Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots

Journal of Experimental Botany

Volumn 64, Issue 14, 2013, Pages 4271-4287

  Xu, Liang ^a   Wang, Yan ^a   Zhai, Lulu ^a   Xu, Yuanyuan ^a   Wang, Liangju ^a   Zhu, Xianwen ^b   Gong, Yiqin ^a   Yu, Rugang ^a   Limera, Cecilia ^a   Liu, Liwang ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

Cadmium stress; Degradome; High throughput sequencing; MicroRNAs; Raphanus sativus; Transcriptome

Indexed keywords

CADMIUM; MESSENGER RNA; MICRORNA; PLANT RNA; TRANSCRIPTOME;

ARTICLE; BASE PAIRING; CADMIUM STRESS; DEGRADOME; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; HIGH-THROUGHPUT SEQUENCING; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT GENE; PLANT ROOT; RADISH; RAPHANUS; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY; RNA STABILITY; SEQUENCE ANALYSIS; TRANSCRIPTOME.;

CADMIUM STRESS; DEGRADOME; HIGH-THROUGHPUT SEQUENCING; MICRORNAS; RAPHANUS SATIVUS; TRANSCRIPTOME.;

BASE PAIRING; BASE SEQUENCE; CADMIUM; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENES, PLANT; MICRORNAS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PLANT ROOTS; RAPHANUS; REAL-TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; RNA STABILITY; RNA, MESSENGER; RNA, PLANT; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84887896162     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert240     Document Type: Article

References (68)

1. Addo-Quaye C., Eshoo TW, Bartel D.P., Axtell MJ 2008. Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Current Biology 18, 758-762.
2. Addo-Quaye C., Miller W, Axtell MJ 2009. CleaveLand, a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 25, 130-131.
3. Allen E, Xie ZX, Gustafson A.M., Carrington JC 2005. MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207-221.
4. Barakat A, Sriram A, Park J., Zhebentyayeva T, Main D, Abbott A. 2012. Genome wide identification of chilling responsive microRNAs in Prunus persica. BMC Genomics 13, 481.
5. Bartel DP. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
6. Benson DA, Karsch-Mizrachi I, Lipman D.J., Ostell J., Sayers EW 2011. GenBank. Nucleic Acids Research 39, D32-D37.
7. Besson-Bard A., Gravot A, Richaud P., Auroy P, Duc C, Gaymard F., Taconnat L, Renou JP, Pugin A, Wendehenne D. 2009. Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiology 149, 1302-1315.
8. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto Y.Y., Sieburth L., Voinnet O. 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190.
9. Chen L, Ren YY, Zhang Y.Y., Xu JC, Sun FS, Zhang ZY, Wang YW 2012a. Genome-wide identification and expression analysis of heat-responsive and novel microRNAs in Populus tomentosa. Gene 504, 160-165.
10. Chen L, Wang TZ, Zhao M.G., Tian QY, Zhang WH 2012b. Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235, 375-386.
11. Cuperus JT, Fahlgren N, Carrington JC 2011. Evolution and functional diversification of MIRNA genes. The Plant Cell 23, 431-442.
12. DalCorso G, Farinati S, Maistri S., Furini A. 2008. How plants cope with cadmium: staking all on metabolism and gene expression. Journal of Integrative Plant Biology 50, 1268-1280.
13. Ding YF, Chen Z, Zhu C. 2011. Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). Journal of Experimental Botany 62, 3563-3573.
14. Ding YF, Zhu C. 2009. The role of microRNAs in copper and cadmium homeostasis. Biochemical and Biophysical Research Communications 386, 6-10.
15. Fabian MR, Sonenberg N, Filipowicz W. 2010. Regulation of mRNA translation and stability by microRNAs. Annual Review of Biochemistry 79, 351-379.
16. German MA, Luo SJ, Schroth G, Meyers B.C., Green PJ 2009. Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nature Protocols 4, 356-362.
17. German MA, Pillay M, Jeong D.H., et al 2008. Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nature Biotechnology 26, 941-946.
18. Grant CA, Clarke JM, Duguid S, Chaney RL 2008. Selection and breeding of plant cultivars to minimize cadmium accumulation. Science of the Total Environment 390, 301-310.
19. Hafiner M, Landgraf P, Ludwig J., Rice A, Ojo T, Lin C., Holoch D, Lim C, Tuschl T. 2008. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods 44, 3-12.
20. Hsieh LC, Lin SI, Shih A.C., Chen JW, Lin WY, Tseng CY, Li W.H., Chiou TJ 2009. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology 151, 2120-2132.
21. Huang SQ, Peng J, Qiu C.X., Yang ZM 2009. Heavy metal-regulated new microRNAs from rice. Journal of Inorganic Biochemistry 103, 282-287.
22. Huang SQ, Xiang AL, Che L.L., Chen S., Li Hui, Song JB, Yang ZM 2010. A set of miRNAs from Brassica napus in response to sulfate-deficiency and cadmium stress. Plant Biotechnology Journal 8, 887-899.
23. Ishikawaa S, Ishimaru Y, Igura M., Kuramata M, Abe T, Senoura T., Hase Y, Arao T, Nishizawa N.K., Nakanishi H. 2012. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proceedings of the National Academy of Sciences, USA, 109, 19166-19171.
24. Jeong DH, Park S, Zhai J., Qurazada SGR, De Paoli E, Meyers BC, Green PJ 2011. Massive analysis of rice small RNAs, mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. The Plant Cell 23, 4185-4207.
25. Jones-Rhoades M.W., Bartel DP, Bartel B. 2006. MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology 57, 19-53.
26. Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya Y.N., Saito K., Takhashi H, Dalmay T. 2009. Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. The Plant Journal 57, 313-321.
27. Khraiwesh B, Zhu JK, Zhu JH 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochimica et Biophysica Acta 1819, 137-148.
28. Lelandais-Brière C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespia M. 2009. Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. The Plant Cell 21, 2780-2796.
29. Li BS, Duan H, Li J.G., Deng XW, Yin WL, Xia XL 2013. Global identification of miRNAs and targets in Populus euphratica under salt stress. Plant Molecular Biology 81, 525-539.
30. Li BS, Qin YR, Duan H, Yin W.L., Xia XL 2011. Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. Journal of Experimental Botany 62, 3765-3779.
31. Li R, Yu C, Li Y., Lam TW, Yiu SM, Kristiansen K, Wang J. 2009. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966-1967.
32. Li YF, Zheng Y, Addo-Quaye C, Zhang L.i., Saini A., Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R. 2010. Transcriptome-wide identification of microRNA targets in rice. The Plant Journal 62, 742-759.
33. Liang G, Yang F, Yu D. 2010. MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. The Plant Journal 62, 1046-1057.
34. Macovei A, Tuteja N. 2012. microRNAs targeting DEAD-box helicases are involved in salinity stress response in rice (Oryza sativa L.) BMC Plant Biology 12, 183.
35. Man MZ, Wang X, Wang Y. 2000. POWER-SAGE: comparing statistical tests for SAGE experiments. Bioinformatics 16, 953-959.
36. Martin RC, Asalina M, Liu P.P., et al 2010. The microRNA156 and microRNA172 gene regulation cascades at post-germinative stages in Arabidopsis. Seed Science Research 20, 79-87.
37. Martínez G., Forment J, Llave C., Pallás V, Gómez G. 2011. High-throughput sequencing, characterization and detection of new and conserved cucumber miRNAs. PLoS One 6, e19523.
38. McCormick KP, Willmann MR, Meyers BC 2011. Experimental design, preprocessing, normalization and differential expression analysis of small RNA sequencing experiments. Silence 2, 2.
39. Meyers BC, Axtell MJ, Bartel B, et al 2008. Criteria for annotation of plant microRNAs. The Plant Cell 20, 3186-3190.
40. Morozova O, Marra MA 2008. Applications of next-generation sequencing technologies in functional genomics. Genomics 92, 255-264.
41. Muvva C, Tewari L, Aruna K., Ranjit P, Zahoorullah SMD, Matheen KA, Veeramachaneni MDH. 2012. In silico identification of miRNAs and their targets from the expressed sequence tags of Raphanus sativus. Bioinformation 8, 98-103.
42. Pant BD, Musialak-Lange M, Nuc P., May P, Buhtz A, Kehr J., Walther D, Scheible WR 2009. Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiology 150, 1541-1555.
43. Rajagopalan R, Vaucheret H, Trejo J., Bartel DP 2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes and Devevelopment 20, 3407-3425.
44. Ruiz-Ferrer V., Voinnet O. 2009. Roles of plant small RNAs in biotic stress responses. Annual Review of Plant Biology 60, 485-510.
45. Satoh-Nagasawa N., Mori M, Nakazawa N., Kawamoto T, Nagato Y, Sakurai K., Takahashi H, Watanabe A, Akagi H. 2012. Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant and Cell Physiology 53, 213-224.
46. Shamimuzzaman M, Vodkin L. 2012. Identification of soybean seed developmental stage-specific and tissue-specific miRNA targets by degradome sequencing. BMC Genomics 13, 310.
47. Shimo H, Ishimaru Y, An G., Yamakawa T, Nakanishi H, Nishizawa NK 2011. Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice. Journal of Experimental Botany 62, 5727-5734.
48. 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. The Plant Cell 18, 2051-2065.
49. Takahashi R, Ishimaru Y, Senoura T., Shimo H, Ishikawa S, Arao T., Nakanishi H, Nishizawa NK 2011. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. Journal of Experimental Botany 62, 4843-4850.
50. Uraguchi S, Mori S, Kuramata M., Kawasaki A, Arao T, Ishikawa S. 2009. Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. Journal of Experimental Botany 60, 2677-2688.
51. Voinnet O. 2009. Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687.
52. Wang LZ, He QW 2005. Chinese radish. Beijing: Scientific and Technical Documents Publishing House.
53. Wang TZ, Chen L, Zhao M.G., Tian QY, Zhang WH 2011. Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12, 367.
54. Wiebe K, Harris NS, Faris J.D., Clarke JM, Knox RE, Taylor GJ, Pozniak CJ 2010. Targeted mapping of Cdu1, a major locus regulating grain cadmium concentration in durum wheat (Triticum turgidum L. var durum). Theoretical and Applied Genetics 121, 1047-1058.
55. Wu G, Park MY, Conway S.R., Wang JW, Weigel D, Poethig RS 2009. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750-759.
56. Xu L, Wang LJ, Gong Y.Q., Dai WH, Wang Y, Zhu XW, Wen T.C., Liu LW 2012. Genetic linkage map construction and QTL mapping of cadmium accumulation in radish (Raphanus sativus L.). Theoretical and Applied Genetics 125, 659-670.
57. Xu L, Wang Y, Xu Y.Y., Wang LJ, Zhai LL, Zhu XW, Gong Y.Q., Ye S., Liu LW 2013. Identification and characterization of novel and conserved microRNAs in radish (Raphanus sativus L.) using high-throughput sequencing. Plant Science 201-202, 108-114.
58. Xu MY, Dong Y, Zhang Q.X., Zhang L., Luo YZ, Sun J, Fan YL, Wang L. 2012. Identification of miRNAs and their targets from Brassica napus by high-throughput sequencing and degradome analysis. BMC Genomics 13, 421.
59. Yang JH, Liu XY, Xu B.C., Zhao N., Yang XD, Zhang MF 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 Genomics 14, 9.
60. Yang XY, Wang LC, Yuan D.J., Lindsey K., Zhang XL 2013. Small RNA and degradome sequencing reveal complex miRNA regulation during cotton somatic embryogenesis. Journal of Experimental Botany 64, 1521-1536.
61. Yu X, Wang H, Lu, YZ, Ruiter M., Cariaso M, Prins M, Tunen A., He YK 2012. Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. Journal of Experimental Botany 63, 1025-1038.
62. Zeng QY, Yang CY, Ma Q.B., Li XP, Dong WW, Nian H. 2012. Identification of wild soybean miRNAs and their target genes responsive to aluminum stress. BMC Plant Biology 12, 182.
63. Zhang J, Xu Y, Huan Q., Chong K. 2009. Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics 10, 449.
64. Zhou L, Liu Y, Liu Z., Kong D, Duan M, Luo L. 2010. Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. Journal of Experimental Botany 61, 4157-4168.
65. Zhou ZS, Huang SQ, Yang ZM 2008. Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochemical and Biophysical Research Communications 374, 538-542.
66. Zhou ZS, Song JB, Yang ZM 2012a. Genome-wide identification of Brassica napus microRNAs and their targets in response to cadmium. Journal of Experimental Botany 63, 4597-4613.
67. Zhou ZS, Zeng HQ, Liu Z.P., Yang ZM 2012b. Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant, Cell and Environment 35, 86-99.
68. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31, 3406-3415.