DOI QR코드

DOI QR Code

Rice OsACDR1 (Oryza sativa Accelerated Cell Death and Resistance 1) Is a Potential Positive Regulator of Fungal Disease Resistance

  • Kim, Jung-A (Department of Molecular Biology, College of Natural Science, Sejong University) ;
  • Cho, Kyoungwon (Environmental Biology Division, National Institute for Environmental Studies (NIES)) ;
  • Singh, Raksha (Department of Molecular Biology, College of Natural Science, Sejong University) ;
  • Jung, Young-Ho (Department of Molecular Biology, College of Natural Science, Sejong University) ;
  • Jeong, Seung-Hee (Department of Molecular Biology, College of Natural Science, Sejong University) ;
  • Kim, So-Hee (Department of Molecular Biology, College of Natural Science, Sejong University) ;
  • Lee, Jae-eun (Department of Molecular Biology, College of Natural Science, Sejong University) ;
  • Cho, Yoon-Seong (Department of Molecular Biology, College of Natural Science, Sejong University) ;
  • Agrawal, Ganesh K. (Research Laboratory for Biotechnology and Biochemistry) ;
  • Rakwal, Randeep (Research Laboratory for Biotechnology and Biochemistry) ;
  • Tamogami, Shigeru (Laboratory of Biologically Active Compounds, Department of Biological Production, Akita Prefectural University) ;
  • Kersten, Birgit (Max Planck Institute for Molecular Plant Physiology, GabiPD Team, Bioinformatics) ;
  • Jeon, Jong-Seong (Graduate School of Biotechnology and Plant Metabolism Research Center, Kyung Hee University) ;
  • An, Gynheung (National Research Laboratory, Department of Life Science and Center for Functional Genomics, Pohang University of Science and Technology) ;
  • Jwa, Nam-Soo (Department of Molecular Biology, College of Natural Science, Sejong University)
  • Received : 2009.07.03
  • Accepted : 2009.10.08
  • Published : 2009.11.30

Abstract

Rice Oryza sativa accelerated cell death and resistance 1 (OsACDR1) encodes a putative Raf-like mitogen-activated protein kinase kinase kinase (MAPKKK). We had previously reported upregulation of the OsACDR1 transcript by a range of environmental stimuli involved in eliciting defense-related pathways. Here we apply biochemical, gain and loss-of-function approaches to characterize OsACDR1 function in rice. The OsACDR1 protein showed autophosphorylation and possessed kinase activity. Rice plants overexpressing OsACDR1 exhibited spontaneous hypersensitive response (HR)-like lesions on leaves, upregulation of defense-related marker genes and accumulation of phenolic compounds and secondary metabolites (phytoalexins). These transgenic plants also acquired enhanced resistance to a fungal pathogen (Magnaporthe grisea) and showed inhibition of appressorial penetration on the leaf surface. In contrast, loss-of-function and RNA silenced OsACDR1 rice mutant plants showed downregulation of defense-related marker genes expressions and susceptibility to M. grisea. Furthermore, transient expression of an OsACDR1:GFP fusion protein in rice protoplast and onion epidermal cells revealed its localization to the nucleus. These results indicate that OsACDR1 plays an important role in the positive regulation of disease resistance in rice.

Keywords

Acknowledgement

Supported by : Korea Science and Engineering Foundation, Ministry of Science and Technology, Ministry of the Environment

References

  1. Akira, S., Uematsu, S., and Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell 124, 783-801 https://doi.org/10.1016/j.cell.2006.02.015
  2. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel F.M., and Sheen, J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983 https://doi.org/10.1038/415977a
  3. Bari, R., and Jones, J.D. (2009). Role of plant hormones in plant defense responses. Plant Mol. Biol. 69, 473-488 https://doi.org/10.1007/s11103-008-9435-0
  4. Chisholm, S.T., Coaker, G., Day, B., and Staskawicz, B.J. (2006). Host–microbe interactions: shaping the evolution of the plant immune response. Cell 24, 803-814
  5. Clarke, K.L., Larsen, P.B., Wang, X., and Chang, C. (1998). Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc. Natl. Acad. Sci. USA 95, 5401-5406 https://doi.org/10.1073/pnas.95.9.5401
  6. Dangl, J.L., and Jones, J.D.G. (2001). Plant pathogens and integrated defence responses to infection. Nature 411, 826-833 https://doi.org/10.1038/35081161
  7. Frye, C.A., and Innes, R.W. (1998). An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10, 947-956 https://doi.org/10.2307/3870681
  8. Frye, C.A., Tang, D., and Innes, R.W. (2001). Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl. Acad. Sci. USA 98, 373-378 https://doi.org/10.1073/pnas.011405198
  9. Hiei, Y., Hta, S., Komari, Y., and Kunashiro, T. (1994). Effective transformation of rice mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271-282 https://doi.org/10.1046/j.1365-313X.1994.6020271.x
  10. Huang, Y., Li, H., Hutchison, C.E., Laskey, J., and Kieber, J.J. (2003). Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J. 33, 221-233 https://doi.org/10.1046/j.1365-313X.2003.01620.x
  11. Ichimura, K. (MAPK Group). (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 7, 301-308 https://doi.org/10.1016/S1360-1385(02)02302-6
  12. Jung, Y.H., Agrawal, G.K., Rakwal, R., Kim, J.A., Lee, M.-O., Choi, P.G., Kim, Y.J., Kim, M.J., Shibato, J., Kim, S.-H., et al. (2006). Functional characterization of OsRacB GTPase-a potentially negative regulator of basal disease resistance in rice. Plant Physiol. Biochem. 44, 68-77 https://doi.org/10.1016/j.plaphy.2005.12.001
  13. Jwa, N.S., Agrawal, G.K., Tamogami, S., Yonekura, M., Han, O., Iwahashi, H., and Rakwal, R. (2006). Role of defense/stressrelated marker genes, proteins and secondary metabolites in defining rice self-defense mechanisms. Plant Physiol. Biochem. 44, 261-273 https://doi.org/10.1016/j.plaphy.2006.06.010
  14. Kim, J.A., Agrawal, G.K., Rakwal, R., Han, K.S., Kim, K.N., Yun, C.H., Heu, S., Park, S.Y., Lee, Y.H., Jwa, N.S., et al. (2003). Molecular cloning and mRNA expression analysis of a novel rice (Oryza sativa L.) MAPK kinase kinase, OsEDR1, an ortholog of Arabidopsis AtEDR1, reveal its role in defense/stress signaling pathways and development. Biochem. Biophys. Res. Commun. 300, 868-876 https://doi.org/10.1016/S0006-291X(02)02944-3
  15. Lee, M.O., Choi, P.G., Kim, J.A, Jung, Y.H., Jung, S.H., Kim, S.H., Kim, J.W., Lee, S.K., Jeon, J.S., Rakwal, R., et al. (2006). Two novel protein kinase genes, OsMSRPK1 and OsMSURPK2, are regulated by diverse environmental stresses in rice. J. Plant Biol. 49, 247-256 https://doi.org/10.1007/BF03030540
  16. Lam, E., Kato, N., and Lawton, M. (2001). Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411, 848-853 https://doi.org/10.1038/35081184
  17. Ligterink, W., and Hirt, H. (2001). Mitogen-activated protein (MAP) kinase pathways in plants: versatile signaling tools. Int. Rev. Cytol. 201, 209-275 https://doi.org/10.1016/S0074-7696(01)01004-X
  18. Lin, Z., Alexander, L., Hackett, R., and Grierson, D. (2008). LeCTR2, a CTR1-like protein kinase from tomato, plays a role in ethylene signalling, development and defence. Plant J. 54, 1083-1093 https://doi.org/10.1111/j.1365-313X.2008.03481.x
  19. Lorrain, S., Vailleau, F., Balague, C., and Roby, D. (2003). Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8, 263-271 https://doi.org/10.1016/S1360-1385(03)00108-0
  20. Nakagami, H., Pitzschke, A., and Hirt, H. (2005). Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci. 10, 339-346 https://doi.org/10.1016/j.tplants.2005.05.009
  21. Pedley, K.F., and Martin, G.B. (2004). Identification of MAPKs and their possible MAPK kinase activators involved in the Ptomediated defense response of tomato. J. Biol. Chem. 279, 49229-49235 https://doi.org/10.1074/jbc.M410323200
  22. Pieterse, C.M.J., and Dicke, M. (2007). Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci. 12, 564-568 https://doi.org/10.1016/j.tplants.2007.09.004
  23. Rakwal, R., Kimura, S., Shibato, J., Nojima, K., Kim, Y.-K., Nahm, B.H., Jwa, N.-S., Endo, S., Tanaka, K., and Iwahashi, H. (2008). Growth retardation and death of rice plants irradiated with carbon ion beams is preceded by very early dose- and timedependent gene expression changes. Mol. Cells 25, 272-278
  24. Tamogami, S., Rakwal, R., and Kodama, O. (1997). Phytoalexin production by amino acid conjugates of jasmonic acid through induction of naringenin-7-O-methyltransferase, a key enzyme on phytoalexin biosynthesis in rice (Oryza sativa L.). FEBS Lett. 401, 239-242 https://doi.org/10.1016/S0014-5793(96)01482-2
  25. Tang, D., and Innes, R.W., (2002). Overexpression of a kinasedeficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J. 32, 975-983 https://doi.org/10.1046/j.1365-313X.2002.01482.x
  26. Tang, D., Christiansen, K.M., and Innes, R.W. (2005). Regulation of plant disease resistance, stress responses, cell death, and ethylene signaling in Arabidopsis by the EDR1 protein kinase. Plant Physiol. 138, 1018-1026 https://doi.org/10.1104/pp.105.060400
  27. Van Etten, H.D., Mansfield, J.W., Bailey, J.A., and Farmer, E.E. (1994). Two classes of plant antibiotics: phytoalexins versus''phytoanticipins'. Plant Cell. 6, 1191-1192 https://doi.org/10.2307/3869817
  28. Wasternack, C. (2007). An update on biosynthesis, signal transduction and action in plant stress responses, growth and development. Ann. Bot. 100, 681-697 https://doi.org/10.1093/aob/mcm079
  29. Yin, Z., Chen, J., Zeng, L., Goh, M., Leung, H., Khush, G.S., and Wang, G.L. (2000). Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol. Plant Microbe Interact. 13, 869-876 https://doi.org/10.1094/MPMI.2000.13.8.869

Cited by

  1. Comparative Phenotypic and Physiological Characteristics of Spotted Leaf 6 (spl6) and Brown Leaf Spot2 (bl2) Lesion Mimic Mutants (LMM) in Rice vol.30, pp.6, 2009, https://doi.org/10.1007/s10059-010-0151-7
  2. Biotechnology and Plant Disease Control-Role of RNA Interference vol.1, pp.2, 2009, https://doi.org/10.4236/ajps.2010.12008
  3. Rice Mitogen-Activated Protein Kinase Interactome Analysis Using the Yeast Two-Hybrid System vol.160, pp.1, 2009, https://doi.org/10.1104/pp.112.200071
  4. SPL5, a cell death and defense-related gene, encodes a putative splicing factor 3b subunit 3 (SF3b3) in rice vol.30, pp.2, 2009, https://doi.org/10.1007/s11032-011-9677-4
  5. Ectopic Expression of Hrf1 Enhances Bacterial Resistance via Regulation of Diterpene Phytoalexins, Silicon and Reactive Oxygen Species Burst in Rice vol.7, pp.9, 2009, https://doi.org/10.1371/journal.pone.0043914
  6. RNA interference: evolutions and applications in plant disease management vol.46, pp.12, 2009, https://doi.org/10.1080/03235408.2013.769315
  7. Proteomic analysis of a disease-resistance-enhanced lesion mimic mutant spotted leaf 5 in rice vol.6, pp.None, 2009, https://doi.org/10.1186/1939-8433-6-1
  8. Metabolomics of cereals under biotic stress: current knowledge and techniques vol.4, pp.None, 2013, https://doi.org/10.3389/fpls.2013.00082
  9. Oscyp71Z2 involves diterpenoid phytoalexin biosynthesis that contributes to bacterial blight resistance in rice vol.207, pp.None, 2009, https://doi.org/10.1016/j.plantsci.2013.02.005
  10. Modulation of Phytoalexin Biosynthesis in Engineered Plants for Disease Resistance vol.14, pp.7, 2009, https://doi.org/10.3390/ijms140714136
  11. The MAPKKK Gene Family in Gossypium raimondii : Genome-Wide Identification, Classification and Expression Analysis vol.14, pp.9, 2013, https://doi.org/10.3390/ijms140918740
  12. Molecular identification and interaction assay of the gene (OsUbc13) encoding a ubiquitin-conjugating enzyme in rice vol.15, pp.7, 2009, https://doi.org/10.1631/jzus.b1300273
  13. Transcriptome profiling of the spl5 mutant reveals that SPL5 has a negative role in the biosynthesis of serotonin for rice disease resistance vol.8, pp.None, 2009, https://doi.org/10.1186/s12284-015-0052-7
  14. Secondary metabolites in fungus-plant interactions vol.6, pp.None, 2009, https://doi.org/10.3389/fpls.2015.00573
  15. Mutation of SPOTTED LEAF3 (SPL3) impairs abscisic acid-responsive signalling and delays leaf senescence in rice vol.66, pp.22, 2009, https://doi.org/10.1093/jxb/erv401
  16. Updated Rice Kinase Database RKD 2.0: enabling transcriptome and functional analysis of rice kinase genes vol.9, pp.None, 2009, https://doi.org/10.1186/s12284-016-0106-5
  17. Rice WRKY11 Plays a Role in Pathogen Defense and Drought Tolerance vol.11, pp.None, 2009, https://doi.org/10.1186/s12284-018-0199-0
  18. The Rice SPOTTED LEAF4 ( SPL4 ) Encodes a Plant Spastin That Inhibits ROS Accumulation in Leaf Development and Functions in Leaf Senescence vol.9, pp.None, 2009, https://doi.org/10.3389/fpls.2018.01925
  19. Transcriptomic Analysis of Oryza sativa Leaves Reveals Key Changes in Response to Magnaporthe oryzae MSP1 vol.34, pp.4, 2009, https://doi.org/10.5423/ppj.oa.01.2018.0008
  20. Identification on mitogen-activated protein kinase signaling cascades by integrating protein interaction with transcriptional profiling analysis in cotton vol.8, pp.None, 2018, https://doi.org/10.1038/s41598-018-26400-w
  21. Functional inactivation of OsGCNT induces enhanced disease resistance to Xanthomonas oryzae pv. oryzae in rice vol.18, pp.None, 2009, https://doi.org/10.1186/s12870-018-1489-9
  22. Identification of a Novel Semi-Dominant Spotted-Leaf Mutant with Enhanced Resistance to Xanthomonas oryzae pv. oryzae in Rice vol.19, pp.12, 2009, https://doi.org/10.3390/ijms19123766
  23. OsMAPKKK63 is involved in salt stress response and seed dormancy control vol.14, pp.3, 2009, https://doi.org/10.1080/15592324.2019.1578633
  24. Update on the Roles of Rice MAPK Cascades vol.22, pp.4, 2009, https://doi.org/10.3390/ijms22041679
  25. Heredity and gene mapping of a novel white stripe leaf mutant in wheat vol.20, pp.7, 2009, https://doi.org/10.1016/s2095-3119(20)63345-7
  26. SPL36 Encodes a Receptor-like Protein Kinase that Regulates Programmed Cell Death and Defense Responses in Rice vol.14, pp.1, 2009, https://doi.org/10.1186/s12284-021-00475-y