Identification of novel and salt-responsive miRNAs to explore miRNA-mediated regulatory network of salt stress response in radish (Raphanus sativus L.)
详细信息 查看全文
- 作者：Xiaochuan Sun (1) (2)
Liang Xu (1) (2)
Yan Wang (1)
Rugang Yu (1)
Xianwen Zhu (3)
Xiaobo Luo (1) (2)
Yiqin Gong (1)
Ronghua Wang (1)
Cecilia Limera (1)
Keyun Zhang (4)
Liwang Liu (1)
1. National Key Laboratory of Crop Genetics and Germplasm Enhancement ; College of Horticulture ; Nanjing Agricultural University ; Nanjing ; 210095 ; P.R. China
2. Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement ; Nanjing ; 210014 ; P.R. China
3. Department of Plant Sciences ; North Dakota State University ; Fargo ; ND ; 58108 ; USA
4. College of Life Sciences ; Nanjing Agricultural University ; Nanjing ; 210095 ; P.R.China - 关键词：Radish (Raphanus sativus L.) ; Salt stress ; MicroRNA ; Target gene ; RT ; qPCR ; High ; throughput sequencing
- 刊名：BMC Genomics
- 出版年：2015
- 出版时间：December 2015
- 年：2015
- 卷：16
- 期：1
- 全文大小：2,573 KB
- 参考文献：1. Munns, R, Tester, M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: pp. 651-81
2. Tester, M, Davenport, R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91: pp. 503-27
3. M盲ser, P, Eckelman, B, Vaidyanathan, R, Horie, T, Fairbairn, DJ, Kubo, M (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531: pp. 157-61
4. Sunkar, R, Li, YF, Jagadeeswaran, G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17: pp. 196-203
5. Kurihara, Y, Takashi, Y, Watanabe, Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12: pp. 206-12
6. Yu, B, Yang, Z, Li, J, Minakhina, S, Yang, M, Padgett, RW (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307: pp. 932-5
7. Liu, HH, Tian, X, Li, YJ, Wu, CA, Zheng, CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14: pp. 836-43
8. Ren, Y, Chen, L, Zhang, Y, Kang, X, Zhang, Z, Wang, Y (2013) Identification and characterization of salt-responsive microRNAs in Populus tomentosa by high-throughput sequencing. Biochimie 95: pp. 743-50
9. Li, B, Qin, Y, Duan, H, Yin, W, Xia, X (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62: pp. 3765-79
10. Eldem, V, Ak莽ay, U脟, Ozhuner, E, Bak谋r, Y, Uranbey, S, Unver, T (2012) Genome-wide identification of miRNAs responsive to drought in peach (Prunus persica) by high-throughput deep sequencing. PLoS One 7: pp. e50298
11. Yu, X, Wang, H, Lu, Y, Ruiter, M, Cariaso, M, Prins, M (2011) Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. J Exp Bot 63: pp. 1025-38
12. Chen, L, Ren, Y, Zhang, Y, Xu, J, Sun, F, Zhang, Z (2012) Genome-wide identification and expression analysis of heat-responsive and novel microRNAs in Populus tomentosa. Gene 504: pp. 160-5
13. Zhang, XN, Li, X, Liu, JH (2014) Identification of conserved and novel cold-Responsive microRNAs in trifoliate orange (Poncirus trifoliata (L.) Raf.) using high-throughput sequencing. Plant Mol Biol Rep 32: pp. 328-41
14. 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: pp. 2051-65
15. 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 103: pp. 29-38
16. Dong, Z, Shi, L, Wang, Y, Chen, L, Cai, Z, Wang, Y (2013) Identification and dynamic regulation of microRNAs involved in salt stress responses in functional soybean nodules by high-throughput sequencing. Int J Mol Sci 14: pp. 2717-38
17. Li, X, Bian, H, Song, D, Ma, S, Han, N, Wang, J (2013) Flowering time control in ornamental gloxinia (Sinningia speciosa) by manipulation of miR159 expression. Ann Bot 111: pp. 791-9
18. Zhu, J, Li, W, Yang, W, Qi, L, Han, S (2013) Identification of microRNAs in Caragana intermedia by high-throughput sequencing and expression analysis of 12 microRNAs and their targets under salt stress. Plant Cell Rep 32: pp. 1339-49
19. Li, H, Dong, Y, Yin, H, Wang, N, Yang, J, Liu, X (2011) Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol 11: pp. 170
20. Zhuang, Y, Zhou, XH, Liu, J (2014) Conserved miRNAs and their response to salt stress in wild Eggplant Solanum linnaeanum roots. Int J Mol Sci 15: pp. 839-49
21. Jiang, Q, Wang, F, Li, MY, Tan, HW, Ma, J, Xiong, AS (2014) High-throughput analysis of small RNAs and characterization of novel microRNAs affected by abiotic stress in a local celery cultivar. Sci Hortic 169: pp. 36-43
22. Tian, Y, Tian, Y, Luo, X, Zhou, T, Huang, Z, Liu, Y (2014) Identification and characterization of microRNAs related to salt stress in broccoli, using high-throughput sequencing and bioinformatics analysis. BMC Plant Biol 14: pp. 226
23. Wang, L, He, Q (2005) China radish. Scientific and Technical Documents Publishing House, Beijing
24. Xu, L, Wang, Y, Xu, Y, Wang, L, Zhai, L, Zhu, X (2013) Identification and characterization of novel and conserved microRNAs in radish (Raphanus sativus L.) using high-throughput sequencing. Plant Sci 201: pp. 108-14
25. Xu, L, Wang, Y, Zhai, L, Xu, Y, Wang, L, Zhu, X (2013) Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots. J Exp Bot 64: pp. 4271-87
26. Zhai, L, Xu, L, Wang, Y, Huang, D, Yu, R, Limera, C (2014) Genome-wide identification of embryogenesis-associated microRNAs in radish (Raphanus sativus L.) by high-throughput sequencing. Plant Mol Biol Rep 32: pp. 900-15
27. Wang Y, Liu W, Shen H, Zhu X, Zhai L, Xu L, et al. Identification of radish ( / Raphanus sativus L.) miRNAs and their target genes to explore miRNA-mediated regulatory networks in lead (Pb) stress responses by high-throughput sequencing and degradome analysis. Plant Mol Biol Rep. 2014. doi:10.1007/s11105-014-0752-y.
28. Yuan, G, Wang, X, Guo, R, Wang, Q (2010) Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chem 121: pp. 1014-9
29. Barakat, A, Wall, PK, DiLoreto, S, Carlson, JE (2007) Conservation and divergence of microRNAs in Populus. BMC Genomics 8: pp. 481
30. Pantaleo, V, Szittya, G, Moxon, S, Miozzi, L, Moulton, V, Dalmay, T (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62: pp. 960-76
31. Meyers, BC, Axtell, MJ, Bartel, B, Bartel, DP, Baulcombe, D, Bowman, JL (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20: pp. 3186-90
32. Srivastava, A, Rai, A, Patade, V, Suprasanna, P Calcium signaling and its significance in alleviating salt stress in plants. In: Ahmad, P, Azooz, MM, Prasad, MNV eds. (2013) Salt stress in plants: signalling, omics and adaptations. Springer, New York, pp. 197-218
33. Lu, S, Li, Q, Wei, H, Chang, MJ, Tunlaya, AS, Kim, H (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci U S A 110: pp. 10848-53
34. Kruszka, K, Pieczynski, M, Windels, D, Bielewicz, D, Jarmolowski, A, Szweykowska, KZ (2012) Role of microRNAs and other sRNAs of plants in their changing environments. J Plant Physiol 169: pp. 1664-72
35. Contreras, CC, Palomar, M, Arteaga, VM, Reyes, JL, Covarrubias, AA (2012) Non-coding RNAs in the plant response to abiotic stress. Planta 236: pp. 943-58
36. Zhao, B, Ge, L, Liang, R, Li, W, Ruan, K, Lin, H (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10: pp. 29
37. Zhu, C, Ding, Y, Liu, H (2011) MiR398 and plant stress responses. Physiol Plant 143: pp. 1-9
38. Woodrow, P, Pontecorvo, G, Ciarmiello, LF, Annunziata, MG, Fuggi, A, Carillo, P Transcription factors and genes in abiotic stress. In: Venkateswarlu, B, Shanker, AK, Shanker, C, Maheswari, M eds. (2012) Crop stress and its management: Perspectives and strategies. Springer, New York, pp. 317-57
39. Stephenson, TJ, McIntyre, CL, Collet, C, Xue, GP (2007) Genome-wide identification and expression analysis of the NF-Y family of transcription factors in Triticum aestivum. Plant Mol Biol 65: pp. 77-92
40. Fujita, M, Fujita, Y, Maruyama, K, Seki, M, Hiratsu, K, Ohme, TM (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39: pp. 863-76
41. Fang, Y, You, J, Xie, K, Xie, W, Xiong, L (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280: pp. 547-63
42. Puranik, S, Sahu, PP, Srivastava, PS, Prasad, M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17: pp. 369-81
43. Hao, YJ, Wei, W, Song, QX, Chen, HW, Zhang, YQ, Wang, F (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68: pp. 302-13
44. Kim, SG, Kim, SY, Park, CM (2007) A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226: pp. 647-54
45. Yang, SD, Seo, PJ, Yoon, HK, Park, CM (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23: pp. 2155-68
46. Rubio, SI, Cuperus, JT, Weigel, D, Carrington, JC (2009) Regulation and functional specialization of small RNA-target nodes during plant development. Curr Opin Plant Biol 12: pp. 622-7
47. Zhu, QH, Helliwell, CA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62: pp. 487-95
48. Schwab, R Roles of miR156 and miR172 in reproductive development. In: Sunkar, R eds. (2012) MicroRNAs in plant development and stress responses. New York, Springer, pp. 69-81
49. Jagadeeswaran, G, Saini, A, Sunkar, R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229: pp. 1009-14
50. Maruta, T, Inoue, T, Noshi, M, Tamoi, M, Yabuta, Y, Yoshimura, K (2012) Cytosolic ascorbate peroxidase 1 protects organelles against oxidative stress by wounding- and jasmonate-induced H2O2 in Arabidopsis plants. Biochim Biophys Acta-Gen Subj 1820: pp. 1901-7
51. Matsui, A, Nguyen, AH, Nakaminami, K, Seki, M (2013) Arabidopsis non-coding RNA regulation in abiotic stress responses. Int J Mol Sci 14: pp. 22642-54
52. Yamasaki, H, Abdel-Ghany, SE, Cohu, CM, Kobayashi, Y, Shikanai, T, Pilon, M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282: pp. 16369-78
53. Fujii, H, Chiou, TJ, Lin, SI, Aung, K, Zhu, JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15: pp. 2038-43
54. Hackenberg, M, Shi, BJ, Gustafson, P, Langridge, P (2013) Characterization of phosphorus-regulated miR399 and miR827 and their isomirs in barley under phosphorus-sufficient and phosphorus-deficient conditions. BMC Plant Biol 13: pp. 214
55. Chinnusamy, V, Zhu, J, Zhu, JK Salt stress signaling and mechanisms of plant salt tolerance. In: Setlow, JK eds. (2006) Genetic engineering: Principles and Methods. Springer, New York, pp. 141-77
56. Xu, L, Wang, L, Gong, Y, Dai, W, Wang, Y, Zhu, X (2012) Genetic linkage map construction and QTL mapping of cadmium accumulation in radish (Raphanus sativus L.). Theor Appl Genet 125: pp. 659-70
57. Hafner, M, Landgraf, P, Ludwig, J, Rice, A, Ojo, T, Lin, C (2008) Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods 44: pp. 3-12
58. Barvkar, VT, Pardeshi, VC, Kale, SM, Qiu, S, Rollins, M, Datla, R (2013) Genome-wide identification and characterization of microRNA genes and their targets in flax (Linum usitatissimum). Planta 237: pp. 1149-61
59. Allen, E, Xie, Z, Gustafson, AM, Carrington, JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: pp. 207-21
60. Schwab, R, Palatnik, JF, Riester, M, Schommer, C, Schmid, M, Weigel, D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8: pp. 517-27
61. Galla, G, Barcaccia, G, Ramina, A, Collani, S, Alagna, F, Baldoni, L (2009) Computational annotation of genes differentially expressed along olive fruit development. BMC Plant Biol 9: pp. 128 - 刊物主题：Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
- 出版者：BioMed Central
- ISSN：1471-2164
文摘
Background Salt stress is one of the most representative abiotic stresses that severely affect plant growth and development. MicroRNAs (miRNAs) are well known for their significant involvement in plant responses to abiotic stresses. Although miRNAs implicated in salt stress response have been widely reported in numerous plant species, their regulatory roles in the adaptive response to salt stress in radish (Raphanus sativus L.), an important root vegetable crop worldwide, remain largely unknown. Results Solexa sequencing of two sRNA libraries from NaCl-free (CK) and NaCl-treated (Na200) radish roots were performed for systematical identification of salt-responsive miRNAs and their expression profiling in radish. Totally, 136 known miRNAs (representing 43 miRNA families) and 68 potential novel miRNAs (belonging to 51 miRNA families) were identified. Of these miRNAs, 49 known and 22 novel miRNAs were differentially expressed under salt stress. Target prediction and annotation indicated that these miRNAs exerted a role by regulating specific stress-responsive genes, such as squamosa promoter binding-like proteins (SPLs), auxin response factors (ARFs), nuclear transcription factor Y (NF-Y) and superoxide dismutase [Cu-Zn] (CSD1). Further functional analysis suggested that these target genes were mainly implicated in signal perception and transduction, regulation of ion homeostasis, basic metabolic processes, secondary stress responses, as well as modulation of attenuated plant growth and development under salt stress. Additionally, the expression patterns of ten miRNAs and five corresponding target genes were validated by reverse-transcription quantitative PCR (RT-qPCR). Conclusions With the sRNA sequencing, salt-responsive miRNAs and their target genes in radish were comprehensively identified. The results provide novel insight into complex miRNA-mediated regulatory network of salt stress response in radish, and facilitate further dissection of molecular mechanism underlying plant adaptive response to salt stress in root vegetable crops.