Plant Molecular Biology

, Volume 71, Issue 1–2, pp 51–59

Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populustremula and Arabidopsisthaliana

  • Xiaoyun Jia
  • Wang-Xia Wang
  • Ligang Ren
  • Qi-Jun Chen
  • Venugopal Mendu
  • Benjamin Willcut
  • Randy Dinkins
  • Xiaoqing Tang
  • Guiliang Tang


MicroRNAs (miRNAs) are endogenous small RNAs of ~22 nucleotides (nt) that play a key role in down regulation of gene expression at the post-transcriptional level in plants and animals. Various studies have identified numerous miRNAs that were either up regulated or down regulated upon stress treatment. Here, we sought to understand the temporal regulation of miRNAs in different plant species under abscisic acid (ABA) and salt (NaCl) stress. Our results showed that the regulation of miR398 in response to ABA and salt stress was more dynamic in plants than previously reported. In poplars, miR398 was first induced upon 3–4 h of ABA or salt stress. However, this induction declined after 48 h and finally accumulated again over a prolonged stress (72 h). We referred to this kind of regulation as dynamic regulation. In contrast, such dynamic regulation of miR398 under salt stress was completely absent in Arabidopsis, in which miR398 was steadily and unidirectionally suppressed. Interestingly, ABA treatment caused a deviate dynamic regulation of miR398 in Arabidopsis, showing an opposite response as compared to that in poplars. We referred to the difference in regulation between Arabidopsis and poplars as differential regulation. Furthermore, the expression of the miR398 target, copper superoxide dismutase1 (CSD1), was in reverse correlation with the miR398 level, suggesting a control of this specific target expression predominantly by miR398 under abiotic stress. Together, these data consistently show a correlated regulation between miR398 and its representative target, CSD1, by ABA and salt stresses, and raise the possibility that regulation of miRNAs in plants is twofold: a dynamic regulation within a plant species and a differential regulation between different plant species.


miRNA Abiotic stress Dynamic regulation ABA Salt stress 



Abscisic acid


ATP sulfurylase


Cu/Zn superoxide dismutase




Quantitative reverse transcrioption PCR


RNA-induced silencing complex

Supplementary material

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  1. Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in arabidopsis. J Biol Chem 283:15932–15945. doi:10.1074/jbc.M801406200 PubMedCrossRefGoogle Scholar
  2. Andrali SS, Qian Q, Ozcan S (2007) Glucose mediates the translocation of NeuroD1 by O-linked glycosylation. J Biol Chem 282:15589–15596. doi:10.1074/jbc.M701762200 PubMedCrossRefGoogle Scholar
  3. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999. doi:10.1104/pp.106.079707 PubMedCrossRefGoogle Scholar
  4. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. doi:10.1016/S0092-8674(04)00045-5 PubMedCrossRefGoogle Scholar
  5. Cartolano M, Castillo R, Efremova N, Kuckenberg M, Zethof J, Gerats T, Schwarz-Sommer Z, Vandenbussche M (2007) A conserved microRNA module exerts homeotic control over petunia hybrida and antirrhinum majus floral organ identity. Nat Genet 39:901–905. doi:10.1038/ng2056 PubMedCrossRefGoogle Scholar
  6. Chen X (2005) MicroRNA biogenesis and function in plants. FEBS Lett 579:5923–5931. doi:10.1016/j.febslet.2005.07.071 PubMedCrossRefGoogle Scholar
  7. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18:412–421. doi:10.1105/tpc.105.038943 PubMedCrossRefGoogle Scholar
  8. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453–1454. doi:10.1093/bioinformatics/bth078 PubMedCrossRefGoogle Scholar
  9. Du T, Zamore PD (2005) MicroPrimer: the biogenesis and function of microRNA. Development 132:4645–4652. doi:10.1242/dev.02070 PubMedCrossRefGoogle Scholar
  10. Dugas DV, Bartel B (2008) Sucrose induction of arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417. doi:10.1007/s11103-008-9329-1 PubMedCrossRefGoogle Scholar
  11. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043. doi:10.1016/j.cub.2005.10.016 PubMedCrossRefGoogle Scholar
  12. Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229:1009–1014. doi:10.1007/s00425-009-0889-3 PubMedCrossRefGoogle Scholar
  13. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799. doi:10.1016/j.molcel.2004.05.027 PubMedCrossRefGoogle Scholar
  14. 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. doi:10.1111/j.1365-313X.2008.03690.x PubMedCrossRefGoogle Scholar
  15. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385. doi:10.1038/nrm1644 PubMedCrossRefGoogle Scholar
  16. Lai EC (2005) miRNAs: whys and wherefores of miRNA-mediated regulation. Curr Biol 15:R458–R460. doi:10.1016/j.cub.2005.06.015 PubMedCrossRefGoogle Scholar
  17. Lichtenthaler HK (1998) The stress concept in plants: an introduction. Ann N Y Acad Sci 851:187–198. doi:10.1111/j.1749-6632.1998.tb08993.x PubMedCrossRefGoogle Scholar
  18. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843. doi:10.1261/rna.895308 PubMedCrossRefGoogle Scholar
  19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−△△CT method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  20. 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. doi:10.1105/tpc.105.033456 PubMedCrossRefGoogle Scholar
  21. Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in populus. Plant J 55:131–151. doi:10.1111/j.1365-313X.2008.03497.x PubMedCrossRefGoogle Scholar
  22. Marsit CJ, Eddy K, Kelsey KT (2006) MicroRNA responses to cellular stress. Cancer Res 66:10843–10848. doi:10.1158/0008-5472.CAN-06-1894 PubMedCrossRefGoogle Scholar
  23. Murchison EP, Hannon GJ (2004) miRNAs on the move: miRNA biogenesis and the RNAi machinery. Curr Opin Cell Biol 16:223–229. doi:10.1016/ PubMedCrossRefGoogle Scholar
  24. Nilsen TW (2007) Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet 23:243–249. doi:10.1016/j.tig.2007.02.011 PubMedCrossRefGoogle Scholar
  25. Okamura K, Phillips MD, Tyler DM, Duan H, Chou YT, Lai EC (2008) The regulatory activity of microRNA* species has substantial influence on microRNA and 3′ UTR evolution. Nat Struct Mol Biol 15:354–363. doi:10.1038/nsmb.1409 PubMedCrossRefGoogle Scholar
  26. Saldanha AJ (2004) Java treeview—extensible visualization of microarray data. Bioinformatics 20:3246–3248. doi:10.1093/bioinformatics/bth349 PubMedCrossRefGoogle Scholar
  27. Shukla LI, Chinnusamy V, Sunkar R (2008) The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim Biophys Acta 1779:743–748PubMedGoogle Scholar
  28. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019. doi:10.1105/tpc.104.022830 PubMedCrossRefGoogle Scholar
  29. 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. doi:10.1105/tpc.106.041673 PubMedCrossRefGoogle Scholar
  30. Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309. doi:10.1016/j.tplants.2007.05.001 PubMedCrossRefGoogle Scholar
  31. Tang G (2005) siRNA and miRNA: an insight into RISCs. Trends Biochem Sci 30:106–114. doi:10.1016/j.tibs.2004.12.007 PubMedCrossRefGoogle Scholar
  32. Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17:49–63. doi:10.1101/gad.1048103 PubMedCrossRefGoogle Scholar
  33. Tang X, Gal J, Zhuang X, Wang W, Zhu H, Tang G (2007) A simple array platform for microRNA analysis and its application in mouse tissues. RNA 13:1803–1822. doi:10.1261/rna.498607 PubMedCrossRefGoogle Scholar
  34. Tang G, Tang X, Mendu V, Jia X, Chen QJ, He L (2008) The art of microRNA: various strategies leading to gene silencing via an ancient pathway. Biochim Biophys Acta 1779:655–662PubMedGoogle Scholar
  35. Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289:3–16. doi:10.1016/j.ydbio.2005.10.036 PubMedCrossRefGoogle Scholar
  36. Zhang B, Wang Q, Pan X (2007) MicroRNAs and their regulatory roles in animals and plants. J Cell Physiol 210:279–289. doi:10.1002/jcp.20869 PubMedCrossRefGoogle Scholar
  37. Zhang Z, Wei L, Zou X, Tao Y, Liu Z, Zheng Y (2008) Submergence-responsive microRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Ann Bot (Lond) 102:509–519. doi:10.1093/aob/mcn129 CrossRefGoogle Scholar
  38. 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 354:585–590. doi:10.1016/j.bbrc.2007.01.022 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Xiaoyun Jia
    • 1
  • Wang-Xia Wang
    • 1
  • Ligang Ren
    • 1
  • Qi-Jun Chen
    • 1
  • Venugopal Mendu
    • 1
  • Benjamin Willcut
    • 1
  • Randy Dinkins
    • 2
  • Xiaoqing Tang
    • 1
  • Guiliang Tang
    • 1
  1. 1.Department of Plant and Soil Sciences and KTRDC, Gene Suppression LaboratoryUniversity of KentuckyLexingtonUSA
  2. 2.Forage-Animal Production UnitUSDA-ARSLexingtonUSA

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