Identification of four functionally important microRNA families with contrasting differential expression profiles between drought-tolerant and susceptible rice leaf at vegetative stage

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Cheah, Boon Huat ^a   Nadarajah, Kalaivani ^a   Divate, Mayur Dashrath ^b   Wickneswari, Ratnam ^a  

^a UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

^b Bionivid Technology Private Limited   (India)

Author keywords

[No Author keywords available]

Indexed keywords

LIGNIN; MICRORNA; MICRORNA 166E 3P; MICRORNA 166H 5P; MICRORNA 169R 3P; MICRORNA 397A; MICRORNA 397B; MICRORNA 398B; MICRORNA 408 5P; MICRORNA 528 5P; STARCH; UNCLASSIFIED DRUG; TRANSCRIPTOME;

ARTICLE; CARBOHYDRATE METABOLISM; CELL TRANSPORT; CONTROLLED STUDY; DNA REPLICATION; DOWN REGULATION; DROUGHT TOLERANCE; GENE EXPRESSION PROFILING; HIGH THROUGHPUT SEQUENCING; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PLANT LEAF; PLANT METABOLISM; PLANT RESPONSE; PLANT STEM; RICE; ROOT DEVELOPMENT; UPREGULATION; VARIETAS; VEGETATIVE STAGE; ADAPTATION; BIOLOGY; CHROMOSOMAL MAPPING; DROUGHT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC DATABASE; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; ORYZA; PROCEDURES; SIGNAL TRANSDUCTION;

ADAPTATION, BIOLOGICAL; CHROMOSOME MAPPING; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DROUGHTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; MOLECULAR SEQUENCE ANNOTATION; MULTIGENE FAMILY; ORYZA; PLANT LEAVES; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84942195295     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1851-3     Document Type: Article

References (89)

1. Swamy BPM, Kumar A. Sustainable rice yield in water short drought prone environments: conventional and molecular approaches. In: Janeza TS, editor. Irrigation systems and practices in challenging environments. Rijeka: InTech; 2011. p. 149-68.
2. Wopereis MCS, Kropff MJ, Maligaya AR, Tuong TP. Drought-stress responses of two lowland rice cultivars to soil water status. Field Crops Res. 1996;46:21-39.
3. Chandra Babu R. Breeding for drought resistance in rice: an integrated view from physiology to genomics. Electronic J Plant Breed. 2010;1(4):1133-41.
4. Chan CS, Zainudin H, Saad A, Azmi M. Productive water use in aerobic rice cultivation. J Trop Agric Fd Sc. 2012;49(1):117-26.
5. Schimid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, et al. A gene expression map of Arabidopsis thaliana development. Nat Genet. 2005;37:501-6.
6. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, et al. Monitoring expression profiles of rice (Oryza sativa L.) genes under cold, drought and high-salinity stresses, and ABA application using both cDNA microarray and RNA gel blot analyses. Plant Physiol. 2003;133:1755-67.
7. Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J Exp Bot. 2007;58(2):221-7.
8. Swamy BP, Vikram P, Dixit S, Ahmed HU, Kumar A. Meta-analysis of grain yield QTL identified during agricultural drought in grasses showed consensus. BMC Genomics. 2011;12:319.
9. Zhang JZ, Creelman RA, Zhu JK. From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol. 2004;135:615-21.
10. Bartels D, Sunkars R. Drought and salt tolerance in plants. CRC Rev Plant Sci. 2005;24:23-58.
11. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K. Engineering drought tolerance in plants: discovering and tailoring genes unlock the future. Curr Opin Biotechnol. 2006;17:113-22.
12. Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, et al. Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell. 2011;23(12):4185-207.
13. Jones-Rhoades MW, Bartel DP, Bartel B. MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol. 2006;57:19-53.
14. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK. Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol. 2008;8:25.
15. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA. 2008;14(5):836-43.
16. Sunkar R, Zhu JK. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell. 2004;16(8):2001-19.
17. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, et al. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell. 2008;20(8):2238-51.
18. Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, et al. Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun. 2007;354(2):585-90.
19. Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L. Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot. 2010;61(15):4157-68.
20. Xu C, Yang RF, Li WC, Fu FL. Identification of 21 microRNAs in maize and their differential expression under drought stress. Afr J Biotechnol. 2010;9(30):4741-53.
21. Kantar M, Unver T, Budak H. Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genomics. 2010;10(4):493-507.
22. Kantar M, Lucas SJ, Budak H. miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta. 2011;233(3):471-84.
23. Kulcheski FR, de Oliveira LF, Molina LG, Almerão MP, Rodrigues FA, Marcolino J, et al. Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics. 2011;12:307.
24. Lu S, Sun YH, Chiang VL. Stress-responsive microRNAs in Populus. Plant J. 2008;55(1):131-51.
25. Trindade I, Capitao C, Dalmay T, Fevereiro MP, Santos DM. miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta. 2010;231(3):705-16.
26. Arenas-Huertero C, Pérez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, et al. Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol. 2009;70(4):385-401.
27. Shen J, Xie K, Xiong L. Global expression profiling of rice microRNAs by one-tube stem-loop reverse transcription quantitative PCR revealed important roles of microRNAs in abiotic stress responses. Mol Genet Genomics. 2010;284(6):477-88.
28. Barrera-Figueroa BE, Gao L, Wu Z, Zhou X, Zhu J, Jin H, et al. High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biol. 2012;12:132.
29. Lee YS, Shibata Y, Malhotra A, Dutta A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev. 2009;23(22):2639-49.
30. 2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res. 2011;39(7):2821-33.
31. Vaucheret H, Vazquez F, Crété P, Bartel DP. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 2004;18:1187-97.
32. Mallory AC, Vaucheret H. Functions of microRNAs and related small RNAs in plants. Nat Genet. 2006;38(Suppl):S31-6.
33. Colaiacovo M, Bernardo L, Centomani I, Crosatti C, Giusti L, Orrù L, et al. A survey of microRNA length variants contributing to miRNome complexity in peach (Prunus persica L.). Front Plant Sci. 2012;3:165.
34. Wu H, Neilson JR, Kumar P, Manocha M, Shankar P, Sharp PA, et al. MiRNA profiling of naive, effector and memory CD8 T Cells. PLoS ONE. 2007;2(10):e1020.
35. Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, et al. A uniform system for microRNA annotation. RNA. 2003;9(3):277-9.
36. Lan Y, Su N, Shen Y, Zhang R, Wu F, Cheng Z, et al. Identification of novel miRNAs and miRNA expression profiling during grain development in indica rice. BMC Genomics. 2012;13:264.
37. 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.
38. Zhu QH, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, et al. A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res. 2008;18(9):1456-65.
39. Jones-Rhoades MW, Bartel DP. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell. 2004;14(6):787-99.
40. Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, et al. Transcriptome-wide identification of microRNA targets in rice. Plant J. 2010;62(5):742-59.
41. Addo-Quaye C, Miller W, Axtell MJ. CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics. 2009;25(1):130-1.
42. Busse-Wicher M, Wicher KB, Kusche-Gullberg M. The exostosin family: proteins with many functions. Matrix Biol. 2014;35:25-33.
43. Xue T, Wang D, Zhang S, Ehlting J, Ni F, Jakab S, et al. Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genomics. 2008;9:550.
44. Riechmann JL, Meyerowitz EM. The AP2/EREBP family of plant transcription factors. Biol Chem. 1998;379(6):633-46.
45. Herold A, Truant R, Wiegand H, Cullen BR. Determination of the functional domain organization of the importin alpha nuclear import factor. J Cell Biol. 1998;143(2):309-18.
46. Görlich D, Prehn S, Laskey RA, Hartmann E. Isolation of a protein that is essential for the first step of nuclear protein import. Cell. 1994;79(5):767-78.
47. Du P, Wu J, Zhang J, Zhao S, Zheng H, Gao G, et al. Viral infection induces expression of novel phased microRNAs from conserved cellular microRNA precursors. PLoS Pathog. 2011;7(8):e1002176.
48. Chen X, Zhang Z, Liu D, Zhang K, Li A, Mao L. SQUAMOSA promoter-binding protein-like transcription factors: star players for plant growth and development. J Integr Plant Biol. 2010;52(11):946-51.
49. De Lima JC, Loss-Morais G, Margis R. MicroRNAs play critical roles during plant development and in response to abiotic stresses. Genet Mol Biol. 2012;35(4 (suppl)):1069-77.
50. Mallory AC, Bartel DP, Bartel B. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell. 2005;17(5):1360-75.
51. Guilfoyle TJ, Hagen G. Auxin response factors. J Plant Growth Regul. 2001;10:281-91.
52. Ding Y, Tao Y, Zhu C. Emerging roles of microRNAs in the mediation of drought stress response in plants. J Exp Bot. 2013;64(11):3077-86.
53. Cai X, Davis EJ, Ballif J, Liang M, Bushman E, Haroldsen V, et al. Mutant identification and characterization of the laccase gene family in Arabidopsis. J Exp Bot. 2006;57(11):2563-9.
54. Zhang YC, Yu Y, Wang CY, Li ZY, Liu Q, Xu J, et al. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol. 2013;31(9):848-52.
55. de Carvalho MH C. Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav. 2008;3(3):156-65.
56. Abdel-Ghany SE, Pilon M. MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem. 2008;283(23):15932-45.
57. Ren L, Tang G. Identification of sucrose-responsive microRNAs reveals sucrose-regulated copper accumulations in an SPL7-dependent and independent manner in Arabidopsis thaliana. Plant Sci. 2012;187:59-68.
58. Mutum RD, Balyan SC, Kansal S, Agarwal P, Kumar S, Kumar M, et al. Evolution of variety-specific regulatory schema for expression of osa-miR408 in indica rice varieties under drought stress. FEBS J. 2013;280(7):1717-30.
59. Hajyzadeh M, Turktas M, Khawar KM, Unver T. miR408 overexpression causes increased drought tolerance in chickpea. Gene. 2015;555(2):186-93.
60. Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y. Rice microRNA effector complexes and targets. Plant Cell. 2009;21(11):3421-35.
61. Xue LJ, Zhang JJ, Xue HW. Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res. 2009;37(3):916-30.
62. Eldem V, Çelikkol Akçay U, Ozhuner E, Bakir Y, Uranbey S, Unver T. Genome-wide identification of miRNAs responsive to drought in peach (Prunus persica) by high-throughput deep sequencing. PLoS ONE. 2012;7(12):e50298.
63. Wei L, Zhang D, Xiang F, Zhang Z. Differentially expressed miRNAs potentially involved in the regulation of defense mechanism to drought stress in maize seedlings. Int J Plant Sci. 2009;170(8):979-89.
64. Inal B, Türktaş M, Eren H, Ilhan E, Okay S, Atak M, et al. Genome-wide fungal stress responsive miRNA expression in wheat. Planta. 2014;240(6):1287-98.
65. Jia X, Wang WX, Ren L, Chen QJ, Mendu V, Willcut B, et al. Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol. 2009;71(1-2):51-9.
66. Venuprasad R, Lafitte HR, Atlin GN. Response to direct selection for grain yield under drought stress in rice. Crop Sci. 2007;47:285-93.
67. Swamy BP, Ahmed HU, Henry A, Mauleon R, Dixit S, Vikram P, et al. Genetic, physiological, and gene expression analyses reveal that multiple QTL enhance yield of rice mega-variety IR64 under drought. PLoS ONE. 2013;8(5):e62795.
68. Sinclair TR, Ludlow MM. Influence of soil water supply on the plant water balance of four tropical grain legumes. Aust J Plant Physiol. 1986;13(3):329-41.
69. Zhao W, Wang J, He X, Huang X, Jiao Y, Dai M, et al. BGI-RIS: an integrated information resource and comparative analysis workbench for rice genomics. Nucleic Acids Res. 2004;32(Database issue):D377-82.
70. Li R, Li Y, Kristiansen K, Wang J. SOAP: short oligonucleotide alignment program. Bioinformatics. 2008;24(5):713-4.
71. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. MiRBase: tools for microRNA genomics. Nucleic Acids Res. 2008;36(Database issue):D154-8.
72. Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, et al. GenBank. Nucleic Acids Res. 2013;41(Database issue):D36-42.
73. Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, et al. Rfam: updates to the RNA families database. Nucleic Acids Res. 2009;37(Database issue):D136-40.
74. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase update, a database of eukaryotic repetitive elements. Cytogen Genome Res. 2005;110(1-4):462-7.
75. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, et al. The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res. 2007;35(Database issue):D883-7.
76. Audic S, Claverie JM. The significance of digital gene expression profiles. Genome Res. 1997;7(10):986-95.
77. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402-8.
78. Dai X, Zhao PX. psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res. 2011;39(Web Server issue):W155-9.
79. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674-6.
80. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498-504.
81. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27-30.
82. Reyes JL, Chua NH. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J. 2007;49(4):592-606.
83. Liu Q, Zhang YC, Wang CY, Luo YC, Huang QJ, Chen SY, et al. Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Lett. 2009;583(4):723-8.
84. Wu MF, Tian Q, Reed JW. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development. 2006;133(21):4211-8.
85. Wang L, Mai YX, Zhang YC, Luo Q, Yang HQ. MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL6-IV genes regulate shoot branching in Arabidopsis. Mol Plant. 2010;3(5):794-806.
86. Barrera-Figueroa BE, Gao L, Diop NN, Wu ZG, Ehlers JD, Roberts PA, et al. Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol. 2011;11:127.
87. Meng Y, Ma X, Chen D, Wu P, Chen M. MicroRNA-mediated signaling involved in plant root development. Biochem Biophys Res Commun. 2010;393(3):345-9.
88. Bari R, Datt Pant B, Stitt M, Scheible WR. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 2006;141(3):988-99.
89. Hackenberg M, Shi BJ, Gustafson P, Langridge P. Characterization of phosphorus-regulated miR399 and miR827 and their isomirs in barley under phosphorus-sufficient and phosphorus-deficient conditions. BMC Plant Biol. 2013;13:214.