Identification and dynamic regulation of microRNAs involved in salt stress responses in functional soybean nodules by high-throughput sequencing

International Journal of Molecular Sciences

Volumn 14, Issue 2, 2013, Pages 2717-2738

  Dong, Zhanghui ^a,b,c   Shi, Lei ^a   Wang, Yanwei ^d   Chen, Liang ^a   Cai, Zhaoming ^a,b   Wang, Youning ^a   Jin, Jingbo ^e   Li, Xia ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c Shijiazhuang Academy of Agriculture and Forestry Sciences   (China)

^d BEIJING FORESTRY UNIVERSITY   (China)

^e INSTITUTE OF BOTANY   (China)

Author keywords

Functional nodules; MiRNA; Nitrogen fixation; Salt stress; Soybean

Indexed keywords

MICRORNA;

ARTICLE; BRADYRHIZOBIUM JAPONICUM; CONTROLLED STUDY; GENE EXPRESSION; HIGH THROUGHPUT SEQUENCING; NITROGEN FIXATION; NODULATION; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALT STRESS; SOYBEAN;

EID: 84875066243     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14022717     Document Type: Article

References (70)

1. Spaink, H.P. Root nodulation and infection factors produced by rhizobial bacteria. Ann. Rev. Microbiol. 2000, 54, 257-288.
2. Gage, D.J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 2004, 68, 280-300.
3. Zahran, H.H. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol. Mol. Biol. Rev. 1999, 63, 968-989.
4. Vance, C.P. Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol. 2001, 127, 390-397.
5. Graham, P.H.; Vance, C.P. Legumes: Importance and constraints to greater use. Plant Physiol. 2003, 131, 872-877.
6. 2 fixation by annual legumes. Field Crops Res. 2000, 65, 211-228.
7. Verdoy, D.; Lucas, M.; Manrique, E.; Covarrubias, A.; de Felipe, M.; Pueyo, J. Differential organ-specific response to salt stress and water deficit in nodulated bean (Phaseolus vulgaris). Plant Cell Environ. 2004, 27, 757-767.
8. Natural Resources and Environment. Available online: http://www.fao.org/ag/agl/agll/spush/ (accessed on 10 November 2012).
9. Wu, W.; Zhang, Q.; Zhu, Y.; Lam, H.M.; Cai, Z.; Guo, D. Comparative metabolic profiling reveals secondary metabolites correlated with soybean salt tolerance. J. Agric. Food Chem. 2008, 56, 11132-11138.
10. Ikeda, J. The effect of short term withdrawal of NaCl stress on nodulation of white clover. Plant Soil 1994, 158, 23-27.
11. Coba de la Peña, T.; Verdoy, D.; Redondo, F.J.; Pueyo, J.J. Salt Tolerance in the Rhizobium-Legume Symbiosis: An Overview. In Recent Research Developments in Plant Molecular Biology; Pandalai, S.G., Ed.; CAB Direct: Oxford, UK, 2003; pp. 187-205.
12. El-Hamdaoui, A.; Redondo-Nieto, M.; Rivilla, R.; Bonilla, I.; Bolanos, L. Effects of boron and calcium nutrition on the establishment of the Rhizobium leguminosarum-pea (Pisum sativum) symbiosis and nodule development under salt stress. Plant Cell Environ. 2003, 26, 1003-1011.
13. Pedersen, A.; Feldner, H.; Rosendahl, L. Effect of proline on nitrogenase activity in symbiosomes from root nodules of soybean (Glycine max L.) subjected to drought stress. J. Exp. Bot. 1996, 47, 1533-1539.
14. Matamoros, M.A.; Baird, L.M.; Escuredo, P.R.; Dalton, D.A.; Minchin, F.R.; Iturbe-Ormaetxe, I.; Rubio, M.C.; Moran, J.F.; Gordon, A.J.; Becana, M. Stress-induced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol. 1999, 121, 97-112.
15. Coba de la Pea, T.; Redondo, F.J.; Manrique, E.; Lucas, M.M.; Pueyo, J.J. Nitrogen fixation persists under conditions of salt stress in transgenic Medicago truncatula plants expressing a cyanobacterial flavodoxin. Plant Biotechnol. J. 2010, 8, 954-965.
16. Serraj, R.; Vasquez-Diaz, H.; Drevon, J. Effects of salt stress on nitrogen fixation, oxygen diffusion, and ion distribution in soybean, common bean, and alfalfa. J. Plant Nutr. 1998, 21, 475-488.
17. Gargantini, P.R.; Gonzalez-Rizzo, S.; Chinchilla, D.; Raices, M.; Giammaria, V.; Ulloa, R.M.; Frugier, F.; Crespi, M.D. A CDPK isoform participates in the regulation of nodule number in Medicago truncatula. Plant J. 2006, 48, 843-856.
18. Carlos, M.; Mainassara, Z.A.; Faheema, K.; Nadia, F.; Ralf, H.; Diana, S.; Laurie, A.; Jean-Jacques, D.; Peter, W.; Günter, K. The salt-responsive transcriptome of chickpea roots and nodules via deepSuperSAGE. BMC Plant Biol. 2011, 11, 1-26.
19. Brodersen, P.; Sakvarelidze-Achard, L.; Bruun-Rasmussen, M.; Dunoyer, P.; Yamamoto, Y.Y.; Sieburth, L.; Voinnet, O. Widespread translational inhibition by plant miRNAs and siRNAs. Science 2008, 320, 1185-1190.
20. Chen, X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 2004, 303, 2022-2025.
21. Sunkar, R.; Zhu, J.K. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 2004, 16, 2001-2019.
22. Jones-Rhoades, M.W.; Bartel, D.P.; Bartel, B. MicroRNAs and their regulatory roles in plants. Ann. Rev. Plant Biol. 2006, 57, 19-53.
23. Shukla, L.I.; Chinnusamy, V.; Sunkar, R. The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim. Biophys. Acta 2008, 1779, 743-748.
24. Gao, P.; Bai, X.; Yang, L.; Lv, D.; Pan, X.; Li, Y.; Cai, H.; Ji, W.; Chen, Q.; Zhu, Y. Osa-MIR393: A salinity-and alkaline stress-related microRNA gene. Mol. Biol. Rep. 2011, 38, 237-242.
25. Ding, D.; Zhang, L.; Wang, H.; Liu, Z.; Zhang, Z.; Zheng, Y. Differential expression of miRNAs in response to salt stress in maize roots. Ann. Bot. 2009, 103, 29-38.
26. Lu, S.; Sun, Y.H.; Chiang, V.L. Stress-responsive microRNAs in Populus. Plant J. 2008, 55, 131-151.
27. Liu, H.H.; Tian, X.; Li, Y.J.; Wu, C.A.; Zheng, C.C. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 2008, 14, 836-843.
28. Li, H.; Dong, Y.; Yin, H.; Wang, N.; Yang, J.; Liu, X.; Wang, Y.; Wu, J.; Li, X. Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol. 2011, 11, 1-12.
29. Gao, P.; Bai, X.; Yang, L.; Lv, D.; Li, Y.; Cai, H.; Ji, W.; Guo, D.; Zhu, Y. Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta 2010, 231, 991-1001.
30. Sunkar, R.; Zhou, X.; Zheng, Y.; Zhang, W.; Zhu, J.K. Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol. 2008, 8, 1-17.
31. Combier, J.P.; Frugier, F.; de Billy, F.; Boualem, A.; El-Yahyaoui, F.; Moreau, S.; Vernié, T.; Ott, T.; Gamas, P.; Crespi, M. MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev. 2006, 20, 3084-3088.
32. Subramanian, S.; Fu, Y.; Sunkar, R.; Barbazuk, W.B.; Zhu, J.K.; Yu, O. Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 2008, 9, 160-173.
33. Li, H.; Deng, Y.; Wu, T.; Subramanian, S.; Yu, O. Misexpression of miR482, miR1512, and miR1515 increases soybean nodulation. Plant Physiol. 2010, 153, 1759-1770.
34. Lelandais-Briere, C.; Naya, L.; Sallet, E.; Calenge, F.; Frugier, F.; Hartmann, C.; Gouzy, J.; Crespi, M. Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 2009, 21, 2780-2796.
35. Wang, Y.; Li, P.; Cao, X.; Wang, X.; Zhang, A.; Li, X. Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochem. Biophys. Res. Commun. 2009, 378, 799-803.
36. Turner, M.; Yu, O.; Subramanian, S. Genome organization and characteristics of soybean microRNAs. BMC Genomics 2012, 13, 169.
37. Lv, S.; Nie, X.; Wang, L.; Du, X.; Biradar, S.S.; Jia, X.; Weining, S. Identification and characterization of microRNAs from Barley (Hordeum vulgare L.) by high-throughput sequencing. Int. J. Mol. Sci. 2012, 13, 2973-2984.
38. Song, Q.X.; Liu, Y.F.; Hu, X.Y.; Zhang, W.K.; Ma, B.; Chen, S.Y.; Zhang, J.S. Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biol. 2011, 11, 1-16.
39. Martins, L.; Xavier, G.; Rangel, F.; Ribeiro, J.; Neves, M.; Morgado, L.; Rumjanek, N. Contribution of biological nitrogen fixation to cowpea: A strategy for improving grain yield in the semi-arid region of Brazil. Biol. Fertil. Soils 2003, 38, 333-339.
40. Mylona, P.; Pawlowski, K.; Bisseling, T. Symbiotic nitrogen fixation. Plant Cell 1995, 7, 869-885.
41. Joshi, T.; Yan, Z.; Libault, M.; Jeong, D.H.; Park, S.; Green, P.; Sherrier, D.J.; Farmer, A.; May, G.; Meyers, B. Prediction of novel miRNAs and associated target genes in Glycine max. BMC Bioinform. 2010, 11, 1-9.
42. miRBase: The microRNA Database Version 19.0. Available online: http://www.mirbase.org/ (accessed on 1 September 2012).
43. The mfold Web Server. Available online: http://mfold.rna.albany.edu/?q=mfold (accessed on 10 September 2012).
44. Wong, C.E.; Zhao, Y.T.; Wang, X.J.; Croft, L.; Wang, Z.H.; Haerizadeh, F.; Mattick, J.S.; Singh, M.B.; Carroll, B.J.; Bhalla, P.L. MicroRNAs in the shoot apical meristem of soybean. J. Exp. Bot. 2011, 62, 2495-2506.
45. Zhang, B.; Pan, X.; Stellwag, E.J. Identification of soybean microRNAs and their targets. Planta 2008, 229, 161-182.
46. Alonso-Peral, M.M.; Li, J.; Li, Y.; Allen, R.S.; Schnippenkoetter, W.; Ohms, S.; White, R.G.; Millar, A.A. The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. Plant Physiol. 2010, 154, 757-771.
47. Arenas-Huertero, C.; Pérez, B.; Rabanal, F.; Blanco-Melo, D.; de la Rosa, C.; Estrada-Navarrete, G.; Sanchez, F.; Covarrubias, A.A.; Reyes, J.L. Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol. Biol. 2009, 70, 385-401.
48. Kidner, C.A.; Martienssen, R.A. The developmental role of microRNA in plants. Curr. Opin. Plant Biol. 2005, 8, 38-44.
49. Brechenmacher, L.; Kim, M.Y.; Benitez, M.; Li, M.; Joshi, T.; Calla, B.; Lee, M.P.; Libault, M.; Vodkin, L.O.; Xu, D. Transcription profiling of soybean nodulation by Bradyrhizobium japonicum. Mol. Plant Microbe Interact. 2008, 21, 631-645.
50. McVay, K.; Radcliffe, D.; Hargrove, W. Winter legume effects on soil properties and nitrogen fertilizer requirements. Soil Sci. Soc. Am. J. 1989, 53, 1856-1862.
51. Jia, X.; Wang, W.X.; Ren, L.; Chen, Q.J.; Mendu, V.; Willcut, B.; Dinkins, R.; Tang, X.; Tang, G. Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populustremula and Arabidopsisthaliana. Plant Mol. Biol. 2009, 71, 51-59.
52. Singh, K.B.; Foley, R.C.; Oñate-Sánchez, L. Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 2002, 5, 430-436.
53. Niu, X.; Bressan, R.A.; Hasegawa, P.M.; Pardo, J.M. Ion homeostasis in NaCl stress environments. Plant Physiol. 1995, 109, 735-742.
54. Zhu, J.K. Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 2003, 6, 441-445.
55. Li, W.X.; Oono, Y.; Zhu, J.; He, X.J.; Wu, J.M.; Iida, K.; Lu, X.Y.; Cui, X.; Jin, H.; Zhu, J.K. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 2008, 20, 2238-2251.
56. Abe, H.; Yamaguchi-Shinozaki, K.; Urao, T.; Iwasaki, T.; Hosokawa, D.; Shinozaki, K. Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. The Plant Cell Online 1997, 9, 1859-1868.
57. 2+/calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants. Proc. Nat. Acad. Sci. 1998, 95, 9681-9686.
58. Fode, B.; Siemsen, T.; Thurow, C.; Weigel, R.; Gatz, C. The Arabidopsis GRAS protein SCL14 interacts with class II TGA transcription factors and is essential for the activation of stress-inducible promoters. Plant Cell 2008, 20, 3122-3135.
59. Sakamoto, H.; Maruyama, K.; Sakuma, Y.; Meshi, T.; Iwabuchi, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol. 2004, 136, 2734-2746.
60. Gluzman, I.; Francis, S.; Oksman, A.; Smith, C.; Duffin, K.; Goldberg, D. Order and specificity of the Plasmodium falciparum hemoglobin degradation pathway. J. Clin. Investig. 1994, 93, 1602-1608.
61. Miller, R.; McRae, D.; Al-Jobore, A.; Berndt, W. Respiration supported nitrogenase activity of isolated Rhizobium meliloti bacteroids. J. Cell. Biochem. 1988, 38, 35-49.
62. Phytozome. Available online: http://www.phytozome.net/soybean (accessed on 5 July 2012).
63. SOAP: Short Oligonucleotide Analysis Package. Available online: http://soap.genomics.org.cn/ (accessed on 5 July 2012).
64. Sanger. Available online: http://www.sanger.ac.uk/Software/Rfam (accessed on 15 July 2012).
65. NCBI Genbank Database. Available online: http://www.ncbi.nlm.nih.gov/blast/Blast.cgi (accessed on 15 July 2012).
66. MicroRNA Discovery by Deep Sequencing. Available online: http://sourceforge.net/projects/ mireap/ (accessed on 27 July 2012).
67. Meyers, B.C.; Axtell, M.J.; Bartel, B.; Bartel, D.P.; Baulcombe, D.; Bowman, J.L.; Cao, X.; Carrington, J.C.; Chen, X.; Green, P.J. Criteria for annotation of plant microRNAs. Plant Cell 2008, 20, 3186-3190.
68. Zuker, M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31, 3406-3415.
69. psRNATarget: A Plant Small RNA Target Analysis Server. Available online: http://plantgrn.noble.org/psRNATarget/ (accessed on 12 August 2012).
70. Schwab, R.; Palatnik, J.F.; Riester, M.; Schommer, C.; Schmid, M.; Weigel, D. Specific effects of microRNAs on the plant transcriptome. Dev. Cell 2005, 8, 517-527.