A Novel Rice MAPK Gene, OsBIMK2, is Involved in Disease-Resistance Responses

Abstract

The mitogen-activated protein kinase (MAPK) cascades play important roles in transmission of extracellular signals to the downstream effector proteins through a mechanism of protein phosphorylation. In this study, we isolated and identified a novel rice MAPK gene, OsBIMK2 (Oryzae sativa L. BTH-Induced MAP Kinase 2). The OsBIMK2 encodes a 506 amino acid protein with molecular weight of 63 kD. The recombinant OsBIMK2 expressed in Escherichia coli showed an autophosphorylation activity in vitro. OsBIMK2 is a single-copy gene in the rice genome. Expression of OsBIMK2 was activated upon treatment with benzothiadiazole (BTH), which is capable of inducing disease resistance in rice. Expression of OsBIMK2 was also up-regulated during early stage after inoculation with Magnaporthe grisea in BTH-treated rice seedlings and during an incompatible interaction between M. grisea and a blast-resistant rice genotype. Over-expression of the rice OsBIMK2 gene in transgenic tobacco resulted in an enhanced disease resistance against tomato mosaic virus and a fungal pathogen, Alternaria alternata. These results suggest that OsBIMK2 plays a role in disease resistance responses.

Key words

MAPK cascades - benzothiadiazole (BTH) - Magnaporthe grisea - disease resistance response - rice (Oryza sativa L.) - transgenic tobacco - tomato mosaic virus (ToMV) - Alternaria alternata

References

• 1 Agrawal G. K., Rakwal R., Iwahashi H.. Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues.  Biochemistry and Biophysics Research Communication. (2002);  294 1009-1016
• 2 Agrawal G. K., Iwahashi H., Rakwal R.. Rice MAPKs.  Biochemistry and Biophysics Research Communication. (2003 a);  302 171-180
• 3 Agrawal G. K., Agrawal S. K., Shibato J., Iwahashi H., Rakwal R.. Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation.  Biochemistry and Biophysics Research Communication. (2003 b);  300 775-783
• 4 Asai T., Tena G., Plotnikova J., Willmann M. R., Chiu W. L., Gomez-Gomez L., Boller T., Ausubel F. M., Sheen J.. MAP kinase signaling cascade in Arabidopsis innate immunity.  Nature. (2002);  415 977-983
• 5 Cardinale F., Jonak C., Ligterink W., Niehaus K., Boller T., Hirt H.. Differential activation of four specific MAPK pathways by distinct elicitors.  Journal of Biological Chemistry. (2000);  275 36734-36740
• 6 Cheong Y. H., Moon B. C., Kim J. K., Kim C. Y., Kim M. C., Kim I. H., Park C. Y., Kim J. C., Park B. O., Koo S. C., Yoon H. W., Chung W. S., Lim C. O., Lee S. Y., Cho M. J.. BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor.  Plant Physiology. (2003);  132 1961-1972
• 7 Desikan R., Hancock J. T., Ichimura K., Shinozaki K., Neill S. J.. Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6.  Plant Physiology. (2001);  126 1579-1587
• 8 del Pozo O., Pedley K. F., Martin G. B.. MAPKKKalpha is a positive regulator of cell death associated with both plant immunity and disease.  The EMBO Journal. (2004);  23 3072-3082
• 9 Ekengren S. K., Liu Y., Schiff M., Dinesh-Kumar S. P., Martin G. B.. Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato.  The Plant Journal. (2003);  36 905-917
• 10 Frye C. A., Tang D., Innes R. W.. Negative regulation of defense responses in plants by a conserved MAPKK kinase.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 373-378
• 11 Fu S. F., Chou W. C., Huang D. D., Huang H. J.. Transcriptional regulation of a rice mitogen-activated protein kinase gene, OsMAPK4, in response to environmental stresses.  Plant Cell and Physiology. (2002);  43 958-963
• 12 He C., Fong S. H., Yang D., Wang G. L.. BWMK1, a novel MAP kinase induced by fungal infection and mechanical wounding in rice.  Molecular Plant-Microbe Interaction. (1999);  12 1064-1073
• 13 Her J., Lakhani S., Zu K., Vila J., Dent P., Sturgill T. W., Weber M. J.. Dual phosphorylation and autophosphorylation in mitogen-activated protein (MAP) kinase activation.  Biochemical Journal. (1993);  296 25-31
• 14 Huang Y., Li H., Gupta R., Morris P. C., Luan S., Kieber J. J.. AtMPK4, an Arabidopsis homolog of mitogen-activated protein kinase, is activated in vitro by AtMEK1 through threonine phosphorylation.  Plant Physiology. (2000);  122 1301-1310
• 15 Huang H. J., Fu S. F., Tai Y. H., Chou W. C., Huang D. D.. Expression of Oryza sativa MAP kinase gene is developmentally regulated and stress-responsive.  Physiologia Plantarum. (2002);  114 572-580
• 16 Ichimura K., Mizoguchi T., Yoshida R., Yuasa T., Shinozaki K.. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6.  The Plant Journal. (2000);  24 655-665
• 17 Jin H., Axtell M. J., Dahlbeck D., Ekwenna O., Zhang S., Staskawicz B., Baker B.. NPK1, an MEKK1-like mitogen-activated protein kinase kinase kinase, regulates innate immunity and development in plants.  Developmental Cell. (2002);  3 291-297
• 18 Jin H., Liu Y., Yang K. Y., Kim C. Y., Baker B., Zhang S.. Function of a mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco.  The Plant Journal. (2003);  33 719-731
• 19 Jonak C., Kiegerl S., Ligterink W., Baker P. J., Huskisson N. S., Hirt H.. Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought.  Proceedings of the National Academy of Sciences of the USA. (1996);  93 11274-11279
• 20 Jonak C., Okresz L., Bogre L., Hirt H.. Complexity, cross talk and integration of plant MAP kinase signaling.  Current Opinion in Plant Biology. (2002);  5 415-424
• 21 Kim C. Y., Zhang S.. Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco.  The Plant Journal. (2004);  38 142-151
• 22 Kovtun Y., Chiu W. L., Tena G., Sheen J.. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants.  Proceedings of the National Academy of Sciences of the USA. (2000);  97 2940-2945
• 23 Kyriakis J. M., Avruch J.. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation.  Physiological Review. (2001);  81 807-869
• 24 Lee D. E., Lee I. J., Han O., Baik M. G., Han S. S., Back K.. Pathogen resistance of transgenic rice plants expressing mitogen-activated protein kinase 1, MK1, from Capsicum annuum.  Molecules and Cells. (2004);  17 81-85
• 25 Ligterink W., Hirt H.. Mitogen-activated protein (MAP) kinase pathways in plants: versatile signaling tools.  International Review of Cytology. (2001);  201 209-275
• 26 Ligterink W., Kroj T., zur Nieden U., Hirt H., Scheel D.. Receptor-mediated activation of a MAP kinase in pathogen defense of plants.  Science. (1997);  276 2054-2057
• 27 Luo H., Song F., Goodman R. M., Zheng Z.. Up-regulation of OsBIHD1, a rice gene encoding BELL homeodomain transcriptional factor, in disease resistance responses.  Plant Biology. (2005 a);  7 459-468
• 28 Luo H., Song F., Zheng Z.. Overexpression in transgenic tobacco reveals different roles for the rice homeodomain gene OsBIHD1 in biotic and abiotic stress responses.  Journal of Experimental Botany. (2005 b);  56 2673-2682
• 29 MAPK Group. . Mitogen-activated protein kinase cascades in plants: a new nomenclature.  Trends in Plant Sciences. (2002);  7 301-308
• 30 Menke F. L., van Pelt J. A., Pieterse C. M., Klessig D. F.. Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis.  Plant Cell. (2004);  16 897-907
• 31 Mikolajczyk M., Awotunde O. S., Muszynska G., Klessig D. F., Dobrowolska G.. Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells.  Plant Cell. (2000);  12 165-178
• 32 Mizoguchi T., Irie K., Hirayama T., Hayashida N., Yamaguchi-Shinozaki K., Matsumoto K., Shinozaki K.. A gene encoding a mitogen-activated protein kinase is induced simultaneously with genes for a mitogen-activated protein kinase and S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana.  Proceedings of the National Academy of Sciences of the USA. (1996);  93 765-769
• 33 Mockaitis K., Howell S. H.. Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings.  The Plant Journal. (2000);  24 785-796
• 34 Nuhse T. S., Peck S. C., Hirt H., Boller T.. Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK6.  Journal of Biological Chemistry. (2000);  275 7521-7526
• 35 Ouaked F., Rozhon W., Lecourieux D., Hirt H.. A MAPK pathway mediates ethylene signaling in plants.  The EMBO Journal. (2003);  22 1282-1288
• 36 Petersen M., Brodersen P., Naested H., Andreasson E., Lindhart U., Johansen B., Nielsen H. B., Lacy M., Austin M. J., Park J. E., Sharma S. B., Klessig D. F., Martienssen R., Mattsson O., Jensen A. B., Mundy J.. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance.  Cell. (2000);  103 1111-1120
• 37 Ren D., Yang H., Zhang S.. Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. .  Journal of Biological Chemistry. (2002);  277 559-565
• 38 Roberts C. J., Nelson B., Marton M. J., Stoughton R., Meyer M. R., Bennett H. A., He Y. D., Dai H., Walker W. L., Hughes T. R., Tyers M., Boone C., Friend S. H.. Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles.  Science. (2000);  287 873-880
• 39 Romeis T., Piedras P., Zhang S., Klessig D. F., Hirt H., Jones J. D. G.. Rapid Avr-9 and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound and salicylate responses.  Plant Cell. (1999);  11 273-287
• 40 Samuel M. A., Miles G. P., Ellis B. E.. Ozone treatment rapidly activates MAP kinase signaling in plants.  The Plant Journal. (2000);  22 367-376
• 41 Schaeffer H. J., Weber M. J.. Mitogen-activated protein kinases: specific messages from ubiquitous messengers.  Molecular and Cellular Biology. (1999);  19 2435-2444
• 42 Schoenbeck M. A., Samac D. A., Fedorova M., Gregerson R. G., Gantt J. S., Vance C. P.. The alfalfa (Medicago sativa) TDY1 gene encodes a mitogen-activated protein kinase homolog.  Molecular Plant-Microbe Interaction. (1999);  12 882-893
• 43 Segar R., Krebs E. G.. The MAP kinase signaling cascade.  FASEB Journal. (1995);  9 726-735
• 44 Seo S., Okamoto M., Seto H., Ishizuka K., Sano H., Ohashi Y.. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways.  Science. (1995);  270 1988-1992
• 45 Song F., Goodman R. M.. OsBIMK1, a rice MAP kinase gene involved in disease resistance responses.  Planta. (2002);  215 997-1005
• 46 Tena G., Asai T., Chiu W. L., Sheen J.. Plant mitogen-activated protein kinase signaling cascades.  Current Opinion in Plant Biology. (2001);  4 392-400
• 47 Wen J. Q., Oono K., Imai R.. Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice.  Plant Physiology. (2002);  129 1880-1891
• 48 Wu J., Rossomando A. J., Her J. H., Del V. R., Weber M. J., Sturgill T. W.. Autophosphorylation in vitro of recombinant 42-kilodalton mitogen-activated protein kinase on tyrosine.  Proceedings of the National Academy of Sciences of the USA. (1991);  88 9508-9512
• 49 Widmann C., Gibson S., Jarpe M. B., Johnson G. L.. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human.  Physiological Review. (1999);  79 143-180
• 50 Xing T., Ouellet T., Miki B. L.. Towards genomic and proteomic studies of protein phosphorylation in plant-pathogen interactions.  Trends in Plant Science. (2002);  7 224-230
• 51 Xing T., Malik K., Martin T., Miki B. L.. Activation of tomato PR and wound-related genes by a mutagenized tomato MAP kinase kinase through divergent pathways.  Plant Molecular Biology. (2001);  46 109-120
• 52 Xiong L. Z., Yang Y. N.. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase.  Plant Cell. (2003);  15 745-759
• 53 Yang K. Y., Liu Y., Zhang S.. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 741-746
• 54 Yeh C. M., Hsiao L. J., Huang H. J.. Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice.  Plant and Cell Physiology. (2004);  45 1306-1312
• 55 Yuasa T., Ichimura K., Mizoguchi T., Shinozaki K.. Oxidative stress activates ATMPK6, an Arabidopsis homologue of MAP kinase.  Plant and Cell Physiology. (2001);  42 1012-1016
• 56 Zhang S., Klessig D. F.. The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK.  Proceedings of the National Academy of Sciences of the USA. (1998);  95 7225-7230
• 57 Zhang S., Klessig D. F.. MAPK cascades in plant defense signaling.  Trends in Plant Science. (2001);  6 520-527
• 58 Zhang S., Liu Y.. Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco.  Plant Cell. (2001);  13 1877-1889
• 59 Zhang S., Du H., Klessig D. F.. Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp.  Plant Cell. (1998);  10 435-450

Editor: J. Cullimore