–217
|
| 16 |
Baurens F C, Bocs S, Rouard M, Matsumoto T, Miller R N, Rodier-Goud M, MBeguie-A-MBeguie D, Yahiaoui N, MBéguié-A-MBéguié D, Yahiaoui N. Mechanisms of haplotype divergence at the RGA08 nucleotide-binding leucine-rich repeat gene locus in wild banana (Musa balbisiana). BMC Plant Biology, 2010, 10(1): 149–165
https://doi.org/10.1186/1471-2229-10-149
|
| 17 |
Subbaraya U. Potential and constraints of using wild Musa. In: Subbaraya U, eds. Farmers’ knowledge of wild Musa in India. Food and Agriculture Organization of the United Nations, 2006, 33–36
|
| 18 |
Ravi I, Uma S, Vaganan M M, Mustaffa M M. Phenotyping bananas for drought resistance. Frontiers in Physiology, 2013, 4: 9
https://doi.org/10.3389/fphys.2013.00009
|
| 19 |
Davey M W, Gudimella R, Harikrishna J A, Sin L W, Khalid N, Keulemans J. A draft Musa balbisiana genome sequence for molecular genetics in polyploid, inter- and intra-specific Musa hybrids. BMC Genomics, 2013, 14(1): 683–703
https://doi.org/10.1186/1471-2164-14-683
|
| 20 |
Chai J, Feng R J, Shi H R, Ren M Y, Zhang Y D, Wang J Y. Bioinformatic identification and expression analysis of banana microRNAs and their targets. PLoS One, 2015, 10(4): e0123083
https://doi.org/10.1371/journal.pone.0123083
|
| 21 |
Ghag S B, Shekhawat U K S, Ganapathi T R. Small RNA profiling of two important cultivars of banana and overexpression of miRNA156 in transgenic banana plants. PLoS One, 2015, 10(5): e0127179
https://doi.org/10.1371/journal.pone.0127179
|
| 22 |
Bi F C, Meng X C, Ma C, Yi G J. Identification of miRNAs involved in fruit ripening in Cavendish bananas by deep sequencing. BMC Genomics, 2015, 16(1): 776–791
https://doi.org/10.1186/s12864-015-1995-1
|
| 23 |
Lee W S, Gudimella R, Wong G R, Tammi M T, Khalid N, Harikrishna J A. Transcripts and microRNAs responding to salt stress in Musa acuminata colla (AAA group) cv. berangan roots. PLoS One, 2015, 10(5): e0127526
https://doi.org/10.1371/journal.pone.0127526
|
| 24 |
Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Research, 2014, 42(D1): 68–73
https://doi.org/10.1093/nar/gkt1181
|
| 25 |
Wen M, Shen Y, Shi S, Tang T. miREvo: an integrative microRNA evolutionary analysis platform for next-generation sequencing experiments. BMC Bioinformatics, 2012, 13(1): 140–150
https://doi.org/10.1186/1471-2105-13-140
|
| 26 |
Friedlander M R, Mackowiak S D, Li N, Chen W, Rajewsky N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Research, 2012, 40(1): 37–52
https://doi.org/10.1093/nar/gkr688
|
| 27 |
Meyers B C, Axtell M J, Bartel B, Bartel D P, Baulcombe D, Bowman J L, Cao X, Carrington J C, Chen X, Green P J, Griffiths-Jones S, Jacobsen S E, Mallory A C, Martienssen R A, Poethig R S, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu J K. Criteria for annotation of plant MicroRNAs. Plant Cell, 2008, 20(12): 3186–3190
https://doi.org/10.1105/tpc.108.064311
|
| 28 |
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): 136–138
https://doi.org/10.1093/bioinformatics/btp612
|
| 29 |
Storey J D. The positive false discovery rate: a Bayesian interpretation and the q-value. Annals of Statistics, 2003, 31(6): 2013–2035
https://doi.org/10.1214/aos/1074290335
|
| 30 |
Livak K J, Schmittgen T D. Analysis of relative gene expression data using realtime quantitative PCR and the 2−Δ ΔCT method. Methods, 2001, 25(4): 402–408
https://doi.org/10.1006/meth.2001.1262
|
| 31 |
Dai X B, Zhao P X. psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research, 2011, 39(suppl. 2): W155–W159
https://doi.org/10.1093/nar/gkr319
|
| 32 |
Young M D, Wakefield M J, Smyth G K, Oshlack A.Goseq: gene ontology testing for RNA-seq datasets. ResearchGate, 2012,1–26
|
| 33 |
Bonnet E, Wuyts J, Rouze P, 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): 2911–2917
https://doi.org/10.1093/bioinformatics/bth374
|
| 34 |
Rajagopalan R, Vaucheret H, Trejo J, Bartel D P. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes & Development, 2006, 20(24): 3407–3425
https://doi.org/10.1101/gad.1476406
|
| 35 |
Sunkar R, Zhou X F, Zheng Y, Zhang W X, Zhu J K. Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biology, 2008, 8(1): 25–42
https://doi.org/10.1186/1471-2229-8-25
|
| 36 |
Xu Q, Liu Y L, Zhu A D, Wu X M, Ye J L, Yu K Q, Guo W W, Deng X X. Discovery and comparative profiling of microRNAs in a sweet orange red-flesh mutant and its wild type. BMC Genomics, 2010, 11(1): 246–263
https://doi.org/10.1186/1471-2164-11-246
|
| 37 |
Jones-Rhoades M W, Bartel D P, Bartel B. MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology, 2006, 57(1): 19–53
https://doi.org/10.1146/annurev.arplant.57.032905.105218
|
| 38 |
Wang B, Sun Y F, Song N, Wei J P, Wang X J, Feng H, Yin Z Y, Kang Z S. MicroRNAs involving in cold, wounding and salt stresses in Triticum aestivum L. Plant Physiology and Biochemistry, 2014, 80: 90–96
https://doi.org/10.1016/j.plaphy.2014.03.020
|
| 39 |
Chen L, Zhang Y, Ren Y, Xu J, Zhang Z, Wang Y. Genome-wide identification of cold-responsive and new microRNAs in Populus tomentosa by high-throughput sequencing. Biochemical and Biophysical Research Communications, 2012, 417(2): 892–896
https://doi.org/10.1016/j.bbrc.2011.12.070
|
| 40 |
Zhang X N, Li X, Liu J H. Identification of conserved and novel cold-responsive microRNAs in trifoliate orange (Poncirus trifoliata (L.) Raf.) using high-throughput sequencing. Plant Molecular Biology Reporter, 2014, 32(2): 328–341
https://doi.org/10.1007/s11105-013-0649-1
|
| 41 |
Agarwal M, Hao Y, Kapoor A, Dong C H, Fujii H, Zheng X, Zhu J K A. R2R3type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. Journal of Biological Chemistry, 2006, 281(49): 37636–37645
https://doi.org/10.1074/jbc.M605895200
|
| 42 |
Liu C, Wu Y, Wang X. bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta, 2012, 235(6): 1157–1169
https://doi.org/10.1007/s00425-011-1564-z
|
| 43 |
Huang X S, Wang W, Zhang Q, Liu J H. A basic helix-loop- helix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiology, 2013, 162(2): 1178–1194
https://doi.org/10.1104/pp.112.210740
|
| 44 |
Giacomelli J I, Weigel D, Chan R L, Manavella P A. Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytologist, 2012, 195(4): 766–773
https://doi.org/10.1111/j.1469-8137.2012.04259.x
|
| 45 |
Olsen A N, Ernst H A, Leggio L L, Skriver K. NAC transcription factors: structurally distinct, functionally diverse. Trends in Plant Science, 2005, 10(2): 79–87
https://doi.org/10.1016/j.tplants.2004.12.010
|
| 46 |
Hu H H, You J, Fang Y J, Zhu X Y, Qi Z Y, Xiong L Z. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Molecular Biology, 2008, 67(1): 169–181
https://doi.org/10.1007/s11103-008-9309-5
|
| 47 |
Kim J S, Mizoi J, Kidokoro S, Maruyama K, Nakajima J, Nakashima K, Mitsuda N, Takiguchi Y, Ohme-Takagi M, Kondou Y, Yoshizumi T, Matsui M, Shinozaki K, Yamaguchi-Shinozaki K. Arabidopsisgrowth-regulating factor7 functions as a transcriptional repressor of abscisic acid- and osmotic stress-responsive genes, including DREB2A. Plant Cell, 2012, 24(8): 3393–3405
https://doi.org/10.1105/tpc.112.100933
|
| 48 |
Tan Y F, O’Toole N, Taylor N L, Millar A H. Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiology, 2010, 152(2): 747–761
https://doi.org/10.1104/pp.109.147942
|
| 49 |
Goldgur Y, Rom S, Ghirlando R, Shkolnik D, Shadrin N, Konrad Z, Bar-Zvi D. Desiccation and zinc binding induce transition of tomato abscisic acid stress ripening 1, a water stress-and salt stress-regulated plant-specific protein, from unfolded to folded state. Plant Physiology, 2007, 143(2): 617–628
https://doi.org/10.1104/pp.106.092965
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