Advertisement

Plant Molecular Biology

, Volume 83, Issue 4–5, pp 459–473 | Cite as

Genome-wide annotation of genes and noncoding RNAs of foxtail millet in response to simulated drought stress by deep sequencing

  • Xin Qi
  • Shaojun Xie
  • Yuwei Liu
  • Fei Yi
  • Jingjuan YuEmail author
Article

Abstract

Drought is a major abiotic stress that affects plant growth, production, and survival. Plants have evolved sophisticated and highly complex reactions to drought stress, including large-scale transcriptome reconfiguration. Foxtail millet (Setaria italica) is a member of the Poaceae family. Because of its outstanding tolerance to drought stress foxtail millet has the potential to become a new model organism. To enrich our knowledge of the processes that contribute to drought resistance, we have used a deep sequencing approach to generate a genome-wide transcriptome of foxtail millet after exposure to simulated drought stress. A large number of differentially expressed genes were characterized; in particular, we examined the roles of small interfering RNAs (siRNAs) and long noncoding RNAs (lncRNAs) in response to a water-deficit condition. These RNAs have remained largely unexplored in previous studies of stress-induced transcriptomes. We found that the reduced levels of 24-nt siRNA flanking genes were associated, for the most part, with proximal up-regulated genes, indicating a potential effect of 24-nt siRNAs on drought-regulated gene expression. Several lncRNAs that responded to the simulated drought stress were also identified, and we found that one of them shared sequence conservation and colinearity with its counterpart in sorghum (Sorghum bicolor). Our findings provide new insights into drought-induced changes in the foxtail millet transcriptome.

Keywords

Drought stress Foxtail millet Transcriptome siRNA Long noncoding RNA 

Notes

Acknowledgments

We thank Prof. Xianmin Diao (Chinese Academy of Agricultural Sciences) for providing the Yugu1 foxtail millet seeds. We also thank Dr. Kerstin Mueller (Simon Fraser University, Canada) for critical reading of this manuscript. This work was supported by the National Basic Research Program of China (Grant No. 2012CB215301) and the National Transgenic Major Program of China (Grant No. 2009ZX08009-093B).

Supplementary material

11103_2013_104_MOESM1_ESM.tif (805 kb)
Supplementary material 1 (TIFF 804 kb)
11103_2013_104_MOESM2_ESM.tif (2.3 mb)
Supplementary material 2 (TIFF 2357 kb)
11103_2013_104_MOESM3_ESM.tif (1.9 mb)
Supplementary material 3 (TIFF 1942 kb)
11103_2013_104_MOESM4_ESM.tif (12.1 mb)
Supplementary material 4 (TIFF 12407 kb)
11103_2013_104_MOESM5_ESM.tif (2.3 mb)
Supplementary material 5 (TIFF 2316 kb)
11103_2013_104_MOESM6_ESM.tif (4.5 mb)
Supplementary material 6 (TIFF 4563 kb)
11103_2013_104_MOESM7_ESM.tif (1.4 mb)
Supplementary material 7 (TIFF 1420 kb)
11103_2013_104_MOESM8_ESM.tif (680 kb)
Supplementary material 8 (TIFF 680 kb)
11103_2013_104_MOESM9_ESM.tif (1.2 mb)
Supplementary material 9 (TIFF 1208 kb)
11103_2013_104_MOESM10_ESM.tif (5.5 mb)
Supplementary material 10 (TIFF 5609 kb)
11103_2013_104_MOESM11_ESM.tif (3.9 mb)
Supplementary material 11 (TIFF 4033 kb)
11103_2013_104_MOESM12_ESM.xlsx (12 kb)
Supplementary material 12 (XLSX 12 kb)
11103_2013_104_MOESM13_ESM.xls (18 kb)
Supplementary material 13 (XLS 18 kb)
11103_2013_104_MOESM14_ESM.xls (292 kb)
Supplementary material 14 (XLS 291 kb)
11103_2013_104_MOESM15_ESM.xlsx (46 kb)
Supplementary material 15 (XLSX 45 kb)
11103_2013_104_MOESM16_ESM.xlsx (14 kb)
Supplementary material 16 (XLSX 13 kb)
11103_2013_104_MOESM17_ESM.xlsx (11 kb)
Supplementary material 17 (XLSX 11 kb)
11103_2013_104_MOESM18_ESM.xlsx (10 kb)
Supplementary material 18 (XLSX 10 kb)
11103_2013_104_MOESM19_ESM.xls (24 kb)
Supplementary material 19 (XLS 23 kb)
11103_2013_104_MOESM20_ESM.xlsx (11 kb)
Supplementary material 20 (XLSX 10 kb)
11103_2013_104_MOESM21_ESM.xlsx (21 kb)
Supplementary material 21 (XLSX 21 kb)
11103_2013_104_MOESM22_ESM.xlsx (99 kb)
Supplementary material 22 (XLSX 98 kb)
11103_2013_104_MOESM23_ESM.xlsx (14 kb)
Supplementary material 23 (XLSX 13 kb)
11103_2013_104_MOESM24_ESM.docx (15 kb)
Supplementary material 24 (DOCX 15 kb)

References

  1. Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12(9):419–426PubMedCrossRefGoogle Scholar
  2. Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24(5):701–713PubMedCrossRefGoogle Scholar
  3. Barber WT, Zhang W, Win H, Varala KK, Dorweiler JE, Hudson ME, Moose SP (2012) Repeat associated small RNAs vary among parents and following hybridization in maize. Proc Natl Acad Sci USA 109:10444–10449PubMedCrossRefGoogle Scholar
  4. Ben Amor B, Wirth S, Merchan F, Laporte P, d’Aubenton-Carafa Y, Hirsch J, Maizel A, Mallory A, Lucas A, Deragon JM, Vaucheret H, Thermes C, Crespi M (2009) Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 19(1):57–69PubMedCrossRefGoogle Scholar
  5. Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X, Wu X, Mitros T, Triplett J, Yang X, Ye CY, Mauro-Herrera M, Wang L, Li P, Sharma M, Sharma R, Ronald PC, Panaud O, Kellogg EA, Brutnell TP, Doust AN, Tuskan GA, Rokhsar D, Devos KM (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30:555–561PubMedCrossRefGoogle Scholar
  6. Boerner S, McGinnis KM (2012) Computational Identification and Functional Predictions of Long Noncoding RNA in Zea mays. PLoS ONE 7(8):e43047PubMedCrossRefGoogle Scholar
  7. Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123(7):1279–1291PubMedCrossRefGoogle Scholar
  8. Boyer JS (1982) Plant productivity and environment. Science 218(4571):443–448PubMedCrossRefGoogle Scholar
  9. Broin M, Cuine S, Peltier G, Rey P (2000) Involvement of CDSP 32, a drought-induced thioredoxin, in the response to oxidative stress in potato plants. FEBS Lett 467(2–3):245–248PubMedCrossRefGoogle Scholar
  10. Bumgarner SL, Dowell RD, Grisafi P, Gifford DK, Fink GR (2009) Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast. Proc Natl Acad Sci USA 106(43):18321–18326PubMedCrossRefGoogle Scholar
  11. Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, Eddy SR, Gardner PP, Bateman A (2013) Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 41(D1):D226–D232PubMedCrossRefGoogle Scholar
  12. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25(18):1915–1927PubMedCrossRefGoogle Scholar
  13. Cantu D, Vanzetti LS, Sumner A, Dubcovsky M, Matvienko M, Distelfeld A, Michelmore RW, Dubcovsky J (2010) Small RNAs, DNA methylation and transposable elements in wheat. BMC Genomics 11:408PubMedCrossRefGoogle Scholar
  14. Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S, Fedele S, Pesce E, Ferrer I, Collavin L, Santoro C, Forrest AR, Carninci P, Biffo S, Stupka E, Gustincich S (2012) Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 494:454–457CrossRefGoogle Scholar
  15. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676PubMedCrossRefGoogle Scholar
  16. Davidson RM, Gowda M, Moghe G, Lin H, Vaillancourt B, Shiu SH, Jiang N, Robin Buell C (2012) Comparative transcriptomics of three Poaceae species reveals patterns of gene expression evolution. Plant J 71(3):492–502PubMedGoogle Scholar
  17. De Lucia F, Dean C (2011) Long non-coding RNAs and chromatin regulation. Curr Opin Plant Biol 14(2):168–173PubMedCrossRefGoogle Scholar
  18. Deepak S, Shailasree S, Kini RK, Hause B, Shetty SH, Mithofer A (2007) Role of hydroxyproline-rich glycoproteins in resistance of pearl millet against downy mildew pathogen Sclerospora graminicola. Planta 226(2):323–333PubMedCrossRefGoogle Scholar
  19. Dezar CA, Gago GM, Gonzalez DH, Chan RL (2005) Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Res 14(4):429–440PubMedCrossRefGoogle Scholar
  20. Diao Xianmin (2005) Advances in foxtail millet biotechnology and its future directions. J Hebei Agric Sci 9:61–68Google Scholar
  21. Diao Xianmin (2007) Foxtail millet production in China and its future development tendency. In: Chai Y, Wan FS (eds) The industrial development of China special crops. Chinese Agricultural Science and Technology Press, Beijing, pp 32–43Google Scholar
  22. Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J, Zhang Q (2012) A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci USA 109(7):2654–2659PubMedCrossRefGoogle Scholar
  23. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci USA 109(32):E2183–E2191PubMedCrossRefGoogle Scholar
  24. Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33(4):751–763PubMedCrossRefGoogle Scholar
  25. Dugas DV, Monaco MK, Olsen A, Klein RR, Kumari S, Ware D, Klein PE (2011) Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid. BMC Genomics 12:514PubMedCrossRefGoogle Scholar
  26. Ergen NZ, Thimmapuram J, Bohnert HJ, Budak H (2009) Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Funct Integr Genomics 9(3):377–396PubMedCrossRefGoogle Scholar
  27. Goday A, Jensen AB, Culianez-Macia FA, Mar Alba M, Figueras M, Serratosa J, Torrent M, Pages M (1994) The maize abscisic acid-responsive protein Rab17 is located in the nucleus and interacts with nuclear localization signals. Plant Cell 6(3):351–360PubMedGoogle Scholar
  28. Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 131(4):1855–1867PubMedCrossRefGoogle Scholar
  29. Groszmann M, Greaves IK, Albertyn ZI, Scofield GN, Peacock WJ, Dennis ES (2011) Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc Natl Acad Sci USA 108(6):2617–2622PubMedCrossRefGoogle Scholar
  30. Guilfoyle TJ, Ulmasov T, Hagen G (1998) The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol Life Sci 54(7):619–627PubMedCrossRefGoogle Scholar
  31. Guo AY, Chen X, Gao G, Zhang H, Zhu QH, Liu XC, Zhong YF, Gu X, He K, Luo J (2008) PlantTFDB: a comprehensive plant transcription factor database. Nucleic Acids Res 36(Database issue):D966–D969PubMedGoogle Scholar
  32. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458(7235):223–227PubMedCrossRefGoogle Scholar
  33. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477(7364):295–300PubMedCrossRefGoogle Scholar
  34. Hall Q, Cannon MC (2002) The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell 14(5):1161–1172PubMedCrossRefGoogle Scholar
  35. Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331(6013):76–79PubMedCrossRefGoogle Scholar
  36. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27(1):297–300PubMedCrossRefGoogle Scholar
  37. Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472(7341):115–119PubMedCrossRefGoogle Scholar
  38. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27(4):325–333PubMedCrossRefGoogle Scholar
  39. Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7(3):106–111PubMedCrossRefGoogle Scholar
  40. Jayaraman A, Puranik S, Rai NK, Vidapu S, Sahu PP, Lata C, Prasad M (2008) cDNA-AFLP analysis reveals differential gene expression in response to salt stress in foxtail millet (Setaria italica L.). Mol Biotechnol 40(3):241–251PubMedCrossRefGoogle Scholar
  41. Kakumanu A, Ambavaram MM, Klumas CM, Krishnan A, Batlang U, Myers E, Grene R, Pereira A (2012) Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol 160:846–867PubMedCrossRefGoogle Scholar
  42. Kim ED, Sung S (2012) Long noncoding RNA: unveiling hidden layer of gene regulatory networks. Trends Plant Sci 17(1):16–21PubMedCrossRefGoogle Scholar
  43. Kim S, Kang JY, Cho DI, Park JH, Kim SY (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40(1):75–87PubMedCrossRefGoogle Scholar
  44. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, Markenscoff-Papadimitriou E, Kuhl D, Bito H, Worley PF, Kreiman G, Greenberg ME (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465(7295):182–187PubMedCrossRefGoogle Scholar
  45. Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35(Web Server issue):W345–W349PubMedCrossRefGoogle Scholar
  46. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39(Database issue):D152–D157PubMedCrossRefGoogle Scholar
  47. Kumagai T, Ito S, Nakamichi N, Niwa Y, Murakami M, Yamashino T, Mizuno T (2008) The common function of a novel subfamily of B-Box zinc finger proteins with reference to circadian-associated events in Arabidopsis thaliana. Biosci Biotechnol Biochem 72(6):1539–1549PubMedCrossRefGoogle Scholar
  48. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):R25PubMedCrossRefGoogle Scholar
  49. Lata C, Sahu PP, Prasad M (2010) Comparative transcriptome analysis of differentially expressed genes in foxtail millet (Setaria italica L.) during dehydration stress. Biochem Biophys Res Commun 393(4):720–727PubMedCrossRefGoogle Scholar
  50. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11(3):204–220PubMedCrossRefGoogle Scholar
  51. Lenka SK, Katiyar A, Chinnusamy V, Bansal KC (2011) Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance. Plant Biotechnol J 9(3):315–327PubMedCrossRefGoogle Scholar
  52. Li P, Brutnell TP (2011) Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses. J Exp Bot 62(9):3031–3037PubMedCrossRefGoogle Scholar
  53. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell TP (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42(12):1060–1067PubMedCrossRefGoogle Scholar
  54. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430(6998):471–476PubMedCrossRefGoogle Scholar
  55. Liu XD, Thiele DJ (1996) Oxidative stress induced heat shock factor phosphorylation and HSF-dependent activation of yeast metallothionein gene transcription. Genes Dev 10(5):592–603PubMedCrossRefGoogle Scholar
  56. Liu J, Jung C, Xu J, Wang H, Deng S, Bernad L, Arenas-Huertero C, Chua NH (2012) Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24:4333–4345PubMedCrossRefGoogle Scholar
  57. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408PubMedCrossRefGoogle Scholar
  58. Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Huang X, Han B (2010) Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res 20(9):1238–1249PubMedCrossRefGoogle Scholar
  59. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49(8):1135–1149PubMedCrossRefGoogle Scholar
  60. Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10(3):155–159PubMedCrossRefGoogle Scholar
  61. Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11(1):31–46PubMedCrossRefGoogle Scholar
  62. Moran VA, Perera RJ, Khalil AM (2012) Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res 40(14):6391–6400PubMedCrossRefGoogle Scholar
  63. Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41(5):697–709PubMedCrossRefGoogle Scholar
  64. Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149(1):88–95PubMedCrossRefGoogle Scholar
  65. Nobuta K, Venu RC, Lu C, Belo A, Vemaraju K, Kulkarni K, Wang W, Pillay M, Green PJ, Wang GL, Meyers BC (2007) An expression atlas of rice mRNAs and small RNAs. Nat Biotechnol 25(4):473–477PubMedCrossRefGoogle Scholar
  66. Nobuta K, Lu C, Shrivastava R, Pillay M, De Paoli E, Accerbi M, Arteaga-Vazquez M, Sidorenko L, Jeong DH, Yen Y, Green PJ, Chandler VL, Meyers BC (2008) Distinct size distribution of endogeneous siRNAs in maize: evidence from deep sequencing in the mop1-1 mutant. Proc Natl Acad Sci USA 105(39):14958–14963PubMedCrossRefGoogle Scholar
  67. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, Guigo R, Shiekhattar R (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143(1):46–58PubMedCrossRefGoogle Scholar
  68. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, Schier AF (2012) Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 22(3):577–591PubMedCrossRefGoogle Scholar
  69. Phillips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581(19):3592–3597PubMedCrossRefGoogle Scholar
  70. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26(6):841–842PubMedCrossRefGoogle Scholar
  71. Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu JK, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63:417–429CrossRefGoogle Scholar
  72. Reynolds A, Leake D, Boese Q, Scaringe S, Marshall WS, Khvorova A (2004) Rational siRNA design for RNA interference. Nat Biotechnol 22(3):326–330PubMedCrossRefGoogle Scholar
  73. Robson F, Costa MM, Hepworth SR, Vizir I, Pineiro M, Reeves PH, Putterill J, Coupland G (2001) Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J 28(6):619–631PubMedCrossRefGoogle Scholar
  74. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18(5):1292–1309PubMedCrossRefGoogle Scholar
  75. Salleh FM, Evans K, Goodall B, Machin H, Mowla SB, Mur LA, Runions J, Theodoulou FL, Foyer CH, Rogers HJ (2012) A novel function for a redox-related LEA protein (SAG21/AtLEA5) in root development and biotic stress responses. Plant, Cell Environ 35(2):418–429CrossRefGoogle Scholar
  76. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27(6):863–864PubMedCrossRefGoogle Scholar
  77. Schweighofer A, Hirt H, Meskiene I (2004) Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci 9(5):236–243PubMedCrossRefGoogle Scholar
  78. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13(1):61–72PubMedGoogle Scholar
  79. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31(3):279–292PubMedCrossRefGoogle Scholar
  80. Shen Q, Ho TH (1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7(3):295–307PubMedGoogle Scholar
  81. Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3(3):217–223PubMedGoogle Scholar
  82. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6(5):410–417PubMedCrossRefGoogle Scholar
  83. Singh K, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5(5):430–436PubMedCrossRefGoogle Scholar
  84. Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12(7):301–309PubMedCrossRefGoogle Scholar
  85. Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462(7274):799–802PubMedCrossRefGoogle Scholar
  86. Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97PubMedCrossRefGoogle Scholar
  87. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515PubMedCrossRefGoogle Scholar
  88. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562–578PubMedCrossRefGoogle Scholar
  89. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329(5992):689–693PubMedCrossRefGoogle Scholar
  90. Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP (2011) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147(7):1537–1550PubMedCrossRefGoogle Scholar
  91. Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96(10):5844–5849PubMedCrossRefGoogle Scholar
  92. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97(21):11632–11637PubMedCrossRefGoogle Scholar
  93. Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M (2009) A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant, Cell Environ 32(9):1211–1229CrossRefGoogle Scholar
  94. Veljovic-Jovanovic S, Kukavica B, Stevanovic B, Navari-Izzo F (2006) Senescence- and drought-related changes in peroxidase and superoxide dismutase isoforms in leaves of Ramonda serbica. J Exp Bot 57(8):1759–1768PubMedCrossRefGoogle Scholar
  95. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63PubMedCrossRefGoogle Scholar
  96. Wang B, Guo G, Wang C, Lin Y, Wang X, Zhao M, Guo Y, He M, Zhang Y, Pan L (2010a) Survey of the transcriptome of Aspergillus oryzae via massively parallel mRNA sequencing. Nucleic Acids Res 38(15):5075–5087PubMedCrossRefGoogle Scholar
  97. Wang L, Feng Z, Wang X, Zhang X (2010b) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138PubMedCrossRefGoogle Scholar
  98. Wilkins O, Brautigam K, Campbell MM (2010) Time of day shapes Arabidopsis drought transcriptomes. Plant J 63(5):715–727PubMedCrossRefGoogle Scholar
  99. Xin M, Wang Y, Yao Y, Song N, Hu Z, Qin D, Xie C, Peng H, Ni Z, Sun Q (2011) Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol 11:61PubMedCrossRefGoogle Scholar
  100. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10(2):88–94PubMedCrossRefGoogle Scholar
  101. Yanez M, Caceres S, Orellana S, Bastias A, Verdugo I, Ruiz-Lara S, Casaretto JA (2009) An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes. Plant Cell Rep 28(10):1497–1507PubMedCrossRefGoogle Scholar
  102. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(Web Server issue):W293–W297PubMedCrossRefGoogle Scholar
  103. Youens-Clark K, Buckler E, Casstevens T, Chen C, Declerck G, Derwent P, Dharmawardhana P, Jaiswal P, Kersey P, Karthikeyan AS, Lu J, McCouch SR, Ren L, Spooner W, Stein JC, Thomason J, Wei S, Ware D (2011) Gramene database in 2010: updates and extensions. Nucleic Acids Res 39(Database issue):D1085–D1094PubMedCrossRefGoogle Scholar
  104. Zeller G, Henz SR, Widmer CK, Sachsenberg T, Ratsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58(6):1068–1082PubMedCrossRefGoogle Scholar
  105. Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G, Luo J (2011) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39(Database issue):D1114–D1117PubMedCrossRefGoogle Scholar
  106. Zhang G, Liu X, Quan Z, Cheng S, Xu X, Pan S, Xie M, Zeng P, Yue Z, Wang W, Tao Y, Bian C, Han C, Xia Q, Peng X, Cao R, Yang X, Zhan D, Hu J, Zhang Y, Li H, Li N, Wang J, Wang C, Wang R, Guo T, Cai Y, Liu C, Xiang H, Shi Q, Huang P, Chen Q, Li Y, Zhao Z (2012) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol 30(6):549–554PubMedCrossRefGoogle Scholar
  107. Zheng J, Fu J, Gou M, Huai J, Liu Y, Jian M, Huang Q, Guo X, Dong Z, Wang H, Wang G (2010) Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Mol Biol 72(4–5):407–421PubMedCrossRefGoogle Scholar
  108. Zhou J, Wang X, Jiao Y, Qin Y, Liu X, He K, Chen C, Ma L, Wang J, Xiong L, Zhang Q, Fan L, Deng XW (2007) Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Mol Biol 63(5):591–608PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Xin Qi
    • 1
  • Shaojun Xie
    • 1
  • Yuwei Liu
    • 1
  • Fei Yi
    • 1
  • Jingjuan Yu
    • 1
    Email author
  1. 1.State Key Laboratory for Agrobiotechnology, College of Biological SciencesChina Agricultural UniversityBeijingChina

Personalised recommendations