MicroRNA as a Tool for Mitigating Abiotic Stress in Rice (Oryza sativa L.)

  • Deepu Pandita
  • Shabir Hussain Wani


Oryza sativa, a model plant species is one of the most imperative food crops of the globe which feeds over two billion people including Indians. Plants are subjected to multiple stresses in chorus leading to colossal changes in the molecular landscape of a cell. Being sessile rice crop is persistently exposed to various abiotic stresses with devastating effect on its survival and productivity. Abiotic stresses can change growth, development and productivity of plants. Rice has developed extremely complex molecular machineries to sense a range of stress signals and bring forth an exact response to minimize the harm. Augmentation of rice productivity can significantly elevate the economic status of India. Recently, non-protein–coding microRNAs have acknowledged tremendous attention due to their value in negative gene regulation. In plants, despite regulating developmental, physiological and biological processes like immune responses, cell differentiation and fate determination, microRNAs have also been allied with varied biotic and abiotic stresses. Modification of miRNA regulatory landscape can significantly modify the product of a stress response which can consequently prove to be essential in understanding the molecular architecture of plant stress response repertoire and the cross-talk between diverse stress responses. The miRNA-mediated post-transcriptional gene silencing is one of the methods to establish plant abiotic stress tolerance. This review provides an up-date on microRNAs, role of miRNA on abiotic stress response in rice, rice miRNA-directed regulatory network and the genetic engineering perspectives of miRNAs applications in rice tolerance to various abiotic stress environments.


Oryza sativa miRNA history miRNA biogenesis Drought Salinity Cold stress Heat stress Oxidative stress Cadmium stress Post-transcriptional gene regulation 



Dr. Saurabh Raghuvanshi is acknowledged for introducing me to the world of micro RNAs while working under his guidance as IASc-INSA-NASI Summer Research Teacher Fellow in 2014 at Laboratory of Structural Genomics & Bioinformatics, Department of Plant Molecular Biology, Delhi University, South Campus, New Delhi, India.


  1. Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellins regulated microRNA. Development 131:3357–3365PubMedCrossRefPubMedCentralGoogle Scholar
  2. Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117–2129PubMedPubMedCentralCrossRefGoogle Scholar
  3. Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X et al (2003a) A uniform system for microRNAs annotation. RNA 9:277–279PubMedPubMedCentralCrossRefGoogle Scholar
  4. Ambros V, Lee RC, Lavanway A, Williams PT, Jewell D (2003b) MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr Biol 13:807–818PubMedCrossRefPubMedCentralGoogle Scholar
  5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal trans- duction. Annu Rev Plant Biol 55:373–399PubMedCrossRefPubMedCentralGoogle Scholar
  6. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  7. Barrera-Figueroa BE, Gao L, Wu Z, Zhou X, Zhu J, Jin H, Liu R, Zhu JK (2012) High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biol 12:132PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  10. Ben Chaabane S, Liu R, Chinnusamy V, Kwon Y, Park JH, Kim SY, Zhu JK, Yang SW, Lee BH (2013) STA1, an Arabidopsis pre-mRNA processing factor 6 homolog, is a new player involved in miRNA biogenesis. Nucleic Acids Res 41:1984–1997CrossRefGoogle Scholar
  11. Bielewicz D, Kalak M, Kalyna M, Windels D, Barta A, Vazquez F, Jarmolowski A (2013) Introns of plant pri-miRNAs enhance miRNA biogenesis. EMBO Rep 14:622–628PubMedPubMedCentralCrossRefGoogle Scholar
  12. Blumwald E, Grover A (2006) Salt tolerance. In: Halford NG (ed) Plant biotechnology: current and future uses of genetically modified crops. Wiley, England, pp 206–224CrossRefGoogle Scholar
  13. Bologna NG, Mateos JL, Bresso EG, Palatnik JF (2009) A loopto ‐ base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159. EMBO J 28:3646–3656PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bologna NG, Schapire AL, Palatnik JF (2013a) Processing of plant microRNA precursors. Brief Funct Genomics 12:37–45PubMedCrossRefPubMedCentralGoogle Scholar
  15. Bologna NG, Schpire AL, Zhai J, Chorostecki U, Boisbouvier J, Meyers BC, Palatnik JF (2013b) Multiple RNA recognition patterns during microRNA biogenesis in plants. Genome Res 23:1675–1689PubMedPubMedCentralCrossRefGoogle Scholar
  16. Breakfield NW, Corcoran DL, Petricka JJ, Shen J, Sae-Seaw J, Rubio-Somoza I, Weigel D, Ohler U, Benfey PN (2012) High resolution experimental and computational profiling of tissue-specific known and novel miRNAs in Arabidopsis. Genome Res 22:163–176PubMedPubMedCentralCrossRefGoogle Scholar
  17. Cai X, Davis EJ, Ballif J, Liang M, Bushman E, Haroldsen V et al (2006) Mutant identification and characterization of the laccase gene family in Arabidopsis. J Exp Bot 57(11):2563–2569PubMedCrossRefPubMedCentralGoogle Scholar
  18. Canto-Pastor A, Molla-Morales E, Ernst W, Dahl J, Zhai Y, Yan B, Meyers C, Shanklin J, Martienssen R (2015) Efficient transformation and artificial miRNA gene silencing in Lemna minor. Plant Biol 17:59–65PubMedCrossRefPubMedCentralGoogle Scholar
  19. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560CrossRefGoogle Scholar
  20. Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025PubMedCrossRefPubMedCentralGoogle Scholar
  21. Chen X (2010) Plant microRNAs at a glance. Semin Cell Dev Biol 21:781PubMedCrossRefPubMedCentralGoogle Scholar
  22. Chen ZH, Bao ML, Sun YZ, Yang YJ, Xu XH, Wang JH, Zhu MY (2011) Regulation of auxin response by miR393-targeted transport inhibitor response protein 1 is involved in normal development in Arabidopsis. Plant Mol Biol 77:619–629PubMedCrossRefPubMedCentralGoogle Scholar
  23. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451PubMedCrossRefPubMedCentralGoogle Scholar
  24. Chinnusamy V, Zhu J-K, Sunkar R (2010) Gene regulation during cold stress acclimation in plants. Methods Mol Biol 639:39–55Google Scholar
  25. Cui N, Sun X, Sun M, Jia B, Duanmu H, Lv D, Duan X, Zhu Y (2015) Overexpression of OsmiR156k leads to reduced tolerance to cold stress in rice (Oryza sativa). Mol Breed 35:214CrossRefGoogle Scholar
  26. Devi SJSR, Madhav MS, Kumar GR, Goel AK, Umakanth B, Jahnavi B, Viraktamath BC (2013) Identification of abiotic stress miRNA transcription factor binding motifs (TFBMs) in rice. Gene 531:15–22PubMedCrossRefPubMedCentralGoogle Scholar
  27. Devos K (2005) Updating the “Crop Circle”. Curr Opin Plant Biol 8:155–162PubMedCrossRefPubMedCentralGoogle Scholar
  28. Ding YF, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62:3563–3573PubMedPubMedCentralCrossRefGoogle Scholar
  29. Ding Y, Qu A, Gong S, Huang S, Lv B, Zhu C (2013) Molecular identification and analysis of Cd-responsive MicroRNAs in rice. J Agric Food Chem 61:11668–11675PubMedCrossRefPubMedCentralGoogle Scholar
  30. Dong CH et al (2009) Disruption of Arabidopsis CHY1 reveals an important role of metabolic status in plant cold stress signaling. Mol Plant 2:59PubMedPubMedCentralCrossRefGoogle Scholar
  31. Eamens AL, Smith NA, Curtin SJ, Wang M, Waterhouse PM (2009) The Arabidopsis thaliana double-stranded RNA binding protein DRB1 directs guide strand selection from microRNAs duplexes. RNA 15:2219–2235PubMedPubMedCentralCrossRefGoogle Scholar
  32. Eamens AL, McHale M, Waterhouse PM (2014) The use of artificial microRNA technology to control gene expression in Arabidopsis thaliana. Arabidopsis Protoc Methods Mol Biol 1062:211–224CrossRefGoogle Scholar
  33. Ferdous J, Hussain SS, Shi B‐J (2015) Role of microRNAs in plant drought tolerance. Plant Biotechnol J 13:293–305PubMedPubMedCentralCrossRefGoogle Scholar
  34. Gao P, Bai X, Yang L, Lv D, Li Y, Cai H, Ji W, Guo D, Zhu Y (2010) Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta 231:991–1001CrossRefGoogle Scholar
  35. Gao P, Bai X, Yang L, Lv D, Pan X, Li Y, Cai H, Ji W, Chen Q, Zhu Y (2011) Osa- MIR393: a salinity-and alkaline stress-related microRNA gene. Mol Biol Rep 38:237–242PubMedCrossRefPubMedCentralGoogle Scholar
  36. Goldgur Y et al (2007) 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 Physiol 143:617PubMedPubMedCentralCrossRefGoogle Scholar
  37. Gong H, Hu WW, Jiao Y, Pua EC (2005) Molecular characterization of Phi-class mustard (Brassica juncea) glutathione S-transferase gene in Arabidopsis thaliana by 5′-deletion analysis of its promoter. Plant Cell Rep 24:439–447PubMedCrossRefPubMedCentralGoogle Scholar
  38. Grad Y, Aach J, Hayes GD, Reinhart BJ, Church GM, Ruvkun G, Kim J (2003) Computational and experimental identification of C. elegans microRNAs. Mol Cell 11:1253–1263PubMedCrossRefPubMedCentralGoogle Scholar
  39. Grover A, Minhas D (2000) Towards the production of abiotic stress tolerant transgenic rice plants: issues, progress and future research needs. Proc Natl Acad Sci U S A 1:13–32Google Scholar
  40. Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ecophysiology and responses of plants under salt stress. Springer, New York, NY, pp 25–87CrossRefGoogle Scholar
  41. Hawker NP, Bowman JL (2004) Roles for class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Physiol 135:2261–2270PubMedPubMedCentralCrossRefGoogle Scholar
  42. Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E, Mitsuhara I, Meshi T, Ishikawa M (2010) In vitro assembly of plant RNAinduced silencing complexes facilitated by molecular chaperone HSP90. Mol Cell 39:282–291PubMedCrossRefPubMedCentralGoogle Scholar
  43. Iki T, Yoshikawa M, Meshi T, Ishikawa M (2012) Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J 31:267–278PubMedCrossRefPubMedCentralGoogle Scholar
  44. Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207PubMedPubMedCentralCrossRefGoogle Scholar
  45. Jian X, Zhang L, Li G, Zhang L, Wang X, Cao X, Fang X, Zha FC (2010) Identification of novel stress-regulated microRNAs from Oryza sativa L. Genomics 95:47–50PubMedCrossRefPubMedCentralGoogle Scholar
  46. Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544PubMedCrossRefPubMedCentralGoogle Scholar
  47. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799PubMedPubMedCentralCrossRefGoogle Scholar
  48. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53PubMedCrossRefPubMedCentralGoogle Scholar
  49. Jouannet V, Moreno AB, Elmayan T, Vaucheret H, Crespi MD, Maizel A (2012) Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for tasiRNA biogenesis. EMBO J 31:1704–1713PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115:727–738PubMedCrossRefPubMedCentralGoogle Scholar
  51. Khraiwesh B, Zhu J, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148PubMedCrossRefPubMedCentralGoogle Scholar
  52. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385PubMedCrossRefPubMedCentralGoogle Scholar
  53. Kim YJ, Zheng B, Yu Y, Won SY, Mo B, Chen X (2011) The role of Mediator in small and long noncoding RNA production in Arabidopsis thaliana. EMBO J 30:814–822PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lai EC (2003) MicroRNAs: runts of the genome assert themselves. Curr Biol 13:R925–R936PubMedCrossRefGoogle Scholar
  55. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843–854PubMedCrossRefPubMedCentralGoogle Scholar
  56. Li B, Qin Y, Duan H, Yin W, Xia X (2011a) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779PubMedPubMedCentralCrossRefGoogle Scholar
  57. Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B, Li H, Dong Y, Yin H, Wang N, Yang J, Liu X, Wang Y, Wu J, Li X (2011b) Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol 11:170PubMedPubMedCentralCrossRefGoogle Scholar
  58. Lim LP, Lau NC, Weinstein EG, Abdelhakim A, Yekta S, Rhoades MW, Burge CB, Bartel DP (2003) The microRNAs of Caenorhabditis elegans. Genes Dev 17:991–1008CrossRefGoogle Scholar
  59. Liu Q, Chen YQ (2010) A new mechanism in plant engineering: the potential roles of microRNAs in molecular breeding for crop improvement. Biotechnol Adv 28:301–307PubMedCrossRefPubMedCentralGoogle Scholar
  60. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14(5):836–843PubMedPubMedCentralCrossRefGoogle Scholar
  61. Liu Q, Zhang YC, Wang CY, Luo YC, Huang QJ, Chen SY, Chen YQ (2009) Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Lett 583:723–728PubMedCrossRefPubMedCentralGoogle Scholar
  62. Lu C, Jeong DH, Kulkarni K, Pillay M, Nobuta K, German R, Green PJ (2008) Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci U S A 105:4951–4956PubMedPubMedCentralCrossRefGoogle Scholar
  63. Lv DK, Bai X, Li Y, Ding XD, Ge Y, Cai H, Ji W, Wu N, Zhu YM (2010) Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459(1–2):39–47PubMedCrossRefPubMedCentralGoogle Scholar
  64. Ma X, Xin Z, Wang Z et al (2015) Identification and comparative analysis of differentially expressed miRNAs in leaves of two wheat (Triticum aestivum L.) genotypes during dehydration stress. BMC Plant Biol 15:21PubMedPubMedCentralCrossRefGoogle Scholar
  65. Macovei A, Tuteja N (2012) microRNAs targeting DEAD-box helicases are involved in salinity stress response in rice (Oryza sativa L.). BMC Plant Biol 12:183PubMedPubMedCentralCrossRefGoogle Scholar
  66. Macovei A, Gill SS, Tuteja N (2012) microRNAs as promising tools for improving stress tolerance in rice. Plant Signal Behav 7:1296–1301PubMedPubMedCentralCrossRefGoogle Scholar
  67. Macrae IJ, Zhou K, Li F, Repic A, Brooks AN, Cande WZ, Adams PD, Doudna JA (2006) Structural basis for double-stranded RNA processing by Dicer. Science 311:195–198PubMedCrossRefPubMedCentralGoogle Scholar
  68. Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet 38(Suppl):S31–S36PubMedCrossRefPubMedCentralGoogle Scholar
  69. Mane SP, Vasquez-Robinet C, Sioson AA, Heath LS, Grene R (2007) Early PLD {alpha}-mediated events in response to progressive drought stress in Arabidopsis: a transcriptome analysis. J Exp Bot 58:241PubMedCrossRefPubMedCentralGoogle Scholar
  70. Mangrauthia SK, Bhogireddy S, Agarwal S, Prasanth VV, Voleti SR, Neelamraju S, Subrahmanyam D (2017) Genome-wide changes in microRNA expression during short and prolonged heat stress and recovery in contrasting rice cultivars. J Exp Bot 68(9):2399–2412PubMedPubMedCentralCrossRefGoogle Scholar
  71. Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature low temperature and oxidative stresses. Plant Physiol Biochem 47(9):785–795PubMedCrossRefPubMedCentralGoogle Scholar
  72. Mittal D, Madhyastha DA, Grover A (2012) Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. PLoS One 7(7):e40899PubMedPubMedCentralCrossRefGoogle Scholar
  73. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefPubMedCentralGoogle Scholar
  74. Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337PubMedPubMedCentralCrossRefGoogle Scholar
  75. Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549PubMedCrossRefPubMedCentralGoogle Scholar
  76. Munns R (2010) Approaches to identifying genes for salinity tolerance and the importance of timescale. Methods Mol Biol 639:25–38PubMedCrossRefPubMedCentralGoogle Scholar
  77. Mutum RD, Balyan SC, Kansal S, Agarwal P, Kumar S, Kumar M et al (2013) Evolution of variety-specific regulatory schema for expression of osa-miR408 in indica rice varieties under drought stress. FEBS J 280:1717–1730PubMedCrossRefPubMedCentralGoogle Scholar
  78. Mutum RD, Kumar S, Balyan S, Kansal S, Mathur S, Raghuvanshi S (2016) Identification of novel miRNAs from drought tolerant rice variety Nagina 22. Sci Rep 6:30786. Scholar
  79. Ni FT, Chu LY, Shao HB, Liu ZH (2009) Gene expression and regulation of higher plants under soil water stress. Curr Genomics 10:269–280PubMedPubMedCentralCrossRefGoogle Scholar
  80. Nozawa M, Miura S, Nei M (2012) Origins and evolution of microRNA genes in plant species. Genome Biol Evol 4:230–239PubMedPubMedCentralCrossRefGoogle Scholar
  81. Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690PubMedCrossRefPubMedCentralGoogle Scholar
  82. Pan J, Huang D, Guo Z, Kuang Z, Zhang H, Xie X, Ma Z, Gao S, Lerdau MT, Chu C, Li L (2018) Overexpression of microRNA408 enhances photosynthesis, growth, and seed yield in diverse plants. J Integr Plant Biol. Scholar
  83. Pandita D (2018a) Plant miRNAs: micro structure and macro character. Res Rev J Agric Allied Sci 7(1):83–84Google Scholar
  84. Pandita D (2018b) RNA interference: what and why? J Genet Mol Biol 2(1):1–3Google Scholar
  85. Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A 101:9903–9908PubMedPubMedCentralCrossRefGoogle Scholar
  86. Pérez-Quintero AL, López C (2010) Artificial microRNAs and their applications in plant molecular biology. Agronomia Colombiana 28:373–381Google Scholar
  87. Raffaele S, Mongrand S, Gamas P, Niebel A, Ott T (2007) Genome-wide annotation of remorins, a plant-specific protein family: evolutionary and functional perspectives. Plant Physiol 145:593PubMedPubMedCentralCrossRefGoogle Scholar
  88. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626PubMedPubMedCentralCrossRefGoogle Scholar
  89. Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–2399PubMedPubMedCentralCrossRefGoogle Scholar
  90. Sailaja B, Voleti SR, Subrahmanyam D, Sarla N, Prasanth V, Bhadana VP, Mangrauthia SK (2014) Prediction and expression analysis of miRNAs associated with heat stress in Oryza sativa. Rice Sci 21(1):3–12CrossRefGoogle Scholar
  91. Sanan-Mishra N, Kumar V, Sopory SK, Mukherjee SK (2009) Cloning and validation of novel miRNA from basmati rice indicates cross talk between abiotic and biotic stresses. Mol Genet Genomics 282:463–474PubMedCrossRefPubMedCentralGoogle Scholar
  92. Sasaki T, Burr B (2000) International rice genome sequencing project: the effort to completely sequence the rice genome. Curr Opin Plant Biol 3:138–141PubMedCrossRefPubMedCentralGoogle Scholar
  93. Sasaki T, Matsumoto T, Yamamoto K, Sakata K, Baba T, Katayose Y, Wu JZ, Niimura Y, Cheng ZK, Nagamura Y et al (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316PubMedCrossRefPubMedCentralGoogle Scholar
  94. Schommer C, Palatnik JF, Aggarwal P, Chetelat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:e230PubMedPubMedCentralCrossRefGoogle Scholar
  95. Sharma N, Tripathi A, Sanan-Mishra N (2015) Profiling the expression domains of a rice-specific microRNA under stress. Front Plant Sci 6:333PubMedPubMedCentralCrossRefGoogle Scholar
  96. Shukla LI, Chinnusamy V, Sunkar R (2008) The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim Biophys Acta 11:743–748CrossRefGoogle Scholar
  97. Singh KB, Foley RC, O ate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436PubMedCrossRefPubMedCentralGoogle Scholar
  98. Singh P, Kaloudas D, Raines CA (2008) Expression analysis of the Arabidopsis CP12 gene family suggests novel roles for these proteins in roots and floral tissues. J Exp Bot 59:3975–3985PubMedPubMedCentralCrossRefGoogle Scholar
  99. Song L, Axtell MJ, Fedoroff NV (2010) RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Curr Biol 20:37–41PubMedCrossRefPubMedCentralGoogle Scholar
  100. Sun TP, Kamiya Y (1994) The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. Plant Cell Online 6:1509Google Scholar
  101. Sun M, Yang J, Cai X, Shen Y, Cui N, Zhu Y, Jia B, Sun X (2018) The opposite roles of OsmiR408 in cold and drought stress responses in Oryza sativa. Mol Breed 38:120CrossRefGoogle Scholar
  102. Sunkar R (2010) MicroRNAs with macro-effects on plant stress responses. Semin Cell Dev Biol 21:805–811PubMedCrossRefPubMedCentralGoogle Scholar
  103. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019PubMedPubMedCentralCrossRefGoogle Scholar
  104. Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411PubMedPubMedCentralCrossRefGoogle Scholar
  105. Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203PubMedCrossRefPubMedCentralGoogle Scholar
  106. Taylor RS, Tarver JE, Hiscock SJ, Donoghue PCJ (2014) Evolutionary history of plant microRNAs. Trends Plant Sci 19:175–182PubMedCrossRefPubMedCentralGoogle Scholar
  107. The Rice Chromosome 10 Sequencing Consortium (2003) In-depth view of structure, activity, and evolution of rice chromosome 10. Science 300:1566–1569CrossRefGoogle Scholar
  108. Tiwari M, Sharma D, Trivedi PK (2014) Artificial microRNAs mediated gene silencing in plants: progress and perspectives. Plant Mol Biol 86:1–18PubMedCrossRefPubMedCentralGoogle Scholar
  109. Van Dyck L, Pearce DA, Sherman F (1994) PIM1 encodes a mitochondrial ATP dependent protease that is required for mitochondrial function in the yeast Saccharomyces cerevisiae. J Biol Chem 269:238PubMedPubMedCentralGoogle Scholar
  110. Wang JF, Zhou H, Chen YQ, Luo QJ, Qu LH (2004) Identification of 20 microRNAs from Oryza sativa. Nucleic Acids Res 32:1688–1695PubMedPubMedCentralCrossRefGoogle Scholar
  111. Wang X, Yang Y, Yu C, Zhou J, Cheng Y, Yan C et al (2010) A highly efficient method for construction of rice artificial MicroRNA vectors. Mol Biotechnol 46:211–218PubMedCrossRefPubMedCentralGoogle Scholar
  112. Wang L, Song X, Gu L (2013) NOT2 proteins promote polymerase II-dependent transcription and interact with multiple microRNAs biogenesis factors in Arabidopsis. Plant Cell 25:715–727PubMedPubMedCentralCrossRefGoogle Scholar
  113. Wang S-t, X-l S, Hoshino Y, Yu Y, Jia B et al (2014) MicroRNA319 positively regulates cold tolerance by targeting OsPCF6 and OsTCP21 in rice (Oryza sativa L.). PLoS One 9(3):e91357PubMedPubMedCentralCrossRefGoogle Scholar
  114. Wen-Wen K, Hong-Bo W, Jing L (2014) Biogenesis of plant microRNAs. J Northeast Agric Univ 21:84–96Google Scholar
  115. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475PubMedCrossRefPubMedCentralGoogle Scholar
  116. Xia K, Wang R, Ou X, Fang Z, Tian C, Duan J (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One 7:e30039PubMedPubMedCentralCrossRefGoogle Scholar
  117. Xie K, Shen J, Hou X, Yao J, Li X, Xiao J, Xiong L (2012) Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiol 158:1382–1394PubMedPubMedCentralCrossRefGoogle Scholar
  118. Xie F, Stewart CN Jr, Taki FA, He Q, Liu H, Zhang B (2014) High-throughput deep sequencing shows that microRNAs play important roles in switch grass responses to drought and salinity stress. Plant Biotechnol J 12:354–366PubMedCrossRefPubMedCentralGoogle Scholar
  119. Xie M, Zhang S, Yu B (2015) microRNA biogenesis, degradation and activity in plants. Cell Mol Life Sci 72:87–99PubMedCrossRefPubMedCentralGoogle Scholar
  120. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803PubMedCrossRefPubMedCentralGoogle Scholar
  121. Yang CH, Li DY, Mao DH, Liu X, Ji CJ et al (2013a) Over expression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environ 36:2207–2218PubMedPubMedCentralCrossRefGoogle Scholar
  122. Yang Z, Huang D, Tang W, Zheng Y, Liang K et al (2013b) Mapping of quantitative trait loci underlying cold tolerance in rice seedlings via high-throughput sequencing of pooled extremes. PLoS One 8(7):e68433PubMedPubMedCentralCrossRefGoogle Scholar
  123. Ye C, Fukai S, Godwin I, Reinke R, Snell P, Schiller J, Basnayake J (2009) Cold tolerance in rice varieties at different growth stages. Crop Pasture Sci 60:328–338CrossRefGoogle Scholar
  124. Yi X, Zhang Z, Ling Y, Xu W, Su Z (2015) PNRD: a plant noncoding RNA database. Nucleic Acids Res 43(D1):D982–D989PubMedPubMedCentralCrossRefGoogle Scholar
  125. Yoshida S (1981) Growth and development of the rice plant. Fundamentals of rice crop science, vol 1. International Rice Research Institute, Los Banos, Philippines, pp 1–36Google Scholar
  126. Yoshikawa M, Iki T, Tsutsui Y, Miyashita K, Poethig RS, Habu Y, Ishikawa M (2013) 3’ fragment of miR173-programmed RISC-cleaved RNA is protected from degradation in a complex with RISC and SGS3. Proc Natl Acad Sci U S A 110:4117–4122PubMedPubMedCentralCrossRefGoogle Scholar
  127. Yu J, Hu SN, Wang J, Wong GKS, Li SG, Liu B, Deng YJ, Dai L, Zhou Y, Zhang XQ et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp indica). Science 296:79–92PubMedCrossRefPubMedCentralGoogle Scholar
  128. Yu J, Wang J, Lin W, Li SG, Li H, Zhou J, Ni PX, Dong W, Hu SN, Zeng CQ et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:266–281CrossRefGoogle Scholar
  129. Yue E, Liu Z, Li C et al (2017) Over expression of miR529a confers enhanced resistance to oxidative stress in rice (Oryza sativa L.). Plant Cell Rep 36:1171PubMedCrossRefPubMedCentralGoogle Scholar
  130. Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66:1749–1761PubMedPubMedCentralCrossRefGoogle Scholar
  131. Zhang B, Wang Q (2015) MicroRNA-based biotechnology for plant improvement. J Cell Physiol 230:1–15PubMedCrossRefPubMedCentralGoogle Scholar
  132. Zhang BH, Pan XP, Wang QL, Cobb GP, Anderson TA (2005) Identification and characterization of new plant microRNAs using EST analysis. Cell Res 15:336–360PubMedCrossRefPubMedCentralGoogle Scholar
  133. Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289:3–16PubMedCrossRefPubMedCentralGoogle Scholar
  134. Zhang YC, Yu Y, Wang CY et al (2013a) Overexpression of microRNAs OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 31:848–852PubMedCrossRefPubMedCentralGoogle Scholar
  135. Zhang S, Yue Y, Sheng L, Wu Y, Fan G, Li A, Hu X, Shang Guan M, Wei C (2013b) PASmiR: a literature curated database for miRNA molecular regulation in plant response to abiotic stress. BMC Plant Biol 13:33PubMedPubMedCentralCrossRefGoogle Scholar
  136. Zhang JP, Yu Y, Feng YZ, Zhou YF, Zhang F, Yang YW, Lei MQ, Zhang YC, Chen YQ (2017) MiR408 regulates grain yield and photosynthesis via a phytocyanin protein. Plant Physiol 175(3):1175–1185. Scholar
  137. Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought- induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590PubMedCrossRefPubMedCentralGoogle Scholar
  138. Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:29PubMedPubMedCentralCrossRefGoogle Scholar
  139. Zhao X, Zhang H, Li L (2013) Identification and analysis of the proximal promoters of microRNA genes in Arabidopsis. Genomics 101:187–194PubMedCrossRefPubMedCentralGoogle Scholar
  140. Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1779:780–788PubMedCrossRefPubMedCentralGoogle Scholar
  141. Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168PubMedCrossRefPubMedCentralGoogle Scholar
  142. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefGoogle Scholar
  143. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedPubMedCentralCrossRefGoogle Scholar
  144. Zou J, Liu AL, Chen XB, Zhou XY, Gao GF, Wang WF, Zhang XW (2009) Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol 166(8):851–861PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Government Department of School EducationJammuIndia
  2. 2.Mountain Research Centre for Field CropsKhudwaniIndia

Personalised recommendations