Identification of cold-responsive miRNAs and their target genes in nitrogen-fixing nodules of soybean

International Journal of Molecular Sciences

Volumn 15, Issue 8, 2014, Pages 13596-13614

  Zhang, Senlei ^a,b   Wang, Youning ^a   Li, Kexue ^a   Zou, Yanmin ^a   Chen, Liang ^a   Li, Xia ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Functional nodules; Glycine max (L.) Merrill; Low temperature; microRNAs

Indexed keywords

MICRORNA; NITROGEN;

COLD; GENE EXPRESSION REGULATION; METABOLISM; NODULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SOYBEAN;

COLD TEMPERATURE; GENE EXPRESSION REGULATION, PLANT; MICRORNAS; NITROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; ROOT NODULES, PLANT; SEQUENCE ANALYSIS, RNA; SOYBEANS;

EID: 84905652920     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms150813596     Document Type: Article

References (75)

1. Chinnusamy, V.; Zhu, J.; Zhu, J.K. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007, 12, 444-451.
2. Yamaguchi-Shinozaki, K.; Shinozaki, K. Transcriptional regulatory networksin cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 2006, 57, 781-803.
3. Achard, P.; Gong, F.; Cheminant, S.; Alioua, M.; Hedden, P.; Genschik, P. The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effecton gibberellin metabolism. Plant Cell 2008, 20, 2117-2129.
4. Chinnusamy, V.; Zhu, J.-K.; Sunkar, R. Gene regulation during cold stress acclimation in plants. Methods Mol. Biol. 2010, 639, 39-55.
5. Khraiwesh, B.; Zhu, J.; Zhu, J. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta 2012, 1819, 137-148.
6. Sunkar, R.; Li, Y.; Jagadeeswaran, G. Functionsof microRNAs in plant stress responses. Cell 2012, 17, 196-203.
7. Miura, K.; Furumoto, T. Cold signaling and cold response in plants. Int. J. Mol. Sci. 2013, 14, 5312-5337.
8. Zhou, X.; Wang, G.; Sutoh, K.; Zhu, J.; Zhang, W. Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim. Biophys. Acta 2008, 1779, 780-788.
9. Sunkar, R. Novel and stress-regulated microRNAs and other small rnas from Arabidopsis. Plant Cell 2004, 16, 2001-2019.
10. Zhang, J.; Xu, Y.; Huan, Q.; Chong, K. Deep sequencing of Brachypodiumsmall RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics 2009, 10, 449.
11. Tang, Z.; Zhang, L.; Xu, C.; Yuan, S.; Zhang, F.; Zheng, Y.; Zhao, C. Uncovering small RNA-mediated responses to cold stress in a wheat thermosensitive genic male-sterile line by deep sequencing. Plant Physiol. 2012, 159, 721-738.
12. Thiebaut, F.; Rojas, C.A.; Almeida, K.L.; Grativol, C.; Domiciano, G.C.; Lamb, C.R.C.; de Almeida Engler, J.; Hemerly, A.S.; Ferreira, P.C. Regulation of miR319 during cold stress in sugarcane. Plant Cell Environ. 2012, 35, 502-512.
13. Lu, S.; Sun, Y.-H.; Chiang, V.L. Stress-responsive microRNAs in Populus. Plant J. 2008, 55, 131-151.
14. Keyser, H.; Li, F. Potential for increasing biological nitrogen fixation in soybean. In Biological Nitrogen Fixation for Sustainable Agriculture; Ladha, J.K., George, T., Bohlool, B.B., Eds.; Springer: Berlin, Germany, 1992; pp. 119-135.
15. Duke, S.; Scharader, L.; Miller, M. Low temperature effects on soybean (Glycine max) mitochondrial respiration and several dehydrogenases during imbibition and germination. Plant Physiol. 1977, 60, 716-722.
16. Walsh, K.; Layzell, D. Carbon and nitrogen assimilation and partitioning in soybeans exposed to low root temperatures. Plant Physiol. 1986, 80, 249-255.
17. 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.
18. Van Heerden, P.D.R.; Kiddle, G.; Pellny, T.K.; Mokwala, P.W.; Jordaan, A.; Strauss, A.J.; de Beer, M.; Schluter, U.; Kunert, K.J.; Foyer, C.H. Regulation of respiration and the oxygen diffusion barrier in soybean protect symbiotic nitrogen fixation from chilling-induced inhibition and shoots from premature senescence. Plant Physiol. 2008, 148, 316-327.
19. Allen, D.J.; Ort, D.R. Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci. 2001, 6, 36-42.
20. Kingston-Smith, A.H.; Harbinson, J.; Williams, J.; Foyer, C.H. Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photoinhibition in maize leaves. Plant Physiol. 1997, 114, 1039-1046.
21. Joshi, T.; Yan, Z.; Libault, M.; Jeong, D.-H.; Park, S.; Green, P.J.; Sherrier, D.J.; Farmer, A.; May, G.; Meyers, B.C. et al. Prediction of novel miRNAs and associated target genes in Glycine max. BMC Bioinform. 2010, 11, S14.
22. 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.
23. 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, 5.
24. Zhang, B.; Pan, X.; Stellwag, E.J. Identification of soybean microRNAs and their targets. Planta 2008, 229, 161-182.
25. 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.
26. Kulcheski, F.R.; de Oliveira, L.F.V.; Molina, L.G.; Almerão, M.P.; Rodrigues, F.A.; Marcolino, J.; Barbosa, J.F.; Stolf-Moreira, R.; Nepomuceno, A.L.; Marcelino-Guimarães, F.C.;et al. Identification of novel soybean microRNAs involvedin abiotic and biotic stresses. BMC Genomics 2011, 12, 307.
27. Pfeiffer, N.E.; Torres, C.M.; Wagner, F.W. Proteolytic activity in soybean root nodules activity in host cell cytosol and bacteroids throughout physiological development and senescence. Plant Physiol. 1983, 71, 797-802.
28. Chen, P.-C.; Phillips, D.A. Induction of root nodule senescence by combined nitrogen in Pisum sativum L. Plant Physiol. 1977, 59, 440-442.
29. Delgado, M.J.; Garrido, J.M.; Ligero, F.; Lluch, C. Nitrogen fixation and carbon metabolism by nodules and bacteroids ofpea plants under sodium chloride stress. Physiol. Plant. 1993, 89, 824-829.
30. Delgado, M.J.; Ligero, F.; Lluch, C. Effects of salt stress on growthand nitrogen fixation by pea, faba-bean, common bean and soybean plants. Soil Biol. Biochem. 1994, 26, 371-376.
31. Balestrasse, K.B.; Gardey, L.; Gallego, S.M.; Tomaro, M. Response of antioxidant defence system in soybean nodules and roots subjected to cadmium stress. Funct. Plant Biol. 2001, 28, 497-504.
32. López, M.; Herrera-Cervera, J.A.; Iribarne, C.; Tejera, N.A.; Lluch, C. Growth and nitrogen fixation in Lotus japonicusand Medicago. truncatulaunder NaCl stress: Nodule carbon metabolism. J. Plant Physiol. 2008, 165, 641-650.
33. Sánchez-Pardo, B.; Carpena, R.O.; Zornoza, P. Cadmium in white lupin nodules: Impact on nitrogen and carbon metabolism. J. Plant Physiol. 2013, 170, 265-271.
34. Navascués, J.; Pérez-Rontomé, C.; Gay, M.; Marcos, M.; Yang, F.; Walker, F.A.; Desbois, A.; Abián, J.; Becana, M. Leghemoglobin green derivatives with nitrated hemes evidence production of highly reactive nitrogen species during aging of legume nodules. Proc. Natl. Acad. Sci. USA 2012, 109, 2660-2665.
35. Vorster, B.J.; Schlüter, U.; du Plessis, M.; van Wyk, S.; Makgopa, M.E.; Ncube, I.; Quain, M.D.; Kunert, K.; Foyer, C.H. The cysteine protease-cysteine protease inhibitor system explored in soybean nodule development. Agronomy 2013, 3, 550-570.
36. Boyd, E.S.; Lange, R.K.; Mitchell, A.C.; Havig, J.R.; Hamilton, T.L.; Lafrenière, M.J.; Shock, E.L.; Peters, J.W.; Skidmore, M. Diversity, abundance, and potential activity of nitrifying and nitrate-reducing microbial assemblages in a subglacial ecosystem. Appl. Environ. Microb. 2011, 77, 4778-4787.
37. Fenta, B.A.; Driscoll, S.P.; Kunert, K.J.; Foyer, C.H. Characterization ofdrought-tolerance traits in nodulated soya beans: The importance of maintaining photosynthesis and shoot biomass under drought-induced limitations on nitrogen metabolism. J. Agron. Crop. Sci. 2012, 198, 92-103.
38. Furlan, A.; Bianucci, E.; del Carmen, T.M.; Castro, S.; Dietz, K. Antioxidant enzyme activities and gene expression patterns in peanut nodules during a drought and rehydration cycle. Funct. Plant Biol. 2014, 41, 81-86.
39. + assimilation in nodulated and N-fertilized Phaseolus. vulgarisL. exposed to high temperature stress. Environ. Exp. Bot. 2014, 98, 32-39.
40. De Costa, W.; Becher, M.; Schubert, S. Effects of water stress on nitrogen fixation of common bean (Phaseolus. vulgarisL.). J. Nat. Sci. Found. Sri Lanka 2012, 25, 83-94.
41. Palma, F.; Tejera, N.A.; Lluch, C. Nodule carbohydrate metabolism and polyols involvement in the response of Medicago sativato salt stress. Environ. Exp. Bot. 2013, 85, 43-49.
42. Plantpan. Available online: http://plantpan.mbc.nctu.edu.tw/ (accessed on 17 July 2012).
43. Dai, X.; Zhao, P. psRNATarget: A plant small RNA target analysis server. Nucleic Acids Res. 2011, 39, 155-159.
44. Ossowski, S.; Schwab, R.; Weigel, D. Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 2008, 53, 674-690.
45. Simon, S.A.; Meyers, B.C.; Sherrier, D.J. MicroRNAs in the rhizobia legume symbiosis. Plant Physiol. 2009, 151, 1002-1008.
46. Devers, E.; Branscheid, A.; May, P.; Krajinski, F. Stars and symbiosis: MicroRNA-and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol. 2011, 156, 1990-2010.
47. Dong, Z.; Shi, L.; Wang, Y.; Chen, L.; Cai, Z.; Wang, Y.; Jin, J.; Li, X. Identification and dynamic regulation of microRNAs involved in salt stress responses in functional soybean nodules by high-throughput sequencing. Int. J. Mol. Sci. 2013, 14, 2717-2738.
48. Lv, D.-K.; Bai, X.; Li, Y.; Ding, X.-D.; Ge, Y.; Cai, H.; Ji, W.; Wu, N.; Zhu, Y.-M. Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 2010, 459, 39-47.
49. Chen, L.; Zhang, Y.; Ren, Y.; Xu, J.; Zhang, Z.; Wang, Y. Genome-wide identification of cold-responsive and new microRNAs in Populus tomentosa by high-throughput sequencing. Biochem. Biophys. Res. Commun. 2012, 417, 892-896.
50. Li, Y.; Fu, Y.; Ji, L.; Wu, C.; Zheng, C. Characterization and expression analysis of the Arabidopsismir169 family. Plant Sci. 2010, 178, 271-280.
51. Zhang, X.-N.; Li, X.; Liu, J.-H. Identification of conserved and novel cold-responsive microRNAs in trifoliate orange (Poncirus. trifoliata(L.) Raf.) using high-throughput sequencing. Plant Mol. Biol. Rep. 2014, 32, 328-341.
52. Boualem, A.; Laporte, P.; Jovanovic, M.; Laffont, C.; Plet, J.; Combier, J.P.; Niebel, A.; Crespi, M.; Frugier, F. microRNA166 controls root and nodule development in Medicago truncatula. Plant J. 2008, 54, 876-887.
53. Høgslund, N.; Radutoiu, S.; Krusell, L.; Voroshilova, V.; Hannah, M.A.; Goffard, N.; Sanchez, D.H.; Lippold, F.; Ott, T.; Sato, S. Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicusmutant and wild-type plants. PLoS One 2009, 4, e6556.
54. Lelandais-Briere, C.; Naya, L.; Sallet, E.; Calenge, F.; Frugier, F.; Hartmann, C.; Gouzy, J.; Crespi, M. Genome-wide Medicago truncatulasmall RNA analysis revealednovel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 2009, 21, 2780-2796.
55. Takahara, M.; Magori, S.; Soyano, T.; Okamoto, S.; Yoshida, C.; Yano, K.; Sato, S.; Tabata, S.; Yamaguchi, K.; Shigenobu, S. TOO MUCH LOVE, a Novel Kelch repeat-containing F-box protein, functions in the long-distance regulation of the legume-rhizobium symbiosis. Plant Cell Physiol. 2013, 54, 433-447.
56. De Luis, A.; Markmann, K.; Cognat, V.; Holt, D.B.; Charpentier, M.; Parniske, M.; Stougaard, J.; Voinnet, O. Two microRNAs linked to nodule infection and nitrogen-fixing ability in the legume Lotus japonicus. Plant Physiol. 2012, 160, 2137-2154.
57. Ding, Y.; Chen, Z.; Zhu, C. Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J. Exp. Bot. 2011, 62, 3563-3573.
58. Ding, D.; Li, W.; Han, M.; Wang, Y.; Fu, Z.; Wang, B.; Tang, J. Identification and characterisation of maize microRNAs involved in developing ears. Plant Biol. 2014, 16, 9-15.
59. Uno, Y. Arabidopsisbasic leucine zipper transcription factors involved inan abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl. Acad. Sci. USA 2000, 97, 11632-11637.
60. Shin, D.; Koo, Y.D.; Lee, J.; Lee, H.-J.; Baek, D.; Lee, S.; Cheon, C.-I.; Kwak, S.-S.; Lee, S.Y.; Yun, D.-J. Athb-12, a homeobox-leucine zipper domain protein from Arabidopsis thaliana, increases salt tolerance in yeast by regulating sodium exclusion. Biochem. Biophys. Res. Commun. 2004, 323, 534-540.
61. Rodriguez-Uribe, L. A root-specific bZIP transcription factor is responsive to water deficit stress in tepary bean (Phaseolus. acutifolius) and common bean (P. vulgaris). J. Exp. Bot. 2006, 57, 1391-1398.
62. Kuo, H.-F.; Chiou, T.-J. The role of microRNAs in phosphorus deficiency signaling. Plant Physiol. 2011, 156, 1016-1024.
63. Liang, G.; He, H.; Yu, D. Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS One 2012, 7, e48951.
64. Hsieh, L.C.; Lin, S.I.; Shih, A.C.C.; Chen, J.W.; Lin, W.Y.; Tseng, C.Y.; Li, W.H.; Chiou, T.J. Uncovering small rna-mediated responses to phosphate deficiency in Arabidopsisby deep sequencing. Plant Physiol. 2009, 151, 2120-2132.
65. Xu, F.; Liu, Q.; Chen, L.; Kuang, J.; Walk, T.; Wang, J.; Liao, H. Genome-wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics 2013, 14, 66.
66. Smit, P.; Raedts, J.; Portyanko, V.; Debellé, F.; Gough, C.; Bisseling, T.; Geurts, R. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 2005, 308, 1789-1791.
67. Murakami, Y.; Miwa, H.; Imaizumi-Anraku, H.; Kouchi, H.; Downie, J.A.; Kawaguchi, M.; Kawasaki, S. Positional cloning identifies Lotus japonicusNSP2, a putative transcription factor of the GRAS family, required for NINand ENOD40gene expression in nodule initiation. DNA Res. 2007, 13, 255-265.
68. Gobbato, E.; Marsh, J.F.; Vernié, T.; Wang, E.; Maillet, F.; Kim, J.; Miller, J.B.; Sun, J.; Bano, S.A.; Ratet, P. A GRAS-type transcription factor witha specific function in mycorrhizal signaling. Curr. Biol. 2012, 22, 2236-2241.
69. Maity, S.N.; de Crombrugghe, B. Role of the CCAAT-binding protein CBF/NF-Y in transcription. Trends Biochem. Sci. 1998, 23, 174-178.
70. Combier, J.P.; Frugier, F.; de Billy, F.; Boualem, A.; El-Yahyaoui, F.; Moreau, S.; Vernie, T.; Ott, T.; Gamas, P.; Crespi, M.;et al. MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Gene. Dev. 2006, 20, 3084-3088.
71. Appleby, C.; Bergersen, F. Preparation and experimental use of leghaemoglobin. In Methods for Evaluating Biological Nitrogen Fixation; Bergersen, F.J., Ed.; John Wiley & Sons: Chichester, UK, 1980; pp. 315-335.
72. Shearer, G.; Kohl, D.H. N2-fixation in field settings: Estimations based on natural 15 N abundance. Funct. Plant Biol. 1986, 13, 699-756.
73. NCBI Genbank Database. Available online: http://www.ncbi.nlm.nih.gov/blast/Blast.cgi (accessed on 15 July 2012).
74. Sanger. Available online: http://www.sanger.ac.uk/Software/Rfam (accessed on 15 July 2012).
75. Phytozome. Available online: http://www.phytozome.net/ (accessed on 20 July 2012).