biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 62:33-44, 2018 | DOI: 10.1007/s10535-017-0737-4

Characterization of Citrus WRKY transcription factors and their responses to phytohormones and abiotic stresses

V. Vives-Peris1, D. Marmaneu1, A. Gómez-Cadenas1, R. M. Pérez-Clemente1,*
1 Departament de Ciències Agràries i del Medi Natural, Universitat Jaume I, Castellón de la Plana, Spain

WRKY transcription factors (TF) family is involved in a huge variety of plant processes, including seed germination, plant development, phytohormone signalling, and defence against both biotic or abiotic stresses. In this work, WRKY TF family has been characterized in citrus. In a first experiment, the relative expression of CsWRKYs was analyzed in shoots and roots of plants treated with abscisic acid (ABA), salicylic acid (SA), and methyl jasmonate (MeJA) under in vitro conditions. Expression of CsWRKYs was also determined in roots of commercial citrus rootstocks subjected to osmotic and salt stresses. A total amount of 50 CsWRKYs has been found and devided into different groups of WRKY family according to the WRKY domain sequences. In response to the applications of phytohormones, the highest differences were observed in roots, and it was found that ABA and SA generally repressed CsWRKYs expressions, but MeJA induced their overexpression. Osmotic stress repressed the expression of most of the CsWRKYs, whereas salt stress induced their expression. Moreover, salt stress induced higher increase in CsWRKY expressions in the tolerant rootstock Citrus macrophylla than in the sensitive rootstock Carrizo citrange, suggesting that these TFs may play an important role in response to this stress.

Keywords: abscisic acid; Carrizo citrange; Citrus macrophylla; Citrus sinensis × Poncirus trifoliata; methyl jasmonate; osmotic stress; salicylic acid; salinity
Subjects: transcription factor; WRKY; methyl jasmonate; salicylic acid; phylogenetic tree; abscisic acid; gene expression; osmotic stress; salinity; citrus

Received: September 7, 2016; Revised: February 21, 2017; Accepted: March 1, 2017; Published: January 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Vives-Peris, V., Marmaneu, D., Gómez-Cadenas, A., & Pérez-Clemente, R.M. (2018). Characterization of Citrus WRKY transcription factors and their responses to phytohormones and abiotic stresses. Biologia plantarum, 62(1), 33-44. doi: 10.1007/s10535-017-0737-4
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download filebpl-201801-0004_S1.pdf

    File size: 2.22 MB

    References

    1. Agarwal, P., Reddy, M.P., Chikara, J.: WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. - Mol. Biol. Rep. 38: 3883-3896, 2011. Go to original source...
    2. Bakshi, M., Oelmüller, R.: WRKY transcription factors: jack of many trades in plants. - Plant Signal. Behav. 9: 1-18, 2014. Go to original source...
    3. Bansal, S., Harrington, C.A., St. Clair, J.B.: Tolerance to multiple climate stressors: a case study of Douglas-fir drought and cold hardiness. - Ecol. Evol. 6: 2074-2083, 2016. Go to original source...
    4. Chen, H., Lai, Z., Shi, J., Xiao, Y., Chen, Z., Xu, X.: Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. - BMC Plant Biol. 10: 281, 2010. Go to original source...
    5. Chen, L., Liu, Y., Liu, H., Kang, L., Geng, J., Gai, Y., Ding, Y., Sun, H., Li, Y.: Identification and expression analysis of MATE genes involved in flavonoid transport in blueberry plants. - PLoS ONE 10: e0118578, 2015. Go to original source...
    6. Chen, L., Song, Y., Li, S., Zhang, L., Zou, C., Yu, D.: The role of WRKY transcription factors in plant abiotic stresses. - Biochim. biophys. Acta 1819: 120-128, 2012. Go to original source...
    7. Czarnecki, O., Yang, J., Wang, X., Wang, S., Muchero, W., Tuskan, G.A., Chen, J.-G.: Characterization of MORE AXILLARY GROWTH genes in Populus. - PLoS ONE 9: e102757, 2014. Go to original source...
    8. De Ollas, C., Hernando, B., Arbona, V., Gómez-Cadenas, A.: Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. - Physiol. Plant. 147: 296-306, 2013. Go to original source...
    9. Durgbanshi, A., Arbona, V., Pozo, O., Miersch, O., Sancho, J. V., Gómez-Cadenas, A.: Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography-electrospray tandem mass spectrometry. - J. Agr. Food Chem. 53: 8437-8442, 2005. Go to original source...
    10. Eulgem, T., Rushton, P.J., Robatzek, S., Somssich, I.E.: The WRKY superfamily of plant transcription factors. - Trends Plant Sci. 5: 199-206, 2000. Go to original source...
    11. Gómez-Cadenas, A., De Ollas, C., Manzi, M., Arbona, V.: Phytohormonal crosstalk under abiotic stress. - In: Phan Tran, L.S., Pal, S. (ed.): Phytohormones: A Window to Metabolism, Signaling and Biotechnological Applications. Vol. 1. Pp. 289-321. Springer, New York - Heidelberg - Dordrecht - London 2014. Go to original source...
    12. Gómez-Cadenas, A., Tadeo, F.R., Primo-Millo, E., Talon, M.: Involvement of abscisic acid and ethylene in the responses of citrus seedlings to salt shock. - Physiol. Plant. 103: 475-484, 1998. Go to original source...
    13. Gómez-Cadenas, A., Vives, V., Zandalinas, S.I., Manzi, M., Sánchez-Pérez, A.M., Pérez-Clemente, R.M., Arbona, V.: Abscisic acid: a versatile phytohormone in plant signaling and beyond. - Curr. Protein Pept. Sci. 16: 413-434, 2015. Go to original source...
    14. Gong, X., Zhang, J., Hu, J., Wang, W., Wu, H., Zhang, Q., Liu, J.-H.: FcWRKY70, a WRKY protein of Fortunella crassifolia, functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene. - Plant Cell Environ. 38: 2248-2262, 2015. Go to original source...
    15. Guo, C., Guo, R., Xu, X., Gao, M., Li, X., Song, J., Zheng, Y., Wang, X.: Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. - J. exp. Bot. 65: 1513-1528, 2014. Go to original source...
    16. Huang, G.T., Ma, S.L., Bai, L.P., Zhang, L., Ma, H., Jia, P., Liu, J., Zhong, M., Guo, Z.F.: Signal transduction during cold, salt, and drought stresses in plants. - Mol. Biol. Rep. 39: 969-987, 2012. Go to original source...
    17. Iglesias, D.J., Levy, Y., Gómez-Cadenas, A., Tadeo, F.R., Primo-Millo, E., Talon, M.: Nitrate improves growth in saltstressed citrus seedlings through effects on photosynthetic activity and chloride accumulation. - Tree Physiol. 24: 1027-1034, 2004. Go to original source...
    18. Jiang, Y., Duan, Y., Yin, J., Ye, S., Zhu, J., Zhang, F., Lu, W., Fan, D., Luo, K.: Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. - J. exp. Bot. 65: 6629-6644, 2014. Go to original source...
    19. Johnson, C.S., Kolevski, B., Smyth, D.R.: TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. - Plant Cell 14: 1359-1375, 2002. Go to original source...
    20. Lamesch, P., Berardini, T.Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., Muller, R., Dreher, K., Alexander, D.L., Garcia-Hernandez, M., Karthikeyan, A.S., Lee, C.H., Nelson, W.D., Ploetz, L., Singh, S., Wensel, A., Huala, E.: The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. - Nucl. Acids Res. 40: D1202-D1210, 2012. Go to original source...
    21. Li, J., Brader, G., Palva, E.T.: The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. - Plant Cell 16: 319-331, 2004. Go to original source...
    22. Liu, J.-H., Peng, T., Dai, W.: Critical cis-acting elements and interacting transcription factors: key players associated with abiotic stress responses in plants. - Plant mol. Biol. Rep. 32: 303-317, 2014. Go to original source...
    23. Llorca, C.M., Potschin, M., Zentgraf, U.: bZIPs and WRKYs: two large transcription factor families executing two different functional strategies. - Front. Plant Sci. 5: 169, 2014. Go to original source...
    24. Mangelsen, E., Kilian, J., Berendzen, K.W., Kolukisaoglu, U.H., Harter, K., Jansson, C., Wanke, D.: Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots. - BMC Genomics 9: 194, 2008. Go to original source...
    25. Michel, B.E., Kaufmann, M.R.: The osmotic potential of polyethylene glycol 6000. - Plant Physiol. 51: 914-916, 1973. Go to original source...
    26. Montoliu, A., Gómez-Cadenas, A., Pérez-Clemente, R.M.: In vitro adventitious rooting of Carrizo citrange microshoots. - HortScience 45: 988-990, 2010. Go to original source...
    27. Montoliu, A., López-Climent, M.F., Arbona, V., Pérez-Clemente, R.M., Gómez-Cadenas, A.: A novel in vitro tissue culture approach to study salt stress responses in citrus. - Plant Growth Regul. 59: 179-187, 2009. Go to original source...
    28. Moya, J.L., Gómez-Cadenas, A., Primo-Millo, E., Talon, M.: Chloride absorption in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin citrus rootstocks is linked to water use. - J. exp. Bot. 54: 825-833, 2003. Go to original source...
    29. Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue cultures. - Physiol. Plant. 15: 473-497, 1962. Go to original source...
    30. Nei, M., Kumar, S.: Molecular Evolution and Phylogenetics. - Oxford University Press, New York 2000.
    31. Pan, L.-J., Jiang, L.: Identification and expression of the WRKY transcription factors of Carica papaya in response to abiotic and biotic stresses. - Mol. Biol. Rep. 41: 1215-1225, 2014. Go to original source...
    32. Pfaffl, M.W.: A new mathematical model for relative quantification in real-time RT-PCR. - Nucl. Acids Res. 29: 2002-2007, 2001. Go to original source...
    33. Pfaffl, M.W., Horgan, G.W., Dempfle, L.: Relative expression software tool (REST ©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. - Nucl. Acids Res. 30: 1-10, 2002. Go to original source...
    34. Ramamoorthy, R., Jiang, S.Y., Kumar, N., Venkatesh, P.N., Ramachandran, S.: A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. - Plant Cell Physiol. 49: 865-879, 2008. Go to original source...
    35. Robatzek, S., Somssich, I.E.: Targets of AtWRKY6 regulation during plant senescence and pathogen defense. - Genes Dev. 16: 1139-1149, 2002. Go to original source...
    36. Roy Choudhury, A., Gupta, B., Sengupta, D.N.: Trans-acting factor designated OSBZ8 interacts with both typical abscisic acid responsive elements as well as abscisic acid responsive element-like sequences in the vegetative tissues of indica rice cultivars. - Plant Cell Rep. 27: 779-794, 2008. Go to original source...
    37. Rushton, P.J., Somssich, I.E., Ringler, P., Shen, Q.J.: WRKY transcription factors. - Trends Plant Sci. 15: 247-258, 2010. Go to original source...
    38. Saeed, A.I., Bhagabati, N.K., Braisted, J.C., Liang, W., Sharov, V., Howe, E.A., Li, J., Thiagarajan, M., White, J.A., Quackenbush, J.: TM4 microarray software suite. - Methods Enzymol. 411: 134-193, 2006. Go to original source...
    39. Sah, S.K., Reddy, K.R., Li, J.: Abscisic acid and abiotic stress tolerance in crop plants. - Front. Plant Sci. 7: 1-26, 2016. Go to original source...
    40. Şahin-Çevik, M.: A WRKY transcription factor gene isolated from Poncirus trifoliata shows differential responses to cold and drought stresses. - Plant Omics J. 5: 438-445, 2012.
    41. Şahin-Çevik, M., Moore, G.A.: Identification of a drought-and cold-stress inducible WRKY gene in the cold-hardy Citrus relative Poncirus trifoliata. - New Zeal. J. Crops hort. Sci. 41: 57-68, 2013. Go to original source...
    42. Saitou, N., Nei, M.: The neighbor-joining nethod: a new method for reconstructing phylogenetic trees. - Mol. Biol. Evol. 4: 406-425, 1987.
    43. Shakirova, F.M., Allagulova, C.R., Maslennikova, D.R., Klyuchnikova, E.O., Avalbaev, A.M., Bezrukova, M.V.: Salicylic acid-induced protection against cadmium toxicity in wheat plants. - Environ. exp. Bot. 122: 19-28, 2016. Go to original source...
    44. Skibbe, M., Qu, N., Galis, I., Baldwin, I.T.: Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. - Plant Cell 20: 1984-2000, 2008. Go to original source...
    45. Song, H., Wang, P., Hou, L., Zhao, S., Zhao, C., Xia, H., Li, P.: Global analysis of WRKY genes and their response to dehydration and salt stress in soybean. - Front. Plant Sci. 7: 9, 2016. Go to original source...
    46. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S.: MEGA6: molecular evolutionary genetics analysis version 6.0. - Mol. Biol. Evol. 30: 2725-2729, 2013. Go to original source...
    47. Van Verk, M.C., Pappaioannou, D., Neeleman, L., Bol, J.F., Linthorst, H.J.M.: A Novel WRKY transcription factor is required for induction of PR-1a gene expression by salicylic acid and bacterial elicitors. - Plant Physiol. 146, 1983-1995, 2008. Go to original source...
    48. Wei, W., Zhang, Y., Han, L., Guan, Z., Chai, T.: A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco. - Plant Cell Rep. 27: 795-803, 2008. Go to original source...
    49. Woo, H.R., Kim, H.J., Nam, H.G., Lim, P.O.: Plant leaf senescence and death-regulation by multiple layers of control and implications for aging in general. - J. cell. Sci. 126: 4823-4833, 2013. Go to original source...
    50. Xie, Z., Zhang, Z.L., Zou, X., Yang, G., Komatsu, S., Shen, Q.J.: Interactions of two abscisic-acid induced WRKY genes in repressing gibberellin signaling in aleurone cells. - Plant J. 46: 231-242, 2006. Go to original source...
    51. Yang, B., Jiang, Y., Rahman, M.H., Deyholos, M.K., Kav, N.N. V: Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. - BMC Plant Biol. 9: 1-19, 2009. Go to original source...
    52. Zandalinas, S.I., Rivero, R.M., Martínez, V., Gómez-Cadenas, A., Arbona, V.: Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. - BMC Plant Biol. 16: 105, 2016. Go to original source...
    53. Zheng, Z., Qamar, S.A., Chen, Z., Mengiste, T.: Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. - Plant J. 48: 592-605, 2006. Go to original source...
    54. Zhou, L., Wang, N.-N., Gong, S.-Y., Lu, R., Li, Y., Li, X.-B.: Overexpression of a cotton (Gossypium hirsutum) WRKY gene, GhWRKY34, in Arabidopsis enhances salt-tolerance of the transgenic plants. - Plant Physiol. Biochem. 96: 311-320, 2015. Go to original source...
    55. Zhou, Q.Y., Tian, A.G., Zou, H.F., Xie, Z.M., Lei, G., Huang, J., Wang, C.M., Wang, H.W., Zhang, J.S., Chen, S.Y.: Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. - Plant Biotechnol. J. 6: 486-503, 2008. Go to original source...

    Return to the content