期刊论文详细信息
BMC Genomics
Integrated analysis of miRNA and mRNA expression profiles in response to Cd exposure in rice seedlings
Caiyan Chen3  Shuhui Song1  Dayong Li2  Liwei Xu3  Donghai Mao3  Mingfeng Tang3 
[1]Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100029, China
[2]State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
[3]Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha 410125, China
关键词: Rice;    High-throughput deep sequencing;    mRNA;    miRNA;    Cd stress;   
Others  :  1139343
DOI  :  10.1186/1471-2164-15-835
 received in 2014-04-20, accepted in 2014-09-24,  发布年份 2014
PDF
【 摘 要 】

Background

Independent transcriptome profile analyses of miRNAs or mRNAs under conditions of cadmium (Cd) stress have been widely reported in plants. However, a combined analysis of sRNA sequencing expression data with miRNA target expression data to infer the relative activities of miRNAs that regulate gene expression changes resulting from Cd stress has not been reported in rice. To elucidate the roles played by miRNAs in the regulation of changes in gene expression in response to Cd stress in rice (Oryza sativa L.), we simultaneously characterized changes in the miRNA and mRNA profiles following treatment with Cd.

Results

A total of 163 miRNAs and 2,574 mRNAs were identified to be differentially expressed under Cd stress, and the changes in the gene expression profile in the shoot were distinct from those in the root. At the miRNA level, 141 known miRNAs belonging to 48 families, and 39 known miRNAs in 23 families were identified to be differentially expressed in the root and shoot, respectively. In addition, we identified eight new miRNA candidates from the root and five from the shoot that were differentially expressed in response to Cd treatment. For the mRNAs, we identified 1,044 genes in the root and 448 genes in the shoot that were up-regulated, while 572 and 645 genes were down-regulated in the root and shoot, respectively. GO and KEGG enrichment analyses showed that genes encoding secondary, metabolite synthases, signaling molecules, and ABC transporters were significantly enriched in the root, while only ribosomal protein and carotenoid biosynthesis genes were significantly enriched in the shoot. Then 10 known miRNA-mRNA interaction pairs and six new candidate ones, that showed the opposite expression patterns, were identified by aligning our two datasets against online databases and by using the UEA sRNA toolkit respectively.

Conclusions

This study is the first to use high throughput DNA sequencing to simultaneously detect changes in miRNA and mRNA expression patterns in the root and shoot in response to Cd treatment. These integrated high-throughput expression data provide a valuable resource to examine global genome expression changes in response to Cd treatment and how these are regulated by miRNAs.

【 授权许可】

   
2014 Tang et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150321095152557.pdf 2053KB PDF download
Figure 8. 85KB Image download
Figure 7. 53KB Image download
Figure 6. 51KB Image download
Figure 5. 69KB Image download
Figure 4. 100KB Image download
Figure 3. 95KB Image download
Figure 2. 77KB Image download
Figure 1. 21KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】
  • [1]Bertin G, Averbeck D: Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 2006, 88(11):1549-1559.
  • [2]Nawrot T, Plusquin M, Hogervorst J, Roels HA, Celis H, Thijs L, Vangronsveld J, Van Hecke E, Staessen JA: Environmental exposure to cadmium and risk of cancer: a prospective population-based study. Lancet Oncol 2006, 7(2):119-126.
  • [3]Watanabe T, Shimbo S, Moon C-S, Zhang Z-W, Ikeda M: Cadmium contents in rice samples from various areas in the world. Sci Total Environ 1996, 184(3):191-196.
  • [4]Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116(2):281-297.
  • [5]Guo H-S, Xie Q, Fei J-F, Chua N-H: MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 2005, 17(5):1376-1386.
  • [6]Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D: Control of leaf morphogenesis by microRNAs. Nature 2003, 425(6955):257-263.
  • [7]Aukerman MJ, Sakai H: Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 2003, 15(11):2730-2741.
  • [8]Sunkar R, Kapoor A, Zhu J-K: 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 2006, 18(8):2051-2065.
  • [9]Abdel-Ghany SE, Pilon M: MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 2008, 283(23):15932-15945.
  • [10]Kawashima CG, Matthewman CA, Huang S, Lee BR, Yoshimoto N, Koprivova A, Rubio‒Somoza I, Todesco M, Rathjen T, Saito K: Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 2011, 66(5):863-876.
  • [11]Fujii H, Chiou T-J, Lin S-I, Aung K, Zhu J-K: A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 2005, 15(22):2038-2043.
  • [12]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(5):836-843.
  • [13]Ding Y, Chen Z, Zhu C: Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 2011, 62(10):3563-3573.
  • [14]Huang SQ, Peng J, Qiu CX, Yang ZM: Heavy metal-regulated new microRNAs from rice. J Inorg Biochem 2009, 103(2):282-287.
  • [15]Ding Y, Qu A, Gong S, Huang S, Lv B, Zhu C: Molecular identification and analysis of Cd-responsive microRNAs in rice. J Agric Food Chem 2013, 61(47):11668-11675.
  • [16]Zhou ZS, Huang SQ, Yang ZM: Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochem Biophys Res Commun 2008, 374(3):538-542.
  • [17]Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette M-L, Cuine S, Auroy P, Richaud P, Forestier C, Bourguignon J: Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 2006, 88(11):1751-1765.
  • [18]ROMERO‒PUERTAS M, RODRÍGUEZ‒SERRANO M, Corpas F, Gomez M, Del Rio L, Sandalio L: Cadmium-induced subcellular accumulation of O2·- and H2O2 in pea leaves. Plant Cell Environ 2004, 27(9):1122-1134.
  • [19]Sandalio L, Dalurzo H, Gomez M, Romero‒Puertas M, Del Rio L: Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 2001, 52(364):2115-2126.
  • [20]Benavides MP, Gallego SM, Tomaro ML: Cadmium toxicity in plants. Braz J Plant Physiol 2005, 17(1):21-34.
  • [21]Clemens S, Palmgren MG, Krämer U: A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 2002, 7(7):309-315.
  • [22]Cobbett CS: Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 2000, 123(3):825-832.
  • [23]Ogawa I, Nakanishi H, Mori S, Nishizawa NK: Time course analysis of gene regulation under cadmium stress in rice. Plant Soil 2009, 325(1–2):97-108.
  • [24]Zhou ZS, Zeng HQ, Liu ZP, Yang ZM: Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 2012, 35(1):86-99.
  • [25]Zhou ZS, Song JB, Yang ZM: Genome-wide identification of Brassica napus microRNAs and their targets in response to cadmium. J Exp Bot 2012, 63(12):4597-4613.
  • [26]Wei Y, Chen S, Yang P, Ma Z, Kang L: Characterization and comparative profiling of the small RNA transcriptomes in two phases of locust. Genome Biol 2009, 10(1):R6. BioMed Central Full Text
  • [27]Wang L, Liu H, Li D, Chen H: Identification and characterization of maize microRNAs involved in the very early stage of seed germination. BMC Genomics 2011, 12(1):154. BioMed Central Full Text
  • [28]Han Y, Chen J, Zhao X, Liang C, Wang Y, Sun L, Jiang Z, Zhang Z, Yang R, Chen J: MicroRNA expression signatures of bladder cancer revealed by deep sequencing. PLoS One 2011, 6(3):e18286.
  • [29]Li R, Yu C, Li Y, Lam T-W, Yiu S-M, Kristiansen K, Wang J: SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009, 25(15):1966-1967.
  • [30]Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, Eddy SR, Gardner PP, Bateman A: Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 2013, 41(D1):D226-D232.
  • [31]Kozomara A, Griffiths-Jones S: miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011, 39(suppl 1):D152-D157.
  • [32]Kozomara A, Griffiths-Jones S: miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014, 42(D1):D68-D73.
  • [33]Li Y, Zhang Z, Liu F, Vongsangnak W, Jing Q, Shen B: Performance comparison and evaluation of software tools for microRNA deep-sequencing data analysis. Nucleic Acids Res 2012, 40(10):4298-4305.
  • [34]Moxon S, Schwach F, Dalmay T, MacLean D, Studholme DJ, Moulton V: A toolkit for analysing large-scale plant small RNA datasets. Bioinformatics 2008, 24(19):2252-2253.
  • [35]A.C.'t Hoen P, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, De Menezes RX, Boer JM, Van Ommen G-JB, Den Dunnen JT: Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 2008, 36(21):e141-e141.
  • [36]Du Z, Zhou X, Ling Y, Zhang Z, Su Z: agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010, 38(suppl 2):W64-W70.
  • [37]Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T: KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008, 36(suppl 1):D480-D484.
  • [38]Kanehisa M, Goto S: KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000, 28(1):27-30.
  • [39]Eisen MB, Spellman PT, Brown PO, Botstein D: Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 1998, 95(25):14863-14868.
  • [40]Kawahara Y, de la Bastide M, Hamilton J, Kanamori H, McCombie WR, Ouyang S, Schwartz D, Tanaka T, Wu J, Zhou S: Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 2013, 6(1):1-10. BioMed Central Full Text
  • [41]Wang Y-P, Li K-B: Correlation of expression profiles between microRNAs and mRNA targets using NCI-60 data. Bmc Genomics 2009, 10(1):218. BioMed Central Full Text
  • [42]Cheng C, Li LM: Inferring microRNA activities by combining gene expression with microRNA target prediction. PloS One 2008, 3(4):e1989.
  • [43]Zhang Z, Yu J, Li D, Zhang Z, Liu F, Zhou X, Wang T, Ling Y, Su Z: PMRD: plant microRNA database. Nucleic Acids Res 2010, 38(suppl 1):D806-D813.
  • [44]Yang J-H, Li J-H, Shao P, Zhou H, Chen Y-Q, Qu L-H: starBase: a database for exploring microRNA–mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data. Nucleic Acids Res 2011, 39(suppl 1):D202-D209.
  • [45]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):25. BioMed Central Full Text
  • [46]Delhaize E, Ryan PR: Aluminum toxicity and tolerance in plants. Plant Physiol 1995, 107(2):315.
  • [47]Sanita Di Toppi L, Gabbrielli R: Response to cadmium in higher plants. Environ Exp Bot 1999, 41(2):105-130.
  • [48]DalCorso G, Farinati S, Maistri S, Furini A: How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol 2008, 50(10):1268-1280.
  • [49]Lin C-Y, Trinh NN, Fu S-F, Hsiung Y-C, Chia L-C, Lin C-W, Huang H-J: Comparison of early transcriptome responses to copper and cadmium in rice roots. Plant Mol Biol 2013, 81(4–5):507-522.
  • [50]Weber M, Trampczynska A, Clemens S: Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd(2+)-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 2006, 29(5):950-963.
  • [51]Suzuki N, Koizumi N, Sano H: Screening of cadmium-responsive genes in Arabidopsis thaliana. Plant Cell Environ 2001, 24(11):1177-1188.
  • [52]Korobeinikova A, Garber M, Gongadze G: Ribosomal proteins: structure, function, and evolution. Biochemistry (Mosc) 2012, 77(6):562-574.
  • [53]Bae W, Chen X: Proteomic study for the cellular responses to Cd2+ in Schizosaccharomyces pombe Through amino acid-coded mass tagging and liquid chromatography tandem mass spectrometry. Mol Cell Proteomics 2004, 3(6):596-607.
  • [54]Sormani R, Masclaux-Daubresse C, Daniele-Vedele F, Chardon F: Transcriptional regulation of ribosome components are determined by stress according to cellular compartments in Arabidopsis thaliana. PloS One 2011, 6(12):e28070.
  • [55]Howitt CA, Pogson BJ: Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ 2006, 29(3):435-445.
  • [56]Fernández R, Bertrand A, Reis R, Mourato MP, Martins LL, González A: Growth and physiological responses to cadmium stress of two populations of Dittrichia viscosa (L.) Greuter. J Hazard Mater 2013, 244–245:555-562.
  • [57]Jiang H-p, Gao B-b, Li W-h, Zhu M, Zheng C-f, Zheng Q-s, Wang C-h: Physiological and Biochemical Responses of Ulva prolifera and Ulva linza to Cadmium Stress. Sci World J 2013, 2013:11.
  • [58]Lu S, Li L: Carotenoid metabolism: biosynthesis, regulation, and beyond. J Integr Plant Biol 2008, 50(7):778-785.
  • [59]Li S-W, Leng Y, Feng L, Zeng X-Y: Involvement of abscisic acid in regulating antioxidative defense systems and IAA-oxidase activity and improving adventitious rooting in mung bean [Vigna radiata (L.) Wilczek] seedlings under cadmium stress. Environ Sci Pollut Res 2014, 21(1):525-537.
  • [60]F-b W, Dong J, Jia G-x, Zheng S-j, Zhang G-p: Genotypic difference in the responses of seedling growth and Cd toxicity in rice (Oryza sativa L.). Agric Sci China 2006, 5(1):68-76.
  • [61]Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP: Prediction of plant microRNA targets. Cell 2002, 110(4):513-520.
  • [62]Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O: Widespread translational inhibition by plant miRNAs and siRNAs. Science 2008, 320(5880):1185-1190.
  • [63]Pei H, Ma N, Chen J, Zheng Y, Tian J, Li J, Zhang S, Fei Z, Gao J: Integrative analysis of miRNA and mRNA profiles in response to ethylene in rose petals during flower opening. PloS One 2013, 8(5):e64290.
  • [64]Thoden JB, Hegeman AD, Wesenberg G, Chapeau MC, Frey PA, Holden HM: Structural analysis of UDP-sugar binding to UDP-galactose 4-epimerase from Escherichia coli. Biochemistry 1997, 36(21):6294-6304.
  • [65]Fusco N, Micheletto L, Dal Corso G, Borgato L, Furini A: Identification of cadmium-regulated genes by cDNA-AFLP in the heavy metal accumulator Brassica juncea L. J Exp Bot 2005, 56(421):3017-3027.
  • [66]Van de Mortel JE, Schat H, Moerland PD, Van Themaat EVL, van der Ent S, Blankestijn H, Ghandilyan A, Tsiatsiani S, Aarts MG: Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 2008, 31(3):301-324.
  文献评价指标  
  下载次数:36次 浏览次数:18次