Expression profiling of genes involved in signaling process in Aegilops tauschii under salinity stress

Document Type : Research Paper

Authors

University of Tehran

Abstract

Salinization of crop lands is one of the most important reasons for reduction in productivity and threats food security. Activation of signaling process in plants is the first step during sense environmental cues and stress signals. Identification of the components of plant intracellular signaling mechanisms, pathways, and networks in response to salt stress in Aegilops tauschii (the D genome donor of bread wheat) by transcriptome analysis tools such as RNA Seq method is very worthwhile. RNA Seq method and functional annotation of data by MapMan suite is an efficient strategy to functional genomics analyses. In order to identify and evaluate some genes involved in signaling process, we performed library construction for two cDNA libraries from leaves of seedlings treated with 200 mM NaCl and control. Results of differential expression showed that out of 4506 differentially expressed genes, 603 (11/59%) BINs assigned to signaling process. It also became clear that receptor kinases are the largest number (222 transcripts) of differentially expressed genes in signaling process components. This study is a fundamental research that provide worthwhile functional sequences for gene transferring study to improve salinity tolerant in bread wheat.

Keywords


  1. Ahmad, P. & Prasad, M. N. V. (2012). Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. Springer New York Dordrecht Heidelberg London
  2. 2.       Allen, T., Koustenis, A., Theodorou, G., Somers, D. E., Kay, S. A., Whitelam, G. C. & Devlin, P. F. (2006). Arabidopsis FHY3 specifically gates phytochrome signaling to the circadian clock. Plant Cell, 18, 2506-2516.
  3. Amin, S.,Prentis, P. J.,Gilding, E. K. & Pavasovic, A. (2014). Assembly and annotation of a non-model gastropod (Nerita melanotragus) transcriptome: a comparison of De novo assemblers. BMC Research Notes, 7, 488.
  4. Ashraf, M., Ozturk, M. & Athar H. R. (2009). Salinity and Water Stress: Improving Crop Efficiency. Springer-Verlag, Berlin.
  5. Cardoso-Silva, C. B., Costa, E. A., Mancini, M. C., Balsalobre, T. W. A., Canesin, L. E. C., Pinto, L. R., Carneiro, M. S., Garcia, A. A., de Souza, A. P. & Vicentini, R. (2014). De Novo Assembly and Transcriptome Analysis of Contrasting Sugarcane Varieties. PLoS ONE 9(2), e88462.
  6. Chinnusamy, V., Jagendorf, A. & Zhu, J-K. (2005).Understanding and Improving Salt Tolerance in Plants. Crop Science, 45, 437-448.
  7. Chory, J. (2010). Light signal transduction: an infinite spectrum of possibilities. Plant Journal, 61, 982-991.
  8. Darwish, E., Testerink, C., Khalil, M., El-Shihy, O. & Munnik, T. (2009). Phospholipid signaling responses in salt-stressed rice leaves. Plant Cell Physiology, 50, 986-997.
  9. DeFalco, T. A., Bender, K. W. & Snedden, W. A. (2010). Breaking the code: Ca 2+ sensors in plant signalling. Biochemical Journal, 425, 27-40.
  10. Dodd, A. N., Kudla, J. & Sanders, D. (2010). The language of calcium signalling. Annual Review of Plant Biology, 61, 593-620.
  11. Falkenburger, B. H, Jensen, J. B., Dickson, E. J., Suh, B. C. & Hille, B. (2010). Phosphoinositides: lipid regulators of membrane proteins. Journal of Physiology, 588, 3179-3185.
  12. Gao, Y., Liu, H., An, C., Shi, Y., Liu, X., Yuan, W., Zhang, B., Yang, J., Yu, C. & Gao, H. (2013). Arabidopsis FRS4/CPD25 and FHY3/CPD45 work cooperatively to promote the expression of the chloroplast division gene ARC5 and chloroplast division. Plant Journal, 75, 795-807.
  13. Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J.Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., Friedman, N. & Regev, A. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29, 644e652.
  14. Hasegawa, P.M., Bressan, R.A., Zhu, J.K. & Bohnert, H.J. (2000). Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 463-499.
  15. Hetherington, A. M. & Brownlee, C. (2004). The generation of Ca2+ signals in plants. Annual Review of Plant Biology, 55, 401-427.
  16. Hudson, M., Ringli, C., Boylan, M. T. & Quail, P. H. (1999). The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes and Development, 13, 2017-2027.
  17. Hunt, L., Mills, L. N., Pical, C., Leckie, C.P., Aitken, F. L., Kopka, J., Mueller‐Roeber, B., McAinsh, M. R., Hetherington, A. M. & Gray, J. E. (2003). Phospholipase C is required for the control of stomatal aperture by ABA. Plant Journal, 34, 47-55.
  18. Jia, J., Zhao, S., Kong, X., Li, Y., Zhao, G., He, W., Appels, R., Pfeifer, M,. Tao, Y., Zhang, X., Jing, R., Zhang, C., Ma, Y., Gao, L., Gao, C., Spannagl, M., Mayer, K. F., Li, D., Pan, S., Zheng, F., Hu, Q., Xia, X., Li, J., Liang, Q., Chen, J., Wicker, T., Gou, C., Kuang, H., He, G., Luo, Y., Keller, B., Xia, Q., Lu, P., Wang, J., Zou, H., Zhang, R., Xu, J., Gao, J., Middleton, C., Quan, Z., Liu, G., Wang, J.; International Wheat Genome Sequencing Consortium, Yang, H., Liu, X., He, Z., Mao, L. & Wang, J. (2013). Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature, 496, 91-95.
  19. Khokhlatchev, A.V., Canagarajah, B., Wilsbacher, J., Robinson, M., Atkinson, M. Goldsmith, E. & Cobb, M. H. (1998). Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell, 93, 605-615.
  20. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome biology 10:R25.
  21. Li, B. & Dewey, C. N. (2011). RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics, 12, 323.
  22. Li, B., Fillmore, N., Bai, Y., Collins, M., Thomson, J.A., Stewart, R. & Dewey, C.N. (2014). Evaluation of de novo transcriptome assemblies from RNA-Seq data. Genome Biology, 15, 553.
  23. Li, W. & Assmann, S. M. (1993). Characterization of a G-protein-regulated outward K+ current in mesophyll cells of Vicia faba L. Proceedings of the National Academy of Sciences. USA, 90, 262-266.
  24. Lin, R. & Wang, H. (2004). Arabidopsis FHY3/FAR1 gene family and distinct roles of its members in light control of Arabidopsis development. Plant Physiology, 136, 4010-4022.
  25. Lohse, M., Nagel, A., Herter, T., May, P., Schroda, M., Zrenner, R., Tohge, T., Fernie, A.R., Stitt, M. & Usadel, A. (2013). Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant, Cell and Environment, 37(5), 1250-8.
  26. Mahajan, S., Pandey, G.K. & Tuteja, N. (2008). Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Archives of Biochemistry and Biophysics, 471, 146-158.
  27. Matsuoka, D., Nanmori, T., Sato, K., Fukami, Y., Kikkawa, U. & Yasuda, T. (2002). Activation of AtMEK1, an Arabidopsis mitogen-activated protein kinase kinase, in vitro and in vivo: analysis of active mutants expressed in E. coli and generation of the active form in stress response in seedlings. Plant Journal, 29, 637-647.
  28. Metzker, M.L. (2010). Sequencing technologies the next generation. Nature Reviews Genetics, 11, 31-46.
  29. Mills, L.N., Hunt, L., Leckie, C.P., Aitken, F.L., Wentworth, M., McAinsh, M.R., Gray, J.E. & Hetherington, A.M. (2004). The effects of manipulating phospholipase C on guard cell ABA-signalling. Journal of Experimental Botany, 55, 199-204.
  30. Monneveux, P., Zaharieva, M. & Rekika, D. (2000).The utilisation of Triticum and Aegilops species for the improvement of durum wheat. In: Royo C. (ed.), Nachit M. (ed.), Di Fonzo N. (ed.), Araus J.L. (ed.). Durum wheat improvement in the Mediterranean region: New challenges. Zaragoza: CIHEAM, 2 000. p. 71-81.
  31. Moreton, J., Dunham, S.P. & Emes, R.D. (2014). A consensus approach to vertebrate de novo transcriptome assembly from RNA-seq data: assembly of the duck (Anas platyrhynchos) transcriptome. Frontiers in Genetics, 5, 190.
  32. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. & Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-seq. Nature Methods, 5, 621-8.
  33. Munns, R. (2013). Hoagland's nutrient solution. Available at: http://prometheuswiki.publish.csiro.au/ tiki-index.php?page=Hoagland%27s+nutrient+solution.
  34. Munns, R. & James, R.A. (2003). Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil, 253, 201-18.
  35. Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K. & Tran, L.S. (2013). Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. Journal of Experimental Botany, 64(2), 445-458.
  36. Pandey, G.K. (2015). Elucidation of Abiotic Stress Signaling in Plants Functional Genomics Perspectives, Volume 1. Springer Science, New York, USA.
  37. Peng, J.H.H., Sun, D.F. & Nevo, E. (2011). Domestication evolution, genetics and genomics in wheat. Molecular Breeding, 28(3), 281-301.
  38. Petersen, G., Seberg, O., Yde, M. & Berthelsen, K. (2006). Phylogenetic relationships of Triticum and Aegilops and evidence for theorigin of the A, B, and D genomes of common wheat (Triticum aestivum). Molecular Phylogenetics and Evolution, 39, 70-82.
  39. Robinson, M.D., McCarthy, D.J. & Smyth, G.K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140.
  40. Saalbach, G., Natura, G., Lein, W., Buschmann, P., Dahse, I., Rohrbeck, M. & Nagy, F. (1999). The subunit of a heterotrimeric G-protein from tobacco, NtGP_1, functions in K+ channel regulation in mesophyll cells. Journal of Experimental Botany, 50, 53-61.
  41. Sanan-Mishra, N., Tuteja, R. & Tuteja, N. (2006). Signaling through MAP kinase networks in plants. Arch Biochem Biophys, 452, 55-68.
  42. Schachtman, D.P. & Munns, R. (1992). Sodium accumulation in leaves of Triticum species that differ in salt tolerance. Australian Journal of Plant Physiology, 19(3), 331-340.
  43. Serra, T., Figueiredo, D.D., Cordeiro, A.M., Almeida, D.M., Lourenço, T., Abreu, I.A., Sebastián, A., Fernandes, L., Contreras-Moreira, B., Oliveira, M.M. & Saibo, N.J. (2013). “OsRMC, a negative regulator of salt stress response in rice, is regulated by two AP2/ERF transcription factors”. Plant Molecular Biology, 82, 439-455.
  44. Sinha, A.K., Jaggi, M., Raghuram, B. & Tuteja, N. (2011). Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signaling and Behavior, 6(2), 196-203
  45. Suh, B.C., Inoue, T., Meyer, T. & Hille, B. (2006). Rapid chemically induced changes of PtdIns(4,5) P2 gate KCNQ ion channels. Science, 314, 1454-1457.
  46. Tang, W., Ji, Q., Huang, Y., Jiang, Z., Bao, M., Wang, H. & Lin, R. (2013). FAR-RED ELONGATED HYPOCOTYL3 and FAR-RED IMPAIRED RESPONSE1 Transcription Factors Integrate Light and Abscisic Acid Signaling in Arabidopsis. Plant Physiology, 163, 857-866.
  47. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L.A., Rhee, S.Y. & Stitt, M. (2004). MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal, 37,914-939.
  48. Wang, H. & Deng, X.W. (2002). Arabidopsis FHY3 defines a key phytochrome A signaling component directly interacting with its homologous partner FAR1. EMBO Journal, 21, 1339-1349.
  49. Wang, H. & Wang, H. (2015). Multifaceted roles of FHY3 and FAR1 in light signaling and beyond. Trends in Plant Science, 20(7), 453-61.
  50. Wang, Z., Gerstein, M. & Snyder, M. (2009). RNA-Seq: a revolutionary tool for transcriptomics. Nature reviews Genetics, 10(1), 57-63.
  51. Wu, W-H. & Assmann, S. M. (1994). A membrane-delimited pathway of G-protein regulation of the guard-cell inward K+ channel. In: Proceedings of the National Academy of Sciences USA, 91, 6310-6314.
  52. Wurzinger, B., Mair, A., Pfister, B. & Teige, M. (2011). Crosstalk of calcium-dependent protein kinase and MAP kinase signalling. Plant Signaling and Behavior, 6, 1-5.
  53. Xie, W. & Nevo, E. (2008). Wild emmer: genetic resources, gene mapping and transfer for wheat improvement. Euphytica, 164, 603-614.
  54. Xiong, L., Schumaker, K.S. & Zhu, J-K. (2002). Cell Signaling during Cold, Drought, and Salt Stress. The Plant Cell, S165-S183.
  55. Yang, Z. (2008). Intracellular Signaling in Plants. Annual Plant Reviews Volume33. Blackwell Publishing Ltd.
  56. Zhu, J.K. (2001). Cell signaling under salt stress, water and cold stresses. Current Opinion in Plant Biology, 5, 401-406.
Volume 47, Issue 2 - Serial Number 2
October 2016
Pages 205-216
  • Receive Date: 15 September 2015
  • Revise Date: 10 November 2015
  • Accept Date: 23 November 2015
  • Publish Date: 22 August 2016