Biologia plantarum 2013, 57:425-432 | DOI: 10.1007/s10535-013-0324-2

Analysis of differentially expressed genes in response to endogenous cytokinins during cotton leaf senescence

P. Zhao1, N. Zhang1, Z. J. Yin1,2, Y. D. Liu1, F. F. Shen1,*
1 State Key Laboratory of Crop Biology, College of Agronomy, Shandong Agricultural University, Taian, Shandong, P.R. China
2 State Key Laboratory of Cotton Biology, Cotton Research Institute, Chinese Academy of Agricultural Sciences, Anyang, Henan, P.R. China

Cytokinins have been implicated in delaying leaf senescence. We previously generated transgenic cotton (Gossypium hirsutum L.) plants that harbor the Agrobacterium isopentenyl transferase gene (ipt) directed by a proteinase gene promoter. Here, we report that mRNAs were isolated from ipt cotton leaves and azygous leaves and were subsequently sequenced using Illumina Solexa technology. The sequence tags were searched against the TIGR database and the related gene expression profiles were compared resulting in the identification of 1 218 differentially expressed genes (DEGs): 719 up-regulated and 499 down-regulated. Analyzing the DEGs in the ipt cotton leaves showed that these genes belonged to four pathways: flavone biosynthesis, arginine and proline metabolism, glyoxylate and dicarboxylate metabolism, and RNA degradation. These pathways increased the activities of antioxidants, inhibited the effect of ethylene, and prevented degradation of macromolecules during senescence. The expression patterns of 17 genes were evaluated by real-time PCR and results were in agreement with the patterns of sequencing analysis. The identification of the DEGs may help us to understand a role of cytokinins in leaf senescence.

Keywords: Gossypium hirsutum; metabolic pathways; Solexa sequencing; TIGR database; transgenic plants
Subjects: gene expression; cytokinin; senescence; metabolic pathways; Solexa sequencing; transgenic plants; cotton
Species: Gossypium hirsutum

Received: September 23, 2012; Accepted: January 8, 2013; Published: September 1, 2013Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Zhao, P., Zhang, N., Yin, Z.J., Liu, Y.D., & Shen, F.F. (2013). Analysis of differentially expressed genes in response to endogenous cytokinins during cotton leaf senescence. Biologia plantarum, 57(3), 425-432. doi: 10.1007/s10535-013-0324-2.
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

    References

    1. Agarwal, P. Jha, B.: Transcription factors in plants and ABA dependent and independent abiotic stress signalling. - Biol. Plant. 54: 201-212, 2010. Go to original source...
    2. Argyros, R.D., Mathews, D.E., Chiang, Y.H., Palmer, C.M., Thibault, D.M., Etheridge, N., Argyros, D.A., Mason, M.G., Kieber, J.J. Schaller, G.E.: Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. - Plant Cell. 20: 2102-2116, 2008. Go to original source...
    3. Audic, S. Claverie, J.M.: The significance of digital gene expression profiles. - Genome Res. 7: 986-995, 1997. Go to original source...
    4. Azevedo, C., Santos-Rosa, M.J. Shirasu, K.: The U-box protein family in plants. - Trends Plant Sci. 6: 354-358, 2001. Go to original source...
    5. Belintani, N., Guerzoni, J., Moreira, R. Vieira, L.: Improving low-temperature tolerance in sugarcane by expressing the ipt gene under a cold inducible promoter. - Biol. Plant. 56: 71-77, 2012. Go to original source...
    6. Benjamini, Y. Yekutieli, D.: The control of the false discovery rate in multiple testing under dependency. - Ann Statistics 29: 1165-1188, 2001.
    7. Brenner, W.G., Romanov, G.A., Kollmer, I., Burkle, L. Schmulling, T.: Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokininsensitive processes and suggest cytokinin action through transcriptional cascades. - Plant J. 44: 314-333, 2005. Go to original source...
    8. Calderini, O., Bovone, T., Scotti, C., Pupilli, F., Piano, E. Arcioni, S.: Delay of leaf senescence in Medicago sativa transformed with the ipt gene controlled by the senescence-specific promoter SAG12. - Plant Cell Rep. 26: 611-615, 2007. Go to original source...
    9. Chang, H., Jones, M.L., Banowetz, G.M. Clark, D.G.: Overproduction of cytokinins in petunia flowers transformed with P(SAG12)-IPT delays corolla senescence and decreases sensitivity to ethylene. - Plant Physiol. 132: 2174-2183, 2003. Go to original source...
    10. Chen, H.H., Li, Z.L., Zhang, J. Ding, Z.N.: [Study on the antiaging effect of flavonoids in hickory leaf.] - Nat. Prod. Res. Dev. 20: 892-895, 2008. [In Chin.].
    11. Debellis, L., Tsugeki, R. Nishimura, M.: Glyoxylate cycle enzymes in peroxisomes isolated from petals of pumpkin (Cucurbita sps.) during senescence. - Plant Cell Physiol. 32: 1227-1235, 1991.
    12. Ekman, D.R., Lorenz, W.W., Przybyla, A.E., Wolfe, N.L. Dean, J.F.: SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene. - Plant Physiol. 133: 1397-1406, 2003. Go to original source...
    13. Graham, I.A., Leaver, C.J. Smith, S.M.: Induction of malate synthase gene expression in senescent and detached organs of cucumber. - Plant Cell. 4: 349-357, 1992. Go to original source...
    14. Gray, W.M.: Hormonal regulation of plant growth and development. - PLoS Biol. 2: E311, 2004. Go to original source...
    15. Guo, Y. Gan, S.: AtNAP, a NAC family transcription factor, has an important role in leaf senescence. - Plant J. 46: 601-612, 2006. Go to original source...
    16. Hayano-Kanashiro, C., Calderon-Vazquez, C., Ibarra-Laclette, E., Herrera-Estrella, L. Simpson, J.: Analysis of gene expression and physiological responses in three Mexican maize landraces under drought stress and recovery irrigation. - PLoS One. 4: e7531, 2009. Go to original source...
    17. Huang, B.R., Xing, J.P., Xu, Y., Tian, J.A. Gianfagna, T.: Suppression of shade- or heat-induced leaf senescence in creeping bentgrass through transformation with the ipt gene for cytokinin synthesis. - J. amer. Soc. hort. Sci. 134: 602-609, 2009.
    18. Huang, Y.J., To, K.Y., Yap, M.N., Chiang, W.J., Suen, D.F. Chen, S.C.: Cloning and characterization of leaf senescence up-regulated genes in sweet potato. - Physiol. Plant. 113: 384-391, 2001. Go to original source...
    19. Jones, B., Gunneras, S.A., Petersson, S.V., Tarkowski, P., Graham, N., May, S., Dolezal, K., Sandberg, G. Ljung, K.: Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. - Plant Cell. 22: 2956-2969, 2010. Go to original source...
    20. Kiba, T., Kudo, T., Kojima, M. Sakakibara, H.: Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. - J. exp. Bot. 62: 1399-1409, 2011. Go to original source...
    21. Kim, H.J., Ryu, H., Hong, S.H., Woo, H.R., Lim, P.O., Lee, I.C., Sheen, J., Nam, H.G. Hwang, I.: Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. - Proc. nat. Acad. Sci. USA. 103: 814-819, 2006. Go to original source...
    22. Köllmer, I., Werner, T. Schmülling, T.: Ectopic expression of different cytokinin-regulated transcription factor genes of Arabidopsis thaliana alters plant growth and development. - J. Plant Physiol. 168: 1320-1327, 2011. Go to original source...
    23. Kurepa, J., Herouart, D., Van Montagu, M. Inze, D.: Differential expression of CuZn- and Fe-superoxide dismutase genes of tobacco during development, oxidative stress, and hormonal treatments. - Plant Cell Physiol. 38: 463-470, 1997. Go to original source...
    24. Lapointe, M., Mackenzie, T.D. Morse, D.: An external deltacarbonic anhydrase in a free-living marine dinoflagellate may circumvent diffusion-limited carbon acquisition. - Plant Physiol. 147: 1427-1436, 2008. Go to original source...
    25. Li, Q., Robson, P.R., Bettany, A.J., Donnison, I.S., Thomas, H. Scott, I.M.: Modification of senescence in ryegrass transformed with IPT under the control of a monocot senescence-enhanced promoter. - Plant Cell Rep. 22: 816-821, 2004. Go to original source...
    26. Liang, W., Li, C., Liu, F., Jiang, H., Li, S., Sun, J. Wu, X.: The Arabidopsis homologs of CCR4-associated factor 1 show mRNA deadenylation activity and play a role in plant defence responses. - Cell. Res. 19: 307-316, 2009. Go to original source...
    27. Lin, Y.J., Cao, M.L., Xu, C.G., Chen, H., Wei, J. Zhang, Q.F.: Cultivating rice with delaying leaf-senescence by PSAG12-IPT gene transformation. - Acta bot. sin. 44: 1333-1338, 2002.
    28. Liu, J., Wu, Y.H., Yan, J.J., Liu, Y.D. Shen, F.F.: Protein degradation and nitrogen remobilization during leaf senescence. - J. Plant Biol. 51: 11-19, 2008. Go to original source...
    29. Liu, Y., Yin, Z., Yu, J., Li, J., Wei, H., Han, X. Shen, F.: Improved salt tolerance and delayed leaf senescence in transgenic cotton expressing the Agrobacterium IPT gene. - Biol. Plant. 56: 237-246, 2012. Go to original source...
    30. McCabe, M.S., Garratt, L.C., Schepers, F., Jordi, W.J., Stoopen, G.M., Davelaar, E., van Rhijn, J.H., Power, J.B. Davey, M.R.: Effects of P(SAG12)-IPT gene expression on development and senescence in transgenic lettuce. - Plant Physiol. 127: 505-516, 2001. Go to original source...
    31. Miller, C.O.: Cytokinin control of some oxidative processes. - Physiol. Biochem. Cytokinins Plants 507: 289-293, 1992.
    32. Naik, G.R., Mukherjee, I., Reid, D.M.: Influence of cytokinins on the methyl jasmonate-promoted senescence in Helianthus annuus cotyledons. - Plant Growth Regul. 38: 61-68, 2002. Go to original source...
    33. Nishiyama, R., Watanabe, Y., Fujita, Y., Le, D.T., Kojima, M., Werner, T., Vankova, R., Yamaguchi-Shinozaki, K., Shinozaki, K., Kakimoto, T., Sakakibara, H., Schmulling, T. Tran, L.S.: Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. - Plant Cell 23: 2169-2183, 2011. Go to original source...
    34. Nooden, L.D., Guiamet, J.J. John, I.: Senescence mechanisms. - Physiol. Plant. 101: 746-753, 1997. Go to original source...
    35. Pandey, S., Ranade, S.A., Nagar, P.K. Kumar, N.: Role of polyamines and ethylene as modulators of plant senescence. - J. Biosci. 25: 291-299, 2000. Go to original source...
    36. Parker, R. Song, H.: The enzymes and control of eukaryotic mRNA turnover. - Natur. Struct. mol. Biol. 11: 121-127, 2004.
    37. Petit-Paly, G., Franck, T., Brisson, L., Kevers, C., Chenieux, J.C. Rideau, M.: Cytokinin modulates catalase activity and coumarin accumulation in in vitro cultures of tobacco. - J. Plant Physiol. 155: 9-15, 1999. Go to original source...
    38. Qin, H., Gu, Q., Zhang, J., Sun, L., Kuppu, S., Zhang, Y., Burow, M., Payton, P., Blumwald, E. Zhang, H.: Regulated expression of an isopentenyltransferase gene (IPT) in peanut significantly improves drought tolerance and increases yield under field conditions. - Plant Cell Physiol. 52: 1904-1914, 2011.
    39. Robson, P.R., Donnison, I.S., Wang, K., Frame, B., Pegg, S.E., Thomas, A. Thomas, H.: Leaf senescence is delayed in maize expressing the Agrobacterium IPT gene under the control of a novel maize senescence-enhanced promoter. - Plant Biotechnol. J. 2: 101-112, 2004. Go to original source...
    40. Saftner, R.A., Baldi, B.G.: Polyamine levels and tomato fruit development: possible interaction with ethylene. - Plant Physiol. 92: 547-550, 1990. Go to original source...
    41. Singla-Pareek, S.L., Reddy, M.K. Sopory, S.K.: Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance. - Proc. nat. Acad. Sci. USA. 101: 6326-6326, 2004.
    42. Sood, S. Nagar, P.K.: The effect of polyamines on leaf senescence in two diverse rose species. - Plant Growth Regul. 39: 155-160, 2003. Go to original source...
    43. Sykorova, B., Kuresova, G., Daskalova, S., Trckova, M., Hoyerova, K., Raimanova, I., Motyka, V., Travnickova, A., Elliott, M.C. Kaminek, M.: Senescence-induced ectopic expression of the A. tumefaciens ipt gene in wheat delays leaf senescence, increases cytokinin content, nitrate influx, and nitrate reductase activity, but does not affect grain yield. - J. exp. Bot. 59: 377-387, 2008. Go to original source...
    44. Synková, H., Semoradová, S., Schnablová, R., Wiitters, E., Husak, M. Valcke, R.: Cytokinin-induced activity of antioxidant enzymes in transgenic Pssu-ipt tobacco during plant ontogeny. - Biol. Plant. 50: 31-41, 2006. Go to original source...
    45. Taniguchi, M., Sasaki, N., Tsuge, T., Aoyama, T. Oka, A.: ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. - Plant Cell Physiol. 48: 263-277, 2007. Go to original source...
    46. Thornalley, P.J.: The glyoxalase system - new developments towards functional-characterization of a metabolic pathway fundamental to biological life. - Biochem J. 269: 1-11, 1990. Go to original source...
    47. Tran, L.S., Urao, T., Qin, F., Maruyama, K., Kakimoto, T., Shinozaki, K. Yamaguchi-Shinozaki, K.: Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. - Proc. nat. Acad. Sci. USA 104: 20623-20628, 2007. Go to original source...
    48. Walley, J.W., Kelley, D.R., Nestorova, G., Hirschberg, D.L. Dehesh, K.: Arabidopsis deadenylases AtCAF1a and AtCAF1b play overlapping and distinct roles in mediating environmental stress responses. - Plant Physiol. 152: 866-875, 2010. Go to original source...
    49. Willige, B.C., Ghosh, S., Nill, C., Zourelidou, M., Dohmann, E.M., Maier, A. Schwechheimer, C.: The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. - Plant Cell 19: 1209-1220, 2007. Go to original source...
    50. Yamada, H., Suzuki, T., Terada, K., Takei, K., Ishikawa, K., Miwa, K., Yamashino, T. Mizuno, T.: The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. - Plant Cell Physiol. 42: 1017-1023, 2001. Go to original source...
    51. Yokoyama, A., Yamashino, T., Amano, Y., Tajima, Y., Imamura, A., Sakakibara, H. Mizuno, T.: Type-B ARR transcription factors, ARR10 and ARR12, are implicated in cytokinin-mediated regulation of protoxylem differentiation in roots of Arabidopsis thaliana. - Plant Cell Physiol. 48: 84-96, 2007. Go to original source...
    52. Zavaleta-Mancera, H.A., Lopez-Delgado, H., Loza-Tavera, H., Mora-Herrera, M., Trevilla-Garcia, C., Vargas-Suarez, M. Ougham, H.: Cytokinin promotes catalase and ascorbate peroxidase activities and preserves the chloroplast integrity during dark-senescence. - J. Plant Physiol. 164: 1572-1582, 2007. Go to original source...
    53. Zhang, X., Zhang, Z., Li, J., Wu, L., Guo, J., Ouyang, L., Xia, Y., Huang, X. Pang, X.: Correlation of leaf senescence and gene expression/activities of chlorophyll degradation enzymes in harvested Chinese flowering cabbage (Brassica rapa var. parachinensis). - J. Plant Physiol. 168: 2081-2087, 2011. Go to original source...

    Return to the content