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Plant Growth Regulation

, Volume 87, Issue 1, pp 139–148 | Cite as

Comparative analysis of microRNAs and their targets in the roots of two cultivars with contrasting salt tolerance in rice (Oryza sativa L.)

  • Xi Huang
  • Jiejie Feng
  • Rui Wang
  • Hongsheng Zhang
  • Ji HuangEmail author
Original paper
  • 63 Downloads

Abstract

MicroRNAs (miRNAs) are small, non-coding RNAs that play essential roles in plant growth, development, and stress responses. Rice cultivars IR26 (sub. xian) and Jiucaiqing (sub. geng) exhibit significant salt tolerance differences during their growth. This study performed a genome-wide discovery of salt responsive miRNAs in rice roots, and in particular, the differentially expressed miRNAs between two cultivars. Specifically- and commonly-regulated miRNAs involved in salt stress between two cultivars were identified. The genes targeted by these miRNAs were involved in multiple biological processes including transcriptional regulation and response to stimulus. This preliminary characterization provides a framework for future analysis of miRNAs and their roles in rice salt stress response and describes the possible mechanisms for miRNA mediated salt tolerance by comparative analysis of miRNAs and their targets in salt-resistant and -sensitive cultivars.

Keywords

Oryza sativa Salt MicroRNA High-throughput sequencing Root 

Notes

Acknowledgements

This work was supported by the National Science Foundation of China (Grant No. 31571627), the Fundamental Research Funds for the Central Universities (Grant No. KYZ201804) and the Jiangsu Collaborative Innovation Center for Modern Crop Production (Grant No. JCICMCP).

Author Contributions

XH performed the most of experiments and analysis and drafted the manuscript. JF and RW participated in data analysis. JH and HZ projected design and supervision.

Supplementary material

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Supplementary material 4—Fig. S1 Length distribution of mappable reads in different samples (JPG 257 KB)
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Supplementary material 5—Fig. S2 Length distribution of counts of sRNAs in different samples (JPG 183 KB)
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Supplementary material 6—Fig. S3 Length distribution of counts of unique sRNAs in different samples (JPG 169 KB)
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Supplementary material 10—Fig. S4 miRNAs predicted by degradome sequencing in two cultivars (JPG 69 KB)
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References

  1. Addo-Quaye C, Miller W, Axtell MJ (2009a) CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 25:130–131.  https://doi.org/10.1093/bioinformatics/btn604 CrossRefGoogle Scholar
  2. Addo-Quaye C, Snyder JA, Park YB, Li YF, Sunkar R, Axtell MJ (2009b) Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome. RNA 15:2112–2121.  https://doi.org/10.1261/rna.1774909 CrossRefGoogle Scholar
  3. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741.  https://doi.org/10.1105/tpc.016238 CrossRefGoogle Scholar
  4. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116:281–297.  https://doi.org/10.1016/S0092-8674(04)00045-5 CrossRefGoogle Scholar
  5. Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102:11928–11933.  https://doi.org/10.1073/pnas.0505461102 CrossRefGoogle Scholar
  6. Beauclair L, Yu A, Bouche N (2010) microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J 62:454–462.  https://doi.org/10.1111/j.1365-313X.2010.04162.x CrossRefGoogle Scholar
  7. Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291.  https://doi.org/10.1016/j.cell.2005.11.035 CrossRefGoogle Scholar
  8. Bressan R, Bohnert H, Zhu JK (2009) Abiotic stress tolerance: from gene discovery in model organisms to crop improvement. Mol Plant 2:1–2.  https://doi.org/10.1093/mp/ssn097 CrossRefGoogle Scholar
  9. Chen C et al (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:e179.  https://doi.org/10.1093/nar/gni178 CrossRefGoogle Scholar
  10. Chen XY, Yang Y, Ran LP, Dong ZD, Zhang EJ, Yu XR, Xiong F (2017) Novel insights into miRNA regulation of storage protein biosynthesis during wheat caryopsis development under drought stress. Front Plant Sci 8:1707.  https://doi.org/10.3389/fpls.2017.01707 CrossRefGoogle Scholar
  11. Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332.  https://doi.org/10.1111/j.1365-3040.2007.01643.x CrossRefGoogle Scholar
  12. Ding YF, Zhu C (2009) The role of microRNAs in copper and cadmium homeostasis. Biochem Biophys Res Commun 386:6–10.  https://doi.org/10.1016/j.bbrc.2009.05.137 CrossRefGoogle Scholar
  13. Dong ZH, Zhang JH, Zhu QZ, Zhao LF, Sui SX, Li ZS, Zhang YL, Wang H, Tian DL, Zhao YK (2017) Identification of microRNAs involved in drought stress responses in early-maturing cotton by high-throughput sequencing. Genes Genom.  https://doi.org/10.1007/s13258-017-0637-1 Google Scholar
  14. Dunoyer P, Himber C, Voinnet O (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat Genet 37:1356–1360.  https://doi.org/10.1038/ng1675 CrossRefGoogle Scholar
  15. Feng J, Liu S, Wang M, Lang Q, Jin C (2014) Identification of microRNAs and their targets in tomato infected with Cucumber mosaic virus based on deep sequencing. Planta 240:1335–1352.  https://doi.org/10.1007/s00425-014-2158-3 CrossRefGoogle Scholar
  16. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105:803–808.  https://doi.org/10.1073/pnas.0709559105 CrossRefGoogle Scholar
  17. He XF, Fang YY, Feng L, Guo HS (2008) Characterization of conserved and novel microRNAs and their targets, including a TuMV-induced TIR-NBS-LRR class R gene-derived novel miRNA in Brassica. FEBS Lett 582:2445–2452.  https://doi.org/10.1016/j.febslet.2008.06.011 CrossRefGoogle Scholar
  18. Hwang E-W, Shin S-J, Yu B-K, Byun M-O, Kwon H-B (2010) miR171 family members are involved in drought response in Solanum tuberosum. J Plant Biol 54:43–48.  https://doi.org/10.1007/s12374-010-9141-8 CrossRefGoogle Scholar
  19. Jagadeeswaran G et al (2009) Cloning and characterization of small RNAs from Medicago truncatula reveals four novel legume-specific microRNA families. New Phytol 184:85–98.  https://doi.org/10.1111/j.1469-8137.2009.02915.x CrossRefGoogle Scholar
  20. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799.  https://doi.org/10.1016/j.molcel.2004.05.027 CrossRefGoogle Scholar
  21. Jung HJ, Kang H (2007) Expression and functional analyses of microRNA417 in Arabidopsis thaliana under stress conditions. Plant Physiol Biochem PPB/Societe francaise de physiologie vegetale 45:805–811.  https://doi.org/10.1016/j.plaphy.2007.07.015 CrossRefGoogle Scholar
  22. 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.  https://doi.org/10.1111/j.1365-313X.2008.03690.x CrossRefGoogle Scholar
  23. Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758.  https://doi.org/10.1073/pnas.0403115101 CrossRefGoogle Scholar
  24. Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746.  https://doi.org/10.1104/pp.108.116269 CrossRefGoogle Scholar
  25. Liu W et al (2014) Analysis of miRNAs and their targets during adventitious shoot organogenesis of Acacia. crassicarpa. PLoS ONE 9:e93438.  https://doi.org/10.1371/journal.pone.0093438 CrossRefGoogle Scholar
  26. Liu MM, Yu HY, Zhao GJ, Huang QF, Lu YG, Ouyang B (2017) Profiling of drought-responsive microRNA and mRNA in tomato using high-throughput sequencing. BMC Genom 18:481.  https://doi.org/10.1186/s12864-017-3869-1 CrossRefGoogle Scholar
  27. Lotfi A, Pervaiz T, Jiu ST, Faghihi F, Jahanbakhshian Z, Khorzoghi EG, Fang JG, Mahdi SS (2017) Role of microRNAs and their target genes in salinity response in plants. Plant Growth Regul 82:377–390.  https://doi.org/10.1007/s10725-017-0277-0 CrossRefGoogle Scholar
  28. Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive MicroRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203.  https://doi.org/10.1105/tpc.105.033456 CrossRefGoogle Scholar
  29. Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55:131–151.  https://doi.org/10.1111/j.1365-313X.2008.03497.x CrossRefGoogle Scholar
  30. Ma MJ et al (2011) Discovery of DNA viruses in wild-caught mosquitoes using small RNA high throughput sequencing. PLoS ONE 6:e24758.  https://doi.org/10.1371/journal.pone.0024758.t001 CrossRefGoogle Scholar
  31. Ma X, Shao C, Wang H, Jin Y, Meng Y (2013) Construction of small RNA-mediated gene regulatory networks in the roots of rice (Oryza sativa). BMC Genom 14:510.  https://doi.org/10.1186/1471-2164-14-510 CrossRefGoogle Scholar
  32. Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738.  https://doi.org/10.1111/j.1365-313X.2007.03363.x CrossRefGoogle Scholar
  33. Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J.  https://doi.org/10.1111/j.1365-313X.2010.04208.x Google Scholar
  34. Shen J, Xie K, Xiong L (2010) 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 Genom MGG 284:477–488.  https://doi.org/10.1007/s00438-010-0581-0 CrossRefGoogle Scholar
  35. Sun SJ et al (2010a) Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J Exp Bot 61:2807–2818.  https://doi.org/10.1093/jxb/erq120 CrossRefGoogle Scholar
  36. Sun X, Fu T, Chen N, Guo J, Ma J, Zou M, Lu C, Zhang L (2010b) The stromal chloroplast Deg7 protease participates in the repair of photosystem II after photoinhibition in Arabidopsis. Plant Physiol 152:1263–1273.  https://doi.org/10.1104/pp.109.150722 CrossRefGoogle Scholar
  37. Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065.  https://doi.org/10.1105/tpc.106.041673 CrossRefGoogle Scholar
  38. Tuteja N, Tarique M, Banu MS, Ahmad M, Tuteja R (2014) Pisum sativum p68 DEAD-box protein is ATP-dependent RNA helicase and unique bipolar DNA helicase. Plant Mol Biol 85:639–651.  https://doi.org/10.1007/s11103-014-0209-6 CrossRefGoogle Scholar
  39. Wang Z et al (2012a) QTL analysis of Na+ and K+ concentrations in roots and shoots under different levels of NaCl stress in rice (Oryza sativa L.). PLoS ONE 7:e51202.  https://doi.org/10.1371/journal.pone.0051202 CrossRefGoogle Scholar
  40. Wang Z, Cheng J, Chen Z, Huang J, Bao Y, Wang J, Zhang H (2012b) Identification of QTLs with main, epistatic and QTL x environment interaction effects for salt tolerance in rice seedlings under different salinity conditions. TAG Theor Appl Genet Theoretische. und angewandte Genetik 125:807–815.  https://doi.org/10.1007/s00122-012-1873-z CrossRefGoogle Scholar
  41. Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y (2009) Rice MicroRNA effector complexes and targets. Plant Cell 21:3421–3435.  https://doi.org/10.1105/tpc.109.070938 CrossRefGoogle Scholar
  42. Xie Z et al (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:E104  https://doi.org/10.1371/journal.pbio.0020104 CrossRefGoogle Scholar
  43. Xu X, Bai H, Liu C, Chen E, Chen Q, Zhuang J, Shen B (2014) Genome-wide analysis of microRNAs and their target genes related to leaf senescence of rice. PLoS ONE 9:e114313.  https://doi.org/10.1371/journal.pone.0114313 CrossRefGoogle Scholar
  44. Xue LJ, Zhang JJ, Xue HW (2009) Characterization and expression profiles of miRNAs in rice seeds. Nucleic acids Res 37:916–930.  https://doi.org/10.1093/nar/gkn998 CrossRefGoogle Scholar
  45. Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361  https://doi.org/10.1105/tpc.108.060137 CrossRefGoogle Scholar
  46. Yang J, Liu X, Xu B, Zhao N, Yang X, Zhang M (2013) Identification of miRNAs and their targets using high-throughput sequencing and degradome analysis in cytoplasmic male-sterile and its maintainer fertile lines of Brassica juncea. BMC Genom 14:15CrossRefGoogle Scholar
  47. Zeng XC, Xu YZ, Jiang JJ, Zhang FQ, Ma L, Wu DW, Wang YP, Sun WC (2018) Identification of cold stress responsive microRNAs in two winter turnip rape (Brassica rapa L.) by high throughput sequencing. BMC Plant Biol 18:52.  https://doi.org/10.1186/s12870-018-1242-4 CrossRefGoogle Scholar
  48. Zhang BH (2014) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66:1749–1761.  https://doi.org/10.1093/jxb/erv013 CrossRefGoogle Scholar
  49. Zhang X et al (2011) Arabidopsis argonaute 2 regulates innate immunity via miRNA393(*)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 42:356–366.  https://doi.org/10.1016/j.molcel.2011.04.010 CrossRefGoogle Scholar
  50. Zhang Y et al (2014) Identification and characterization of cold responsive microRNAs in tea plant (Camellia sinensis) and their targets using high-throughput sequencing and degradome analysis. BMC Plant Biol 14:18CrossRefGoogle Scholar
  51. Zhao B et al (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590  https://doi.org/10.1016/j.bbrc.2007.01.022 CrossRefGoogle Scholar
  52. Zhao GJ, Yu HY, Liu MM, Lu YE, Ouyang B (2017) Identification of salt-stress responsive microRNAs from Solanum lycopersicum and Solanum pimpinellifolium. Plant Growth Regul 83:129–140.  https://doi.org/10.1007/s10725-017-0289-9 CrossRefGoogle Scholar
  53. Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012) Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 35:86–99.  https://doi.org/10.1111/j.1365-3040.2011.02418.x CrossRefGoogle Scholar
  54. Zhu J-K (2002) Salt And drought stress signal transduction. plants. Ann Rev Plant Biol 53:247–273.  https://doi.org/10.1146/annurev.arplant.53.091401.143329 CrossRefGoogle Scholar
  55. Zhuang Y, Zhou XH, Liu J (2014) Conserved miRNAs and their response to salt stress in wild eggplant Solanum linnaeanum roots. Int J Mol Sci 15:839–849.  https://doi.org/10.3390/ijms15010839 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Xi Huang
    • 1
  • Jiejie Feng
    • 1
  • Rui Wang
    • 1
  • Hongsheng Zhang
    • 1
  • Ji Huang
    • 1
    Email author
  1. 1.State Key Laboratory of Crop Genetics and Germplasm EnhancementNanjing Agricultural UniversityNanjingChina

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