Skip to main content
Log in

Difference in miRNA expression profiles between two cotton cultivars with distinct salt sensitivity

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are a class of endogenous, non-coding small RNAs that play important roles in many developmental processes and stress responses in plants and animals. Cotton (Gossypium hirsutum L.) is considered a relatively salt-tolerant non-halophytic plant species. To study the role of miRNAs in salt adaptation, a salt-tolerant cotton cultivar SN-011 and a salt-sensitive cultivar LM-6 were used to detect differentially expressed miRNAs. Using miRNA microarray analysis and a computational approach, 17 cotton miRNAs belonging to eight families were identified. Although they are conserved, 12 of them showed a genotype-specific expression model in both the cultivars. Under salt stress treatment, miR156a/d/e, miR169, miR535a/b and miR827b were dramatically down-regulated in SN-011, while miR167a, miR397a/b and miR399a were up-regulated. Only miR159 was found to be down-regulated in LM-6 under salt stress. To gain insight into their functional significance, 26 target genes were predicted and their functional similarity was further analyzed. Quantitative real-time PCR showed that the expression of seven target genes showed a significant inverse correlation with corresponding miRNAs. These differentially expressed miRNAs can help in further study into the role of transcriptome homeostasis in the adaptation responses of cotton to salt.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

miRNA:

microRNA

ARF:

Auxin response factor

MFEI:

Minimal folding free energy index

HAP:

Heme activator protein

PHO2:

Phosphate-responsive mutant 2

SBP:

Squamosa promoter-binding protein

SPL:

SBP-like proteins

GH3:

Grim helix 3

References

  1. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–527

    Article  PubMed  CAS  Google Scholar 

  2. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed  CAS  Google Scholar 

  3. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

  4. Wakeel A, Asif AR, Pitann B, Schubert S (2010) Proteome analysis of sugar beet (Beta vulgaris L.) elucidates constitutive adaptation during the first phase of salt stress. J Plant Physiol. doi:10.1016/j.jplph.2010.1008.1016

  5. 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(7):301–309

    Article  PubMed  CAS  Google Scholar 

  6. Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301(5631):336–338

    Article  PubMed  CAS  Google Scholar 

  7. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8(4):517–527

    Article  PubMed  CAS  Google Scholar 

  8. Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19(6):1750–1769

    Article  PubMed  CAS  Google Scholar 

  9. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  PubMed  CAS  Google Scholar 

  10. Sunkar R (2010) MicroRNAs with macro-effects on plant stress responses. Semi Cell Dev Biol 21(8):805–811

    Article  CAS  Google Scholar 

  11. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14(5):836–843

    Article  PubMed  CAS  Google Scholar 

  12. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25

    Article  PubMed  Google Scholar 

  13. 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 10:29

    Article  PubMed  Google Scholar 

  14. Gao P, Bai X, Yang L, Lv D, Pan X, Li Y, Cai H, Ji W, Chen Q, Zhu Y (2010) osa-MIR393: a salinity- and alkaline stress-related microRNA gene. Mol Biol Rep 38(1):237–242

    Article  PubMed  Google Scholar 

  15. 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(1–2):51–59

    Article  PubMed  CAS  Google Scholar 

  16. 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 (Lond) 103(1):29–38

    Article  CAS  Google Scholar 

  17. Leidi EO, Saiz JF (1997) Is salinity tolerance related to Na accumulation in Upland cotton (Gossypium hirsutum) seedlings? Plant Soil 190(1):67–75

    Article  CAS  Google Scholar 

  18. Zhang B, Wang Q, Wang K, Pan X, Liu F, Guo T, Cobb GP, Anderson TA (2007) Identification of cotton microRNAs and their targets. Gene 397(1–2):26–37

    Article  PubMed  CAS  Google Scholar 

  19. Khan Barozai MY, Irfan M, Yousaf R, Ali I, Qaisar U, Maqbool A, Zahoor M, Rashid B, Hussnain T, Riazuddin S (2008) Identification of micro-RNAs in cotton. Plant Physiol Biochem 46(8–9):739–751

    Article  PubMed  CAS  Google Scholar 

  20. Ruan MB, Zhao YT, Meng ZH, Wang XJ, Yang WC (2009) Conserved miRNA analysis in Gossypium hirsutum through small RNA sequencing. Genomics 94(4):263–268

    Article  PubMed  CAS  Google Scholar 

  21. Qiu CX, Xie FL, Zhu YY, Guo K, Huang SQ, Nie L, Yang ZM (2007) Computational identification of microRNAs and their targets in Gossypium hirsutum expressed sequence tags. Gene 395(1–2):49–61

    Article  PubMed  CAS  Google Scholar 

  22. Chen CX, Yu YJ, Wang HG, Shen FF, Liu FZ (1999) RAPD analysis and physiologic studies on salt-tolerance variation of cotton. Acta Agronomica Sinica 5(5):644–646

    Google Scholar 

  23. Chen CX, Yu YJ, Liu FZ, Shen FF, Wang HG (2000) Genetic analysis of salt-tolerance variant in cotton. Acta Bot Boreali-Occidental Sin 20(2):234–237

    Google Scholar 

  24. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33(20):e179

    Article  PubMed  Google Scholar 

  25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25(4):402–408

    Article  PubMed  CAS  Google Scholar 

  26. Zhang BH, Pan XP, Wang QL, Cobb GP, Anderson TA (2005) Identification and characterization of new plant microRNAs using EST analysis. Cell Res 15(5):336–360

    Article  PubMed  Google Scholar 

  27. Yin Z, Li C, Han X, Shen F (2008) Identification of conserved microRNAs and their target genes in tomato (Lycopersicon esculentum). Gene 414(1–2):60–66

    Article  PubMed  CAS  Google Scholar 

  28. Nasaruddin NM, Harikrishna K, Othman RY, Lim SH, Harikrishna JA (2007) Computational prediction of microRNAs from Oil Palm (Elaeis guineensis Jacq.) expressed sequence tags. Asia Pac J Mol Biol Biotechnol 15(3):107–113

    Google Scholar 

  29. Zhang BH, Pan XP, Cox SB, Cobb GP, Anderson TA (2006) Evidence that miRNAs are different from other RNAs. Cell Mol Life Sci 63(2):246–254

    Article  PubMed  CAS  Google Scholar 

  30. Kwak PB, Wang QQ, Chen XS, Qiu CX, Yang ZM (2009) Enrichment of a set of microRNAs during the cotton fiber development. BMC Genomics 10:457

    Article  PubMed  Google Scholar 

  31. Sunkar R, Jagadeeswaran G (2008) In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol 8:37

    Article  PubMed  Google Scholar 

  32. Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55(1):131–151

    Article  PubMed  CAS  Google Scholar 

  33. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019

    Article  PubMed  CAS  Google Scholar 

  34. Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67(1–2):183–195

    Article  PubMed  CAS  Google Scholar 

  35. Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738–749

    Article  PubMed  CAS  Google Scholar 

  36. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and post transcriptionally to promote drought resistance. Plant Cell 20(8):2238–2251

    Article  PubMed  CAS  Google Scholar 

  37. Thirumurugan T, Ito Y, Kubo T, Serizawa A, Kurata N (2008) Identification, characterization and interaction of HAP family genes in rice. Mol Genet Genomics 279(3):279–289

    Article  PubMed  CAS  Google Scholar 

  38. Flattery-O’Brien JA, Grant CM, Dawes IW (1997) Stationary-phase regulation of the Saccharomyces cerevisiae SOD2 gene is dependent on additive effects of HAP2/3/4/5- and STRE-binding elements. Mol Microbiol 23(2):303–312

    Article  PubMed  Google Scholar 

  39. Gao X, Ren Z, Zhao Y, Zhang H (2003) Overexpression of SOD2 increases salt tolerance of Arabidopsis. Plant Physiol 133(4):1873–1881

    Article  PubMed  CAS  Google Scholar 

  40. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36:D154–D158

    Article  PubMed  CAS  Google Scholar 

  41. Lin SI, Santi C, Jobet E, Lacut E, El Kholti N, Karlowski WM, Verdeil JL, Breitler JC, Perin C, Ko SS, Guiderdoni E, Chiou TJ, Echeverria M (2011) Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 51(12):2119–2131

    Article  Google Scholar 

  42. Pamp SJ, Frees D, Engelmann S, Hecker M, Ingmer H (2006) Spx is a global effector impacting stress tolerance and biofilm formation in Staphylococcus aureus. J Bacteriol 188(13):4861–4870

    Article  PubMed  CAS  Google Scholar 

  43. Yang JH, Han SJ, Yoon EK, Lee WS (2006) Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res 34(6):1892–1899

    Article  PubMed  CAS  Google Scholar 

  44. Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282(13):10036–10046

    Article  PubMed  CAS  Google Scholar 

  45. Teichmann T, Bolu-Arianto WH, Olbrich A, Langenfeld-Heyser R, Gobel C, Grzeganek P, Feussner I, Hansch R, Polle A (2008) GH3:GUS reflects cell-specific developmental patterns and stress-induced changes in wood anatomy in the poplar stem. Tree Physiol 28(9):1305–1315

    Article  PubMed  CAS  Google Scholar 

  46. Junghans U, Polle A, Duchting P, Weiler E, Kuhlman B, Gruber F, Teichmann T (2006) Adaptation to high salinity in poplar involves changes in xylem anatomy and auxin physiology. Plant Cell Environ 29(8):1519–1531

    Article  PubMed  CAS  Google Scholar 

  47. Ke Y, Pan T (2002) Effects of NaCl stress on seedling growth and IAA metabolism of sweet potato and its relation to salt-tolerance. Ying yong sheng tai xue bao 13(10):1303–1306

    PubMed  CAS  Google Scholar 

  48. Khraiwesh B, Zhu J-K, Zhu J (2011) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta. doi:10.1016/j.bbagrm.2011.05.001

  49. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15(22):2038–2043

    Article  PubMed  CAS  Google Scholar 

  50. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141(3):988–999

    Article  PubMed  CAS  Google Scholar 

  51. 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(5):731–738

    Article  PubMed  CAS  Google Scholar 

  52. Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Natl Rev Mol Cell Biol 10(6):385–397

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the China Key Development Project for Basic Research (973) (Grant No. 2007CB116208), and the China Major Projects for Transgenic Breeding (Grant No. 2008ZX005-004, 2008ZX08005-002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fafu Shen.

Additional information

Yan Li and Zujun Yin contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1 Flowchart for the prediction of potential miRNAs and target genes in cotton. (TIFF 87 kb)

11033_2011_1292_MOESM2_ESM.tif

Supplementary Fig. 2 Predicted fold-back structures of the cotton miRNA precursors. Sequences of mature miRNAs are underlined. (TIFF 318 kb)

11033_2011_1292_MOESM3_ESM.tif

Supplementary Fig. 3 Northern validation of the microarray result. RNA was isolated from the control and from the salt-treated plants of two cotton cultivars. (S) LM-6, a salt-sensitive cultivar; (T) SN-011, a salt-tolerant cultivar; (CK) untreated plants; (Tr) plants treated with 300 mM NaCl for 24 h. The antisense (AS) and sense (S) oligonucleotides were used as controls. Size markers (21–24 nt RNA fraction) are shown on the left, and the relative amounts of RNA loading is visualized by the degree of ethidium bromide staining of tRNA. (TIFF 210 kb)

Supplementary Table 1 (DOC 85 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yin, Z., Li, Y., Yu, J. et al. Difference in miRNA expression profiles between two cotton cultivars with distinct salt sensitivity. Mol Biol Rep 39, 4961–4970 (2012). https://doi.org/10.1007/s11033-011-1292-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-011-1292-2

Keywords

Navigation