Regulation of Leaf Senescence by NTL9-mediated Osmotic Stress Signaling in Arabidopsis

  • Yoon, Hye-Kyung (Molecular Signaling Laboratory, Department of Chemistry, Seoul National University) ;
  • Kim, Sang-Gyu (Molecular Signaling Laboratory, Department of Chemistry, Seoul National University) ;
  • Kim, Sun-Young (Molecular Signaling Laboratory, Department of Chemistry, Seoul National University) ;
  • Park, Chung-Mo (Molecular Signaling Laboratory, Department of Chemistry, Seoul National University)
  • Received : 2007.10.16
  • Accepted : 2007.12.06
  • Published : 2008.05.31


Leaf senescence is a highly regulated genetic process that constitutes the last stage of plant development and provides adaptive fitness by relocating metabolites from senescing leaves to reproducing seeds. Characterization of various senescence mutants, mostly in Arabidopsis, and genome-wide analyses of gene expression, have identified a wide array of regulatory components, including transcription factors and enzymes as well as signaling molecules mediating growth hormones and environmental stress responses. In this work we demonstrate that a membrane-associated NAC transcription factor, NTL9, mediates osmotic stress signaling in leaf senescence. The NTL9 gene is induced by osmotic stress. Furthermore, activation of the dormant, membrane-associated NTL9 is elevated under the same conditions. A series of senescence-associated genes (SAGs) were upregulated in transgenic plants overexpressing an activated form of NTL9, and some of them were slightly but reproducibly downregulated in a T-DNA insertional NTL9 knockout mutant. These observations indicate that NTL9 mediates osmotic stress responses that affect leaf senescence, providing a genetic link between intrinsic genetic programs and external signals in the control of leaf senescence.


Supported by : National Research Laboratory, Korea Research Foundation, Korea Science and Engineering Foundation


  1. Binyamin, L., Falah, M., Portnoy, V., Soudry, E., and Gepstein, S. (2001). The early light-induced protein is also produced during leaf senescence of Nicotiana tabacum. Planta 212, 591-597
  2. Bohnert, H.J., Nelson, D.E., and Jensen, R.G. (1995). Adaptations to environmental stresses. Plant Cell 7, 1099-1111
  3. Brown, M.S., Ye, J., Rawson, R.B., and Goldstein, J.L. (2000). Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100, 391-398
  4. Buchanan-Wollaston, V. (1994). Isolation of cDNA clones for genes that are expressed during leaf senescence in Brassica napus. Identification of a gene encoding a senescencespecific metallothionein-like protein. Plant Physiol. 105, 839-846
  5. Buchanan-Wollaston, V., and Ainsworth, C. (1997). Leaf sensecence in Brassica napus: cloning of senescence related genes by subtractive hybridization. Plant Mol. Biol. 33, 821-834
  6. Buchanan-Wollaston, V., Page, T., Harrison, E., Breeze, E., Lim, P.O., Nam, H.G., Lin, J.F., Wu, S.H., Swidzinski, J., and Ishizaki, K., et al. (2005). Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation- induced senescence in Arabidopsis. Plant J. 42, 567-585
  7. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743
  8. Dangl, J.L., Dietrich, R.A., and Thomas, H. (2000). Senescence and programmed cell death. In Biochemistry and Molecular Biology of Plants, B.B. Buchanan, W. Gruissem and R.L. Jones, eds. (Rockville: Courier Companies), pp. 1044-1099
  9. Gan, S., and Amasino, R.M. (1997). Making sense of sensecence. Plant Physiol. 113, 313-319
  10. Gepstein, S., Sabehi, G., Carp, M.J., Hajouj, T., Nesher, M.F., Yariv, I., Dor, C., and Bassani, M. (2003). Large-scale identification of leaf senescence-associated genes. Plant J. 36, 629-642
  11. Guo, Y., Cai, Z., and Gan, S. (2004). Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ. 27, 521-549
  12. Guo, Y., and Gan, S. (2006). AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46, 601-612
  13. Hanfrey, C., Fife, M., and Buchanan-Wollaston, V. (1996). Leaf senescence in Brassica napus: expression of genes encoding pathogenesis-related proteins. Plant Mol. Biol. 30, 597-609
  14. He, Y., Fukushige, H., Hildebrand, D.F., and Gan, S. (2002). Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol. 128, 876-884
  15. Hoppe, T., Rape, M., and Jentsch, S. (2001). Membrane-bound transcription factors: regulated release by RIP or RUP. Curr. Opin. Cell Biol. 13, 344-348
  16. Iwata, Y., and Koizumi, N. (2005). An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc. Natl. Acad. Sci. USA 102, 5280-5285
  17. John, I., Hackett, R., Cooper, W., Drake, R., Farrell, A., and Grierson, D. (1997). Cloning and characterization of tomato leaf senescence-related cDNAs. Plant Mol. Biol. 33, 641-651
  18. Kaffman, A., and O'Shea, E.K. (1999). Regulation of nuclear localization: a key to a door. Annu. Rev. Cell Dev. Biol. 15, 291-339
  19. Kim, Y.S., Kim, S.G., Park, J.E., Park, H.Y., Lim, M.H., Chua, N.H., and Park, C.M. (2006). A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18, 3132-3144
  20. Kim, S.G., Kim, S.Y., and Park, C.M. (2007a). A membraneassociated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226, 647-654
  21. Kim, S.Y., Kim, S.G., Kim, Y.S., Seo, P.J., Bae M., Yoon, H.K., and Park, C.M. (2007b). Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucleic Acids Res. 35, 203-213
  22. Lim, P.O., and Nam, H.G. (2005). The molecular and genetic control of leaf senescence and longevity in Arabidopsis. Curr. Top. Dev. Biol. 67, 49-83
  23. Lim, P.O., Woo, H.R., and Nam, H.G. (2003). Molecular genetics of leaf senescence in Arabidopsis. Trends Plant Sci. 8, 272-278
  24. Lim, P.O., Kim, H.J., and Nam, H.G. (2007). Leaf senescence. Annu. Rev. Plant Biol. 58, 115-136
  25. Lin, J.F., and Wu, S.H. (2004). Molecular events in senescing Arabidopsis leaves. Plant J. 39, 612-628
  26. Morris, K., MacKerness, S.A., Page, T., John, C.F., Murphy, A.M., Carr, J.P., and Buchanan-Wollaston, V. (2000). Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J. 23, 677-685
  27. Olsen, A.N., Ernst, H.A., Leggio, L.L., and Skriver, K. (2005). NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci. 10, 79-87
  28. Ooka, H., Satoh, K., Doi, K., Nagata, T., Otomo, Y., Murakami, K., Matsubara, K., Osato, N., Kawai, J., Carninci P., et al. (2003). Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res. 10, 239-247
  29. Pourtau, N., Mares, M., Purdy, S., Quentin, N., Ruel, A., and Wingler, A. (2004). Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence. Planta 219, 765-772
  30. Pourtau, N., Jennings, R., Pelzer, E., Pallas, J., and Wingler, A. (2006). Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224, 556-568
  31. Quirino, B.F., Normanly, J., and Amasino, R.M. (1999). Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defenserelated genes. Plant Mol. Biol. 40, 267-278
  32. Quirino, B.F., Noh, Y.S., Himelblau, E., and Amasino, R.M. (2000). Molecular aspects of leaf senescence. Trends Plant Sci. 5, 278-282
  33. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K., Catoni, E., Desimone, M., Frommer, W.B., Flügge, U.I., and Kunze, R. (2003). ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131,16-26
  34. Verslues, P.E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J., and Zhu, J.K. (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J. 45, 523-539
  35. Vik, A., and Rine, J. (2000). Membrane biology: membraneregulated transcription. Curr. Biol. 10, R869-R871
  36. Weaver, L.M., Gan, S., Quirino, B., and Amasino, R.M. (1998). A comparison of the expression patterns of several senescenceassociated genes in response to stress and hormone treatment. Plant Mol. Biol. 37, 455-469
  37. Xiong, L., and Zhu, J.K. (2002). Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ. 25, 131-139
  38. Yoo, S.C., Cho, S.H., Zhang, H., Paik, H.C., Lee, C.H., Li, J., Yoo, J.H., Lee, B.W., Koh, H.J., Seo, H.S., et al. (2007). Quantitative trait loci associated with functional stay-green SNU-SG1 in rice. Mol. Cells 24, 83-94
  39. Yoshida, S. (2003). Molecular regulation of leaf senescence. Curr. Opin. Plant Biol. 6, 79-84
  40. Zhu, J.K. (2001). Cell signaling under salt, water and cold stresses. Curr. Opin. Plant Biol. 4, 401-406
  41. Zhu, J.K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273