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Regulation mechanism of microRNA in plant response to abiotic stress and breeding

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Abstract

microRNAs (miRNAs) in plants are a class of small RNAs consisting of approximately 21–24 nucleotides. The mature miRNA binds to the target mRNA through the formation of a miRNA-induced silencing complex (MIRISC), and cleaves or inhibits translation, thereby achieving negative regulation of the target gene. Based on miRNA plays an important role in regulating plant gene expression, studies on the prediction, identification, function and evolution of plant miRNAs have been carried out. In addition, many researches prove that miRNAs are also involved in many kinds of abiotic and biotic stress, under abiotic stress, plants can express some miRNA, and act on stress-related target genes, which can make plants adapt to stress in physiological response. In this review, the synthetic pathway and mechanism of plant miRNA are briefly described, and we discuss the biological functions and regulatory mechanisms of miRNAs responding to abiotic stresses including low temperature, salt, drought stress and breeding to lay the foundation for further exploring the mechanism of action of miRNAs in stress resistance of plant. And analyze its utilization prospects in plant stress resistance research.

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(Reproduced with permission from Sun et al. [92])

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(Reproduced with permission from Ding et al. [114])

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References

  1. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    Article  CAS  PubMed  Google Scholar 

  3. Meng L, Yangzhou X (2011) The role of miRNA in regulate physiological functions of plant such as stress responses. Shandong For Sci Technol 2:030

    CAS  Google Scholar 

  4. Reis RS, Eamens AL, Waterhouse PM (2015) Missing pieces in the puzzle of plant microRNAs. Trends Plant Sci 20:721–728

    Article  CAS  PubMed  Google Scholar 

  5. Katiyaragarwal S, Gao S, Viviansmith A, Jin H (2007) A novel class of bacteria-induced small RNAs in Arabidopsis. Gene Dev 21:3123

    Article  CAS  Google Scholar 

  6. Jin H (2008) Endogenous small RNAs and antibacterial immunity in plants. FEBS Lett 582:2679–2684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Budak H, Akpinar BA (2015) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genomics 15:523–531

    Article  CAS  PubMed  Google Scholar 

  8. Kim YK, Kim B, Kim VN (2016) Re-evaluation of the roles of DROSHA, Exportin 5, and DICER in microRNA biogenesis. Proc Natl Acad Sci USA 113:E1881–E1889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. BBA-Gene Regul Mech 1819:137–148

    CAS  Google Scholar 

  10. Li Z, Rana TM (2014) Therapeutic targeting of microRNAs: current status and future challenges. Nat Rev Drug discov 13:622

    Article  CAS  PubMed  Google Scholar 

  11. Kou SJ, Wu XM, Liu Z, Liu YL, Xu Q, Guo WW (2012) 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 31:2151–2163

    Article  CAS  PubMed  Google Scholar 

  12. Jin W, Wu F, Xiao L, Liang GW, Zhen Y, Guo ZK, Guo AG (2012) Microarray-based analysis of tomato miRNA regulated by Botrytis cinerea. J Plant Growth Regul 31:38–46

    Article  CAS  Google Scholar 

  13. Zhao M, Meyers BC, Ca C, Xu W, Ma J (2015) Evolutionary patterns and coevolutionary consequences of MIRNA genes and MicroRNA targets triggered by multiple mechanisms of genomic duplications in soybean. Plant Cell 27:546–562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhao M, Ding H, Zhu JK, Zhang F, Li WX (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190:906–915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hu B, Zhu C. Li F, Tang J, Wang Y, Lin A, Liu L, Che R, Chu C (2011) LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol 156:1101–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321

    Article  CAS  PubMed  Google Scholar 

  17. Xu Z, Zhong S, Li X, Li W, Rothstein SJ, Zhang S, Bi Y, Xie C (2011) Genome-wide identifi cation of microRNAs in response to low nitrate availability in maize leaves and roots. PLoS ONE 6:e28009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lei KJ, Liu H (2016) Research advances in plant regulatory hub miR156 and targeted SPL family. Chem Life 2016:13–20

    Google Scholar 

  19. Bao H, Sun FS, Xu QH, Wang YW (2018) Differential expression of 10 miRNAs in poplar under low nitrogen stress and identification of target genes. Mol Plant Breed 7:1–14

    Google Scholar 

  20. Yang JC, Li M, Xie XZ, Han GL, Sui N, Wang BS (2013) Deficiency of phytochrome B alleviates chilling-induced photoinhibition in rice. Am J Bot 100:1860–1870

    Article  PubMed  Google Scholar 

  21. Cheng S, Yang Z, Wang MJ, Song J, Sui N, Fan H (2014) Salinity improves chilling resistance in Suaeda salsa. Acta Physiol Plant 36:1823–1830

    Article  CAS  Google Scholar 

  22. Sui N (2015) Photoinhibition of Suaeda salsa to chilling stress is related to energy dissipation and water-water cycle. Photosynthetica 53:207–212

    Article  CAS  Google Scholar 

  23. Yang Y, Zhang X, Su Y, Zou J, Wang Z, Xu L, Que Y (2017) miRNA alteration is an important mechanism in sugarcane response to low-temperature environment. BMC Genomics 18:833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chen L, Zhang Y, Ren Y, Xu J, Zhang Z, Wang Y (2012) Genome-wide identification of cold-responsive and new microRNAs in Populus tomentosa by high-throughput sequencing. Biochem Biophys Res Commun 417:892–896

    Article  CAS  PubMed  Google Scholar 

  25. Zeng X, Xu Y, Jiang J, Zhang F, Ma L, Wu D, Wang Y, Sun W (2018) Identification of cold stress responsive microRNAs in two winter turnip rape (Brassica rapa L.) by high throughput sequencing. BMC Plant Biol 18:52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Yang CH, Li DY, Mao DH, Liu X, Ji CJ, Li XB, Zhao XF, Cheng ZK, Chen CY, Zhu LH (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environ 36:2207–2218

    Article  CAS  PubMed  Google Scholar 

  27. Gupta OP, Meena NL, Sharma I, Sharma P (2014) Differential regulation of microRNAs in response to osmotic, salt and cold stresses in wheat. Mol Biol Rep 41:4623–4629

    Article  CAS  PubMed  Google Scholar 

  28. An FM, Chan MT (2012) Transcriptome-wide characterization of miRNA-directed and non-miRNA-directed endonucleolytic cleavage using degradome analysis under low ambient temperature in Phalaenopsis aphrodite subsp. formosana. Plant Cell Physiol 53:1737

    Article  CAS  PubMed  Google Scholar 

  29. Lee H, Yoo SJ, Lee JH, Kim W, Yoo SK, Fitzgerald H, Carrington JC, Ahn JH (2010) Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res 38:3081–3093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Dong C, Song Y, Tian M, Zhang D (2015) Methylation of miRNA genes in the response to temperature stress in Populus simonii. Front Plant Sci 6:921

    Google Scholar 

  31. Xin M, Yu W, Yao Y, Ni Z, Sun Q (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10:123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Giacomelli JI, Weigel D, Chan RL, Manavella PA (2012) Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytol 195:766–773

    Article  CAS  PubMed  Google Scholar 

  33. Hivrale V, Zheng Y, Puli COR, Jagadeeswaran G, Gowdu K, Kakani VG, Barakat A, Sunkar R (2015) Characterization of drought- and heat-responsive microRNAs in switchgrass. Plant Sci 242:214–223

    Article  CAS  PubMed  Google Scholar 

  34. Sui N, Han GL (2014) Salt-induced photoinhibition of PSII is alleviated in halophyte Thellungiella halophila, by increases of unsaturated fatty acids in membrane lipids. Acta Physiol Plant 36:983–992

    Article  CAS  Google Scholar 

  35. Liu SS, Wang WQ, Li M, Wan SB, Sui N (2017) Antioxidants and unsaturated fatty acids are involved in salt tolerance in peanut. Acta Physiol Plant 39:207

    Article  CAS  Google Scholar 

  36. Feng ZT, Deng YQ, Fan H, Sun QJ, Sui N, Wang BS (2014) Effects of NaCl stress on the growth and photosynthetic characteristics of Ulmus pumila, L. seedlings in sand culture. Photosynthetica 52:313–320

    Article  CAS  Google Scholar 

  37. Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik I, Goltsev V, Ladle JR (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102

    Article  CAS  Google Scholar 

  38. Sui N, Yang Z, Liu M, Wang BS (2015) Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves. BMC Genomics 16:534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Cheng TL, Chen JH, Zhang JB, Shi SQ, Zhou YW, Lu L, Wang PK, Jiang ZP, Yang JC, Zhang SG, Shi JS (2015) Physiological and proteomic analyses of leaves from the halophyte Tangut Nitraria reveals diverse response pathways critical for high salinity tolerance. Front Plant Sci 6:30

    PubMed  PubMed Central  Google Scholar 

  40. Li X, Liu Y, Chen M, Song YP, Song J, Wang BS (2012) Relationships between ion and chlorophyll accumulation in seeds and adaptation to saline environments in Suaeda salsa populations. Plant Biosyst 146:142–149

    Article  Google Scholar 

  41. Zhang S, Song J, Wang H, Feng G (2010) Effect of salinity on seed germination, ion content and photosynthesis of cotyledons in halophytes or xerophyte growing in Central Asia. J Plant Ecol 3:259–267

    Article  Google Scholar 

  42. Cui F, Sui N, Duan G, Liu YY, Han Y, Liu SS, Wan SB, Li GW (2018) Identification of metabolites and transcripts involved in salt stress and recovery in peanut. Front Plant Sci 9:217

    Article  PubMed  PubMed Central  Google Scholar 

  43. Dinneny JR (2015) Traversing organizational scales in plant salt-stress responses. Curr Opin Plant Biol 23:70–75

    Article  CAS  PubMed  Google Scholar 

  44. Liu J, Cai H, Liu Y, Zhu YM, Ji W, Bai X (2015) A study on physiological characteristics and cmparison of salt resistance of two Medicago sativa at the seedling stage. Acta Pratacult Sin 22:250–256

    CAS  Google Scholar 

  45. Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK (2011) Additive effects of Na+ and Cl ions on barley growth under salinity stress. J Exp Bot 62:2189–2203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hazman M, Hause B, Eiche E, Nick P, Riemann M (2015) Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked to an increased ROS-scavenging activity. J Exp Bot 66:3339–3352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Tao LI, Liu RJ, Xin-Hua HE, Wang BS (2012) Enhancement of superoxide dismutase and catalase activities and salt tolerance of euhalophyte Suaeda salsa L. by mycorrhizal fungus Glomus mosseae. Pedosphere 22:217–224

    Article  Google Scholar 

  48. Song J, Zhou J, Zhao W, Xu HL, Wang FX, Xu YG, Wang L, Tian CY (2016) Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa. Plant Spec Biol 31:19–28

    Article  Google Scholar 

  49. Zhou JC, Fu TT, Sui N, Gou JR, Feng G, Fan JL, Song J (2016) The role of salinity in seed maturation of the euhalophyte Suaeda salsa. Plant Biosyst 150:83–90

    Article  Google Scholar 

  50. Guo Y, Jia W, Song J, Wang D, Chen M, Wang BS (2012) Thellungilla halophila is more adaptive to salinity than Arabidopsis thaliana at stages of seed germination and seedling establishment. Acta Physiol Plant 34:1287–1294

    Article  CAS  Google Scholar 

  51. Vu TS, Zhang DW, Xiao WH, Chi CY, Xing Y, Fu DD, Yuan ZN (2015) Mechanisms of combined effects of salt and alkaline stresses on seed germination and seedlings of Melilotus Officinalis (Fabaceae) in Northeast of China. Pak J Bot 47:1603–1611

    Google Scholar 

  52. Yao S, Chen S, Zhao J, Xu DS, Lan HY, Zhang FC (2010) Effect of three salts on germination and seedling survival of dimorphic seeds of Chenopodium album. Botany 88:821–828

    Article  CAS  Google Scholar 

  53. Wang F, Xu YG, Wang S, Shi W, Liu R, Feng G, Song J (2015) Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiol Biochem 95:41–48

    Article  CAS  PubMed  Google Scholar 

  54. Xu Y, Liu R, Sui N, Shi WW, Wang L, Tian CY, Song J (2016) Changes in endogenous hormones and seed-coat phenolics during seed storage of two Suaeda salsa populations. Aust J Bot 64:325–332

    Article  CAS  Google Scholar 

  55. Guo J, Suo S, Wang BS (2015) Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa. Seed Sci Res 25:335–344

    Article  CAS  Google Scholar 

  56. Guo JR, Li YD, Han G, Song J, Wang BS (2018) NaCl markedly improved the reproductive capacity of the euhalophyte Suaeda salsa. Funct Plant Biol 45:350–361

    Article  CAS  PubMed  Google Scholar 

  57. Liu QQ, Liu RR, Ma YC, Song J (2018) Physiological and molecular evidence for Na+ and Cl exclusion in the roots of two Suaeda salsa populations. Aquat Bot 146:1–7

    Article  CAS  Google Scholar 

  58. Zhang T, Song J, Fan J, Feng G (2015) Effects of saline-waterlogging and dryness/moist alternations on seed germination of halophyte and xerophyte. Plant Spec Biol 30:231–236

    Article  Google Scholar 

  59. Ruiz KB, Biondi S, Martinez EA, Orsini F, Antognoni F, Jacobsen SE (2016) Quinoa-a model crop for understanding salt-tolerance mechanisms in halophytes. Plant Biosyst 150:357–371

    Article  Google Scholar 

  60. Han N, Shao Q, Bao H, Wang BS (2010) Cloning and characterization of a Ca2+/H+, antiporter from halophyte Suaeda salsa L. Plant Mol Biol Rep 29:449–457

    Article  CAS  Google Scholar 

  61. Feng ZT, Deng YQ, Zhang SC, Liang X, Yuan F, Hao JL, Zhang JC, Sun SF, Wang BS (2015) K(+) accumulation in the cytoplasm and nucleus of the salt gland cells of Limonium bicolor accompanies increased rates of salt secretion under NaCl treatment using NanoSIMS. Plant Sci 238:286–296

    Article  CAS  PubMed  Google Scholar 

  62. Song J, Shi W, Liu R, Xu YG, Sui N, Zhou JC, Feng G (2017) The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity. Plant Spec Biol 32:107–114

    Article  Google Scholar 

  63. Shaheen HL, Iqbal M, Azeem M, Shahbaz M, Shahbaz M (2016) K-priming positively modulates growth and nutrient status of salt-stressed cotton (Gossypium hirsutum) seedlings. Arch Agron Soil Sci 62:759–768

    Article  CAS  Google Scholar 

  64. Dai LY, Zhang LJ, Jiang SJ, Yin KD (2014) Saline and alkaline stress genotypic tolerance in sweet sorghum is linked to sodium distribution. Acta Agric Scand 64:471–481

    CAS  Google Scholar 

  65. Guo P, Wei HX, Zhang WJ, Bao Y (2016) Physiological responses of alfalfa to high-level salt stress: root ion flux and stomatal characteristics. Int J Agric Biol 18:125–133

    Article  CAS  Google Scholar 

  66. Zhao KF, Song J, Fan H, Zhou S, Zhao M (2010) Growth response to ionic and osmotic stress of NaCl in salt-tolerant and salt-sensitive maize. J Integr Plant Biol 52:468–475

    Article  CAS  PubMed  Google Scholar 

  67. Tang X, Mu X, Shao H, Wang H, Brestic M (2015) Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Crit Rev Biotechnol 35(4):425–437

    Article  CAS  PubMed  Google Scholar 

  68. Nxele X, Klein A, Ndimba BK (2017) Drought and salinity stress alters ROS accumulation, water retention, and osmolyte content in sorghum plants. S Afr J Bot 108:261–266

    Article  CAS  Google Scholar 

  69. Song J, Wang BS (2014) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115:541–553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Yuan F, Chen M, Yang J, Ling BY, Wang BS (2014) A system for the transformation and regeneration of the recretohalophyte Limonium bicolor. In Vitro Cell Dev 50:610–617

    Article  Google Scholar 

  71. Yuan F, Leng B, Wang BS (2016) Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt? Front Plant Sci 7:977

    PubMed  PubMed Central  Google Scholar 

  72. Feng ZT, Sun QJ, Deng YQ, Sun SF, Zhang JG, Wang BS (2014) Study on pathway and characteristics of ion secretion of salt glands of Limonium bicolor. Acta Physiol Plant 36:2729–2741

    Article  CAS  Google Scholar 

  73. Leng BY, Yuan F, Dong XX, Wang J, Wang BS (2018) Distribution pattern and salt excretion rate of salt glands in two recretohalophyte species of Limonium, (Plumbaginaceae). S Afr J Bot 115:74–80

    Article  CAS  Google Scholar 

  74. Yuan F, Lyu MJ, Leng BY, Zheng GY, Feng ZT, Li PH, Zhu XG, Wang BS (2015) Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation. Plant Cell Environ 38:1637–1657

    Article  CAS  PubMed  Google Scholar 

  75. Yuan F, Chen M, Yang J, Song J, Wang BS (2015) The optimal dosage of60co gamma irradiation for obtaining salt gland mutants of exo-recretohalophyte Limonium bicolor (Bunge) O. Kuntze. Pak J Bot 47:71–76

    CAS  Google Scholar 

  76. Yuan F, Lyu MJA, Leng BY, Zhu XG, Wang BS (2016) The transcriptome of NaCl-treated Limonium bicolor, leaves reveals the genes controlling salt secretion of salt gland. Plant Mol Biol 91:241–256

    Article  CAS  PubMed  Google Scholar 

  77. Zhang H, Zhang L, Gao B, Fan H, Jin J, Botella MA, Jiang L, Lin J (2011) Golgi apparatus-localized synaptotagmin 2 is required for unconventional secretion in Arabidopsis. PLoS ONE 6:e26477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Han G, Wang M, Yuan F, Sui N, Song J, Wang BS (2014) The CCCH zinc finger protein gene AtZFP1, improves salt resistance in Arabidopsis thaliana. Plant Mol Biol 86:237–253

    Article  CAS  PubMed  Google Scholar 

  79. Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Qi YC, Liu WQ, Qiu LY, Zhang SM, Ma L, Zhang H (2010) Overexpression of glutathione S-transferase gene increases salt tolerance of arabidopsis. Russ J Plant Physiol 57:233–240

    Article  CAS  Google Scholar 

  81. Qi YC, Wang FF, Zhang H, Liu WQ (2010) Overexpression of Suadea salsa S-adenosylmethionine synthetase gene promotes salt tolerance in transgenic tobacco. Acta Physiol Plant 32:263–269

    Article  CAS  Google Scholar 

  82. Sun Z, Qi X, Wang Z, Li P, Wu C, Zhang H, Zhao Y (2013) Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol Biochem 69:82–89

    Article  CAS  PubMed  Google Scholar 

  83. Chen M, Song J, Wang BS (2010) NaCl increases the activity of the plasma membrane H+-ATPase in C3 halophyte Suaeda salsa callus. Acta Physiol Plant 32:27–36

    Article  CAS  Google Scholar 

  84. Li K, Pang CH, Ding F, Sui N, Feng ZT, Wang BS (2012) Overexpression of Suaeda salsa, stroma ascorbate peroxidase in Arabidopsis, chloroplasts enhances salt tolerance of plants. S Afr J Bot 78:235–245

    Article  CAS  Google Scholar 

  85. Shao Q, Han N, Ding T, Zhou F, Wang BS (2014) SsHKT1;1 is a potassium transporter of the C3 halophyte Suaeda salsa that is involved in salt tolerance. Funct Plant Biol 41:790–802

    Article  CAS  PubMed  Google Scholar 

  86. Sui N, Tian S, Wang W, Wang M, Fan H (2017) Overexpression of glycerol-3-phosphate acyltransferase from Suaeda salsa improves salt tolerance in arabidopsis. Front Plant Sci 8:1337

    Article  PubMed  PubMed Central  Google Scholar 

  87. Yang Z, Wang Y, Wei X, Zhao X, Wang B (2017) Transcription profiles of genes related to hormonal regulations under salt stress in sweet sorghum. Plant Mol Biol Rep 35:1–14

    Article  CAS  Google Scholar 

  88. Shen X, Wang Z, Song X, Xu J, Jiang C, Zhao Y (2014) Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis. Plant Mol Biol 86:303–317

    Article  CAS  PubMed  Google Scholar 

  89. Ding F, Chen M, Sui N, Wang BS (2010) Ca2+ significantly enhanced development and salt-secretion rate of salt glands of Limonium bicolor under NaCl treatment. S Afr J Bot 76:95–101

    Article  CAS  Google Scholar 

  90. Han N, Lan W, He X, Shao Q, Wang BS (2011) Expression of a Suaeda salsa, vacuolar H+/Ca2+, transporter gene in arabidopsis, contributes to physiological changes in salinity. Plant Mol Biol Rep 30:470–477

    Article  CAS  Google Scholar 

  91. Kumar V, Khare T, Shriram V, Wani SH (2018) Plant small RNAs: the essential epigenetic regulators of gene expression for salt-stress responses and tolerance. Plant Cell Rep 37:1–15

    Article  CAS  Google Scholar 

  92. Sun X, Xu L, Wang Y, Yu R, Zhu X (2015) Identification of novel and salt-responsive miRNAs to explore miRNA-mediated regulatory network of salt stress response in radish (Raphanus sativus L.). BMC Genomics 16:197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Mondal TK, Panda AK, Rawal HC, Sharma TR (2018) Discovery of microRNA-target modules of African rice (Oryza glaberrima) under salinity stress. Sci Rep 8:570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38

    Article  CAS  PubMed  Google Scholar 

  95. Li B, Duan H, Li J, Deng XW, Yin W, Xia X (2013) Global identification of miRNAs and targets in Populus euphratica under salt stress. Plant Mol Biol 81:525–539

    Article  CAS  PubMed  Google Scholar 

  96. Yin Z, Li Y, Yu J, Liu Y, Li C, Han X, Shen F (2012) Difference in miRNA expression profiles between two cotton cultivars with distinct salt sensitivity. Mol Biol Rep 39:4961–4970

    Article  CAS  PubMed  Google Scholar 

  97. Gao S, Yang L, Zeng HQ, Zhou ZS, Yang ZM, Li H, Sun D, Xie F, Zhang B (2016) A cotton miRNA is involved in regulation of plant response to salt stress. Sci Rep 6:19736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Wang M, Wang Q, Zhang B (2013) Response of miRNAs and their targets to salt and drought stresses in cotton (Gossypium hirsutum L.). Gene 530:26–32

    Article  CAS  PubMed  Google Scholar 

  99. Bai Q, Wang X, Chen X, Shi G, Liu Z, Guo C (2018) Wheat miRNA TaemiR408 acts as an essential mediator in plant tolerance to Pi deprivation and salt stress via modulating stress-associated physiological processes. Front Plant Sci 9:499

    Article  PubMed  PubMed Central  Google Scholar 

  100. Peng T, Wen H, Zhao Y, Wang B, Jin Y, Sun HZ, Zhao QZ (2018) Identification and expressions analysis of rice miRNA related to salt and drought stresses. Acta Agric Boreali-Sinica 8:2114

    Google Scholar 

  101. Luo M, Gao Z, Li H, Li Q, Zhang C, Xu W, Song S, Ma C, Wang S (2018) Selection of reference genes for miRNA qRT-PCR under abiotic stress in grapevine. Sci Rep 8:4444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Jia X, Wang WX, Ren L, Chen QJ, Mendu V, Willcut B, Dinkins R, Tang X, Tang G (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71:51–59

    Article  CAS  PubMed  Google Scholar 

  103. Nagaraju M, Reddy PS, Kumar SA, Kumara AS, Kumar A, Suravajhala P, Alia A, Srivastavab RK, Raoa DM (2018) Genome-wide in silico, analysis of dehydrins in Sorghum bicolor, Setaria italica, and Zea mays, and quantitative analysis of dehydrin gene expressions under abiotic stresses in Sorghum bicolor. Plant Gene 13:64–75

    Article  CAS  Google Scholar 

  104. Bouzroud S, Gouiaa S, Hu N, Bernadac A, Mila I, Bendaou N, Smouni A, Bouzayen M, Zouine M (2018) Auxin response factors (ARFs) are potential mediators of auxin action in tomato response to biotic and abiotic stress (Solanum lycopersicum). PLoS ONE 13:e0193517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Mondal TK, Ganie SA (2014) Identification and characterization of salt responsive miRNA-SSR markers in rice (Oryza sativa). Gene 535:204–209

    Article  CAS  PubMed  Google Scholar 

  106. Zheng Y, Liao CC, Zhao SS, Wang CW, Guo Y (2017) The glycosyltransferase QUA1 regulates chloroplast-associated calcium signaling during salt and drought stress in arabidopsis. Plant Cell Physiol 58:329–341

    CAS  PubMed  Google Scholar 

  107. Guo YY, Tian SS, Liu SS, Wang WQ, Sui N (2018) Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress. Photosynthetica 2018:1–12

    Google Scholar 

  108. Hou L, Liu W, Li Z, Huang C, Fang XL, Wang Q, Liu X (2014) Identification and expression analysis of genes responsive to drought stress in peanut. Russ J Plant Physiol 61:842–852

    Article  CAS  Google Scholar 

  109. Liu J, Zhang F, Zhou JJ, Chen F, Wang BS, Xie XZ (2012) Phytochrome B control of total leaf area and stomatal density affects drought tolerance in rice. Plant Mol Biol 78:289–300

    Article  CAS  PubMed  Google Scholar 

  110. Tang GY, Shao FX, Xu PL, Shan L, Liu ZJ (2017) Overexpression of a peanut NAC gene, AhNAC4, confers enhanced drought tolerance in tobacco. Russ J Plant Physiol 64:525–535

    Article  CAS  Google Scholar 

  111. Zhang D, Tong J, He X, Xu Z, Xu L, Wei P, Huang Y, Brestic M, Ma H, Shao H (2016) A novel soybean intrinsic protein gene, GmTIP2;3, involved in responding to osmotic stress. Front Plant Sci 6:1237

    PubMed  PubMed Central  Google Scholar 

  112. Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, Xiao F, Ye Z (2011) Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol Lett 33:403–409

    Article  CAS  PubMed  Google Scholar 

  113. Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66:1749–1761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Ding Y, Tao Y, Zhu C (2013) Emerging roles of microRNAs in the mediation of drought stress response in plants. J Exp Bot 64:3077

    Article  CAS  PubMed  Google Scholar 

  115. Li WX, Oono YJ, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Ni Z, Hu Z, Jiang Q, Zhang H (2012) Overexpression of gma-MIR394a confers tolerance to drought in transgenic Arabidopsis thaliana. Biochem Biophys Res Commun 427:330–335

    Article  CAS  PubMed  Google Scholar 

  117. Zhou M, Li D, Li Z, Hu Q, Yang C, Zhu LH, Luo H (2014) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Signal Behav 161:1375–1391

    Google Scholar 

  118. Zhang F, Luo Y, Zhang M, Zhou Y, Chen HP, Hu BL, Xie JK (2018) Identification and characterization of drought stress- responsive novel microRNAs in dongxiang wild rice. Rice Sci 25:175–184

    Article  Google Scholar 

  119. Zhang J, Zhang H, Srivastava AK, Pan Y, Bai J, Fang J, Shi H, Zhu JK (2018) Knock-down of rice microRNA166 confers drought resistance by causing leaf rolling and altering stem xylem development. Plant Physiol 176:2082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Liu M, Yu H, Zhao G, Huang Q, Lu Y, Ouyang B (2018) Identification of drought-responsive microRNAs in tomato using high-throughput sequencing. Funct Integr Genomics 18:67–78

    Article  CAS  PubMed  Google Scholar 

  121. Magwanga RO, Lu P, Kirungu JN, Diouf L, Dong Q, Hu Y, Cai X, Xu Y, Hou Y, Zhou Z, Wang X, Wang K, Liu F (2018) GBS mapping and analysis of genes conserved between Gossypium tomentosum and Gossypium hirsutum cotton cultivars that respond to drought stress at the seedling stage of the BC2 F2 generation. Int J Mol Sci 9:32

    Google Scholar 

  122. Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233:471–484

    Article  CAS  PubMed  Google Scholar 

  123. Akdogan G, Tufekci ED, Uranbey S, Unver T (2016) miRNA-based drought regulation in wheat. Funct Integr Genomics 16:221–233

    Article  CAS  PubMed  Google Scholar 

  124. Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genomics 10:493–507

    Article  CAS  PubMed  Google Scholar 

  125. Wang T, Lei C, Zhao M, Tian Q, Zhang WH (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Shuai P, Liang D, Zhang Z, Yin W, Xia X (2013) Identification of drought-responsive and novel Populus trichocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis. BMC Genomics 14:233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Wei L, Zhang D, Fang X, Zhang Z (2009) Differentially expressed miRNAs potentially involved in the regulation of defense mechanism to drought stress in maize seedlings. Int J Plant Sci 170:979–989

    Article  CAS  Google Scholar 

  128. Ferreira TH, Gentile A, Vilela RD, Costa GG, Dias LI, Endres L, Menossi M (2012) microRNAs associated with drought response in the bioenergy crop sugarcane (Saccharum spp.). PLoS ONE 7:e46703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo LJ (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168

    Article  CAS  PubMed  Google Scholar 

  130. Barrera-Figueroa BE, Gao L, Diop NN, Wu Z, Ehlers JD, Roberts PA, Close TJ, Zhu JK, Liu R (2011) Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol 11:127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Frazier TP, Sun G, Burklew CE, Zhang B (2011) Salt and drought stresses induce the aberrant expression of microRNA genes in tobacco. Mol Biotechnol 49:159

    Article  CAS  PubMed  Google Scholar 

  132. Chen Q, Li M, Zhang Z, Tie W, Chen X, Jin L, Zhai N, Zheng Q, Zhang J, Wang R, Xu G, Zhang H, Liu P, Zhou H (2017) Integrated mRNA and microRNA analysis identifies genes and small miRNA molecules associated with transcriptional and post-transcriptional-level responses to both drought stress and re-watering treatment in tobacco. BMC Genomics 18:62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Xie F Jr, Taki SC, He FA, Liu Q, Zhang H B (2014) High-throughput deep sequencing shows that microRNAs play important roles in switchgrass responses to drought and salinity stress. Plant Biotechnol J 12:354–366

    Article  CAS  PubMed  Google Scholar 

  134. Hwang EW, Shin SJ, Yu BK, Byun MO, Kwon HB (2011) miR171 family members are involved in drought response in Solanum tuberosum. J Plant Biol 54:43–48

    Article  CAS  Google Scholar 

  135. Budak H, Akpinar A (2011) Dehydration stress-responsive miRNA in Brachypodium distachyon: evident by genome-wide screening of microRNAs expression. Omics 15:791–799

    Article  CAS  PubMed  Google Scholar 

  136. Li B, Qin Y, Hui D, Yin W, Xia X (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Akpinar BA, 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 15:587–598

    Article  CAS  PubMed  Google Scholar 

  138. Zhang N, Yang J, Wang Z, Wen Y, Wang J, He W, Liu B, Si H, Wang D (2014) Identification of novel and conserved microRNAs related to drought stress in potato by deep sequencing. PLoS ONE 9:e95489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Eldem V, Akçay U, Ozhuner E, Bakır Y, Uranbey S, Unver T (2012) Genome-wide identification of miRNAs responsive to drought in peach (Prunus persica) by high-throughput deep sequencing. PLoS ONE 7:e50298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Mutum RD, Balyan SC, Kansal S, Agarwal P, Kumar S, Kumar M, Raghuvanshi S (2013) Evolution of variety-specific regulatory schema for expression of osa-miR408 in indica rice varieties under drought stress. Febs J 280:1717–1730

    Article  CAS  PubMed  Google Scholar 

  141. Shen J, Xing T, Yuan H, Liu Z, Jin Z, Zhang L, Pei Y (2013) Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions. PLoS ONE 8:e77047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Chen X, Yang RF, Li WC et al (2010) Identification of 21 microRNAs in maize and their differential expression under drought stress. Afr J Biotechnol 9:4741–4753

    Google Scholar 

  143. Zhang J, Long Y, Xue M, Xiao XG, Pei XW (2017) Identification of microRNAs in response to drought in common wild rice (Oryza rufipogon Griff.) shoots and roots. PLoS ONE 12:e0170330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Xie F, Wang Q, Sun R, Zhang B (2015) Deep sequencing reveals important roles of microRNAs in response to drought and salinity stress in cotton. J Exp Bot 66:789–804

    Article  CAS  PubMed  Google Scholar 

  145. Parizotto EA, Dunoyer P, Rahm N, Himber C, Voinnet O (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Gene Dev 18:2237–2242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Wei Y, Chen Z, Chen G, Xiong L, Wu C (2011) Study of overexpressing miRNA 167a to regulate the architecture in Oryza sativa. Mol Plant Breed 9:390–396

    CAS  Google Scholar 

  147. Li J, Guo G, Guo W et al (2012) miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biol 12:220–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Yao L, Zhang N, Yang J et al (2016) Prediction of miRNA164 target genes and construction of amiRNA164 expression vector of potato. Mol Plant Breed 14:1482–1490

    Google Scholar 

  149. Guo HS, Xie Q, Fei JF, Chua NH (2005) microRNA directs mRNA cleavage of the transcription factor NAC1 todownregu late auxin signa ls for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Zhang Y, Wang W, Chen J, Liu J, Xia M, Niu Y, Shen F (2015) Identification and characterization of miRN and their targets associated with the Verticillium wilt resistance in cotton. Mol Plant Breed 13:156–164

    CAS  Google Scholar 

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Acknowledgements

We are grateful for financial support from Shandong Provincial Natural Science Foundation (ZR2016JL028), Major Program of Shandong Provincial Natural Science Foundation (2017C03), Shandong Provincial Natural Science Foundation (ZR2015EM007).

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XS wrote the manuscript. NS and LL modified the article. All authors read and approved the final manuscript.

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Correspondence to Na Sui.

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Sun, X., Lin, L. & Sui, N. Regulation mechanism of microRNA in plant response to abiotic stress and breeding. Mol Biol Rep 46, 1447–1457 (2019). https://doi.org/10.1007/s11033-018-4511-2

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