Table of Contents Author Guidelines Submit a Manuscript
International Journal of Genomics
Volume 2013 (2013), Article ID 857986, 10 pages
http://dx.doi.org/10.1155/2013/857986
Research Article

Identification of Cassava MicroRNAs under Abiotic Stress

1Agrobiodiversity and Biotechnology Project, International Center for Tropical Agriculture (CIAT), A.A. 6713, Cali, Colombia
2Department of Systems Biology, Columbia University, 1130 Saint Nicholas Avenue, New York, NY 10032, USA
3The Genome Analysis Centre, Norwich Research Park, Norwich NR4 7UH, UK

Received 2 August 2013; Accepted 11 October 2013

Academic Editor: Gaurav Sablok

Copyright © 2013 Carolina Ballén-Taborda et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. P. Bartel, “MicroRNAs: genomics, biogenesis, mechanism, and function,” Cell, vol. 116, no. 2, pp. 281–297, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Song, M. Han, J. Lesicka, and N. Fedoroff, “Arabidopsis primary microRNA processing proteins HYL1 and DCL1 define a nuclear body distinct from the Cajal body,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 13, pp. 5437–5442, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. M. W. Jones-Rhoades, D. P. Bartel, and B. Bartel, “MicroRNAs and their regulatory roles in plants,” Annual Review of Plant Biology, vol. 57, pp. 19–53, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. O. Voinnet, “Origin, biogenesis, and activity of plant MicroRNAs,” Cell, vol. 136, no. 4, pp. 669–687, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Brodersen, L. Sakvarelidze-Achard, M. Bruun-Rasmussen et al., “Widespread translational inhibition by plant miRNAs and siRNAs,” Science, vol. 320, no. 5880, pp. 1185–1190, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Wu, “Plant microRNAs and development,” Journal of Genetics and Genomics, vol. 40, no. 5, pp. 217–230, 2013. View at Google Scholar
  7. R. Sunkar, V. Chinnusamy, J. Zhu, and J. Zhu, “Small RNAs as big players in plant abiotic stress responses and nutrient deprivation,” Trends in Plant Science, vol. 12, no. 7, pp. 301–309, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. L. I. Shukla, V. Chinnusamy, and R. Sunkar, “The role of microRNAs and other endogenous small RNAs in plant stress responses,” Biochimica et Biophysica Acta, vol. 1779, no. 11, pp. 743–748, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. B. Khraiwesh, J. Zhu, and J. Zhu, “Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants,” Biochimica et Biophysica Acta, vol. 1819, no. 2, pp. 137–148, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Sunkar, “MicroRNAs with macro-effects on plant stress responses,” Seminars in Cell and Developmental Biology, vol. 21, no. 8, pp. 805–811, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Griffiths-Jones, H. K. Saini, S. van Dongen, and A. J. Enright, “miRBase: tools for microRNA genomics,” Nucleic Acids Research, vol. 36, supplement 1, pp. D154–D158, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. B. C. Meyers, F. F. Souret, C. Lu, and P. J. Green, “Sweating the small stuff: microRNA discovery in plants,” Current Opinion in Biotechnology, vol. 17, no. 2, pp. 139–146, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Sun, “MicroRNAs and their diverse functions in plants,” Plant Molecular Biology, vol. 80, no. 1, pp. 17–36, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. El-Sharkawy, “Cassava biology and physiology,” Plant Molecular Biology, vol. 56, no. 4, pp. 481–501, 2004. View at Google Scholar · View at Scopus
  15. H. Mathews, C. Schopke, R. Carcamo, P. Chavarriaga, C. Fauquet, and R. N. Beachy, “Improvement of somatic embryogenesis and plant recovery in cassava,” Plant Cell Reports, vol. 12, no. 6, pp. 328–333, 1993. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Sakurai, G. Plata, F. Rodríguez-Zapata et al., “Sequencing analysis of 20,000 full-length cDNA clones from cassava reveals lineage specific expansions in gene families related to stress response,” BMC Plant Biology, vol. 7, p. 66, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Amiteye, J. M. Corral, and T. F. Sharbel, “Overview of the potential of microRNAs and their target gene detection for cassava (Manihot esculenta) improvement,” African Journal of Biotechnology, vol. 10, no. 14, pp. 2562–2573, 2011. View at Google Scholar · View at Scopus
  18. O. Patanun, M. Lertpanyasampatha, P. Sojikul, U. Viboonjun, and J. Narangajavana, “Computational identification of MicroRNAs and their targets in Cassava (Manihot esculenta Crantz.),” Molecular Biotechnology, vol. 53, no. 3, pp. 257–269, 2013. View at Publisher · View at Google Scholar
  19. Á. L. Pérez-Quintero, A. Quintero, O. Urrego, P. Vanegas, and C. López, “Bioinformatic identification of cassava miRNAs differentially expressed in response to infection by Xanthomonas axonopodis pv. manihotis,” BMC Plant Biology, vol. 12, no. 1, p. 29, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Zeng, W. Wang, Y. Zheng et al., “Conservation and divergence of microRNAs and their functions in Euphorbiaceous plants,” Nucleic Acids Research, vol. 38, no. 3, Article ID gkp1035, pp. 981–995, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Lv, X. Nie, L. Wang et al., “Identification and characterization of microRNAs from barley (hordeum vulgare L.) by high-throughput sequencing,” International Journal of Molecular Sciences, vol. 13, no. 3, pp. 2973–2984, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Sunkar, T. Girke, P. K. Jain, and J. Zhu, “Cloning and characterization of microRNAs from rice,” Plant Cell, vol. 17, no. 5, pp. 1397–1411, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Martin, “Cutadapt removes adapter sequences from high-throughput sequencing reads,” EMBnet.Journal, vol. 17, no. 1, 2011. View at Google Scholar
  24. S. W. Burge, J. Daub, R. Eberhardt et al., “Rfam 11.0:10 years of RNA families,” Nucleic Acids Research, vol. 41, Database issue, pp. D226–D232, 2013. View at Google Scholar
  25. P. Lamesch, T. Z. Berardini, D. Li et al., “The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools,” Nucleic Acids Research, vol. 40, Database issue, pp. D1202–D1210, 2012. View at Google Scholar
  26. P. Pelaez, M. S. Trejo, L. P. Iniguez et al., “Identification and characterization of microRNAs in Phaseolus vulgaris by high-throughput sequencing,” BMC Genomics, vol. 13, p. 83, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. S. F. Altschul, T. L. Madden, A. A. Schäffer et al., “Gapped BLAST and PSI-BLAST: a new generation of protein database search programs,” Nucleic Acids Research, vol. 25, no. 17, pp. 3389–3402, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. B. Langmead, C. Trapnell, M. Pop, and S. L. Salzberg, “Ultrafast and memory-efficient alignment of short DNA sequences to the human genome,” Genome Biology, vol. 10, no. 3, p. R25, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Prochnik, P. R. Marri, B. Desany et al., “The Cassava genome: current progress, future directions,” Tropical Plant Biology, vol. 5, no. 1, pp. 88–94, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. T. P. Frazier, F. Xie, A. Freistaedter, C. E. Burklew, and B. Zhang, “Identification and characterization of microRNAs and their target genes in tobacco (nicotiana tabacum),” Planta, vol. 232, no. 6, pp. 1289–1308, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. R. Zhang, D. Marshall, G. J. Bryan, and C. Hornyik, “Identification and characterization of miRNA transcriptome in potato by high-throughput sequencing,” PLoS One, vol. 8, no. 2, Article ID e57233, 2013. View at Google Scholar
  32. X. Yang and L. Li, “miRDeep-P: a computational tool for analyzing the microRNA transcriptome in plants,” Bioinformatics, vol. 27, no. 18, Article ID btr430, pp. 2614–2615, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. M. R. Friedländer, W. Chen, C. Adamidi et al., “Discovering microRNAs from deep sequencing data using miRDeep,” Nature Biotechnology, vol. 26, no. 4, pp. 407–415, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. I. L. Hofacker, W. Fontana, P. F. Stadler, L. S. Bonhoeffer, M. Tacker, and P. Schuster, “Fast folding and comparison of RNA secondary structures,” Monatshefte für Chemie Chemical Monthly, vol. 125, no. 2, pp. 167–188, 1989. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Moxon, F. Schwach, T. Dalmay, D. MacLean, D. J. Studholme, and V. Moulton, “A toolkit for analysing large-scale plant small RNA datasets,” Bioinformatics, vol. 24, no. 19, pp. 2252–2253, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. B. C. Meyers, M. J. Axtell, B. Bartel et al., “Criteria for annotation of plant microRNAs,” Plant Cell, vol. 20, no. 12, pp. 3186–3190, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Mathelier and A. Carbone, “MIReNA: finding microRNAs with high accuracy and no learning at genome scale and from deep sequencing data,” Bioinformatics, vol. 26, no. 18, Article ID btq329, pp. 2226–2234, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. M. W. Jones-Rhoades and D. P. Bartel, “Computational identification of plant MicroRNAs and their targets, including a stress-induced miRNA,” Molecular Cell, vol. 14, no. 6, pp. 787–799, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. X. Dai and P. X. Zhao, “PsRNATarget: a plant small RNA target analysis server,” Nucleic Acids Research, vol. 39, supplement 2, pp. W155–W159, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. D. M. Goodstein, S. Shu, R. Howson et al. et al., “Phytozome: a comparative platform for green plant genomics,” Nucleic Acids Research, vol. 40, Database issue, pp. D1178–D1186, 2012. View at Google Scholar
  41. Z. Du, X. Zhou, Y. Ling, Z. Zhang, and Z. Su, “agriGO: a GO analysis toolkit for the agricultural community,” Nucleic Acids Research, vol. 38, no. 2, Article ID gkq310, pp. W64–W70, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. H. J. Bussemaker, L. D. Ward, and A. Boorsma, “Dissecting complex transcriptional responses using pathway-level scores based on prior information,” BMC Bioinformatics, vol. 8, supplement 6, p. S6, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Benjamini and D. Yekutieli, “The control of the false discovery rate in multiple testing under dependency,” Annals of Statistics, vol. 29, no. 4, pp. 1165–1188, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Chen, R. Tan, L. Wong, R. Fekete, and J. Halsey, “Quantitation of MicroRNAs by real-time RT-qPCR,” in PCR Protocols, D. Park, Ed., pp. 113–134, Humana Press, New York, NY, USA, 2011. View at Google Scholar
  45. J. Feng, K. Wang, X. Liu, S. Chen, and J. Chen, “The quantification of tomato microRNAs response to viral infection by stem-loop real-time RT-PCR,” Gene, vol. 437, no. 1-2, pp. 14–21, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. S. D. Fiedler, M. Z. Carletti, and L. K. Christenson, “Quantitative RT-PCR methods for mature microRNA expression analysis,” Methods in Molecular Biology, vol. 630, pp. 49–64, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Fahlgren, M. D. Howell, K. D. Kasschau et al., “High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of miRNA genes,” PLoS ONE, vol. 2, no. 2, Article ID e219, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. G. Szittya, S. Moxon, D. M. Santos et al., “High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families,” BMC Genomics, vol. 9, p. 593, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Moxon, R. Jing, G. Szittya et al., “Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening,” Genome Research, vol. 18, no. 10, pp. 1602–1609, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. R. D. Morin, G. Aksay, E. Dolgosheina et al., “Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa,” Genome Research, vol. 18, no. 4, pp. 571–584, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. J. R. Puzey, A. Karger, M. Axtell, and E. M. Kramer, “Deep annotation of populus trichocarpa micrornas from diverse tissue sets,” PLoS ONE, vol. 7, no. 3, Article ID e33034, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. B. Zhang, X. Pan, C. H. Cannon, G. P. Cobb, and T. A. Anderson, “Conservation and divergence of plant microRNA genes,” Plant Journal, vol. 46, no. 2, pp. 243–259, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. G. B. Martin, A. J. Bogdanove, and G. Sessa, “Understanding the functions of plant disease resistance proteins,” Annual Review of Plant Biology, vol. 54, pp. 23–61, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. Utsumi, M. Tanaka, T. Morosawa et al., “Transcriptome analysis using a high-density oligomicroarray under drought stress in various genotypes of cassava: an important tropical crop,” DNA Research, vol. 19, no. 4, pp. 335–345, 2012. View at Google Scholar
  55. A. A. Covarrubias and J. L. Reyes, “Post-transcriptional gene regulation of salinity and drought responses by plant microRNAs,” Plant, Cell and Environment, vol. 33, no. 4, pp. 481–489, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. L. Zhou, Y. Liu, Z. Liu, D. Kong, M. Duan, and L. Luo, “Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa,” Journal of Experimental Botany, vol. 61, no. 15, pp. 4157–4168, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Xin, Y. Wang, Y. Yao et al., “Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.),” BMC Plant Biology, vol. 10, p. 123, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Sunkar and J. Zhu, “Novel and stress regulated microRNAs and other small RNAs from Arabidopsis w inside box sign,” Plant Cell, vol. 16, no. 8, pp. 2001–2019, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. B. Li, Y. Qin, H. Duan, W. Yin, and X. Xia, “Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica,” Journal of Experimental Botany, vol. 62, no. 11, pp. 3765–3779, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. I. Trindade, C. Capitão, T. Dalmay, M. P. Fevereiro, and D. M. dos Santos, “miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula,” Planta, vol. 231, no. 3, pp. 705–716, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. H. H. Liu, X. Tian, Y. J. Li, C. A. Wu, and C. C. Zheng, “Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana,” RNA, vol. 14, no. 5, pp. 836–843, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Gallo, M. Tandon, I. Alevizos, and G. G. Illei, “The majority of microRNAs detectable in serum and saliva is concentrated in exosomes,” PLoS ONE, vol. 7, no. 3, Article ID e30679, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. G. Hyman, A. Bellotti, L. Lopez-Lavalle, N. Palmer, and B. Creamer, “Cassava and overcoming the challenges of global climatic change: report of the second scientific conference of the Global Cassava Partnership for the 21st century,” Food Security, vol. 4, no. 4, pp. 671–674, 2012. View at Google Scholar
  64. L. F. Turyagyenda, E. B. Kizito, M. Ferguson et al., “Physiological and molecular characterization of drought responses and identification of candidate tolerance genes in cassava,” AoB Plants, vol. 5, Article ID plt007, 2013. View at Publisher · View at Google Scholar
  65. Y. Ding, Y. Tao, and C. Zhu, “Emerging roles of microRNAs in the mediation of drought stress response in plants,” Journal of Experimental Botany, vol. 64, no. 11, pp. 3077–3086, 2013. View at Publisher · View at Google Scholar
  66. Y. Ding, Y. Tao, and C. Zhu, “Emerging roles of microRNAs in the mediation of drought stress response in plants,” Journal of Experimental Botany, vol. 64, no. 11, pp. 3077–3086, 2013. View at Publisher · View at Google Scholar
  67. S. Zhang, Y. Yue, L. Sheng et al., “PASmiR: a literature-curated database for miRNA molecular regulation in plant response to abiotic stress,” BMC Plant Biology, vol. 13, p. 33, 2013. View at Google Scholar
  68. A. S. Saad, X. Li, H. P. Li et al., “A rice stress-responsive NAC gene enhances tolerance of transgenic wheat to drought and salt stresses,” Plant Science, vol. 203-204, pp. 33–40, 2013. View at Google Scholar
  69. K. Nakashima, H. Takasaki, J. Mizoi, K. Shinozaki, and K. Yamaguchi-Shinozaki, “NAC transcription factors in plant abiotic stress responses,” Biochimica et Biophysica Acta, vol. 1819, no. 2, pp. 97–103, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. X. Cai, E. J. Davis, J. Ballif et al., “Mutant identification and characterization of the laccase gene family in Arabidopsis,” Journal of Experimental Botany, vol. 57, no. 11, pp. 2563–2569, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. T. H. Ferreira, A. Gentile, R. D. Vilela et al., “microRNAs associated with drought response in the bioenergy crop sugarcane (Saccharum spp.),” PLoS One, vol. 7, no. 10, Article ID e46703, 2012. View at Google Scholar
  72. N. Tuteja, “Abscisic acid and abiotic stress signaling,” Plant Signaling and Behavior, vol. 2, no. 3, pp. 135–138, 2007. View at Google Scholar · View at Scopus
  73. X. Dai, X. Cheng, Y. Li, W. Tang, and L. Han, “Differential expression of gibberellin 20 oxidase gene induced by abiotic stresses in Zoysiagrass (Zoysia japonica),” Biologia, vol. 67, no. 4, pp. 681–688, 2012. View at Google Scholar
  74. M. J. Jeong, B. S. Choi, D. W. Bae et al., “Differential expression of kenaf phenylalanine ammonia-lyase (PAL) ortholog during developmental stages and in response to abiotic stresses,” Plant Omics Journal, vol. 5, no. 4, pp. 392–399, 2012. View at Google Scholar
  75. J. M. Bardzik, H. V. Marsh, and J. R. Havis, “Effects of water stress on the activities of three enzymes in maize seedlings,” Plant Physiology, vol. 47, no. 6, pp. 828–831, 1971. View at Google Scholar
  76. A. Gholizadeh, “Effects of drought on the activity of Phenylalanine ammonia lyase in the leaves and roots of maize inbreds,” Australian Journal of Basic and Applied Sciences, vol. 5, no. 9, pp. 952–956, 2011. View at Google Scholar · View at Scopus
  77. D. Golldack, I. Lüking, and O. Yang, “Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network,” Plant Cell Reports, vol. 30, no. 8, pp. 1383–1391, 2011. View at Publisher · View at Google Scholar · View at Scopus