Wheat BAX inhibitor-1 contributes to wheat resistance to Puccinia striiformis

Journal of Experimental Botany

Volumn 63, Issue 12, 2012, Pages 4571-4584

  Wang, Xiaojie ^a   Tang, Chunlei ^a   Huang, Xueling ^a   Li, Fangfang ^a   Chen, Xianming ^b   Zhang, Gang ^a   Sun, Yanfei ^a   Han, Dejun ^a   Kang, Zhensheng ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Bax inhibitor1; Plant resistance; Plant pathogen interactions; Puccinia striiformis; VIGS; Wheat

Indexed keywords

VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BASIDIOMYCETES; CELL DEATH; DISEASE RESISTANCE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; PLANT; PLANT DISEASE; PLANT ROOT; PROTEIN TERTIARY STRUCTURE; SEEDLING; SEQUENCE ALIGNMENT; TOBACCO; TRANSGENE; WHEAT;

AMINO ACID SEQUENCE; BASIDIOMYCOTA; CELL DEATH; DISEASE RESISTANCE; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENOTYPE; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT COMPONENTS, AERIAL; PLANT DISEASES; PLANT PROTEINS; PLANT ROOTS; PROTEIN STRUCTURE, TERTIARY; SEEDLING; SEQUENCE ALIGNMENT; TOBACCO; TRANSGENES; TRITICUM;

ANIMALIA; NICOTIANA TABACUM; PUCCINIA STRIIFORMIS; PUCCINIA STRIIFORMIS F. SP. TRITICI; TRITICUM AESTIVUM;

EID: 84866637318     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers140     Document Type: Article

References (65)

1. Babaeizad V, Imani J, Kogel K-H, Eichmann R, Hückelhoven R. 2009. Over-expression of the cell death regulator BAX inhibitor-1 in barley confers reduced or enhanced susceptibility to distinct fungal pathogens. Theoretical and Applied Genetics 118, 455-463.
2. Baek D, Nam J, Koo YD, et al. 2004. Bax-induced cell death of Arabidopsis is meditated through reactive oxygen-dependent and independent processes. Plant Molecular Biology 56, 15-27.
3. Beers EP, McDowell JM. 2001. Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues. Current Opinion in Plant Biology 4, 561-567.
4. Bolduc N, Ouellet M, Pitre F, Brisson LF. 2003. Molecular characterization of two plant BI-1 homologues which suppress Baxinduced apoptosis in human 293 cells. Planta 216, 377-386.
5. Dangl JL, Dietrich RA, Richberg MH. 1996. Death don't have no mercy: cell death programs in plant-microbe interactions. The Plant Cell 8, 1793-1807.
6. Delledonne M, Xia Y, Dixon RA, Lamb C. 1998. Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585-588.
7. Delledonne M, Zeier J, Marocco A, Lamb C. 2001. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences, USA 98, 13454-13459.
8. Dickman MB, Park YK, Oltersdorf T, Clemente T, French R. 2001. Abrogation of disease development in plants expressing animal antiapoptotic genes. Proceedings of the National Academy of Sciences, USA 98, 6957-6962.
9. Dou DL, Kale SD, Wang XL, et al. 2008. Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. The Plant Cell 20, 1118-1133.
10. Duan YF, Zhang WS, Li B, Wang YN, Li KX, Sodmergen, Han CY, Zhang YZ, Li X. 2010. An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytologist 186, 681-695.
11. Eichmann R, Bischof M, Weis C, Shaw J, Lacomme C, Schweizer P, Duchkov D, Hensel G, Kumlehn J, Hückelhoven R. 2010. BAX INHIBITOR-1 is required for full susceptibility of barley to powdery mildew. Molecular Plant-Microbe Interactions 23, 1217-1227.
12. Eichmann R, Dechert C, Kogel K-H, Hückelhoven R. 2006. Transient over-expression of barley BAX inhibitor-1 weakens oxidative defence and MLA12-mediated resistance to Blumeria graminis f.sp. hordei. Molecular Plant Pathology 7, 543-552.
13. Eichmann R, Holger S, Kogel K-H, Hückelhoven R. 2004. The barley apoptosis suppressor homologue Bax inhibitor-1 compromises nonhost penetration resistance of barley to the inappropriate pathogen Blumeria graminis f. sp. tritici. Molecular Plant-Microbe Interactions 17, 484-490.
14. Fadeel B, Zhivotovsky B, Orrenius S. 1999. All along the watchtower: on the regulation of apoptosis regulators. The FASEB Journal 13, 1647-1657.
15. Flor HH. 1955. Host-parasite interaction in flax rust: its genetics and other implications. Phytopathology 45, 680-685.
16. Gilchrist DG. 1998. Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annual Review of Phytopathology 36, 393-414.
17. Hammond-Kosack KE, Jones JD. 1996. Resistance genedependent plant defense responses. The Plant Cell 8, 1773-1791.
18. Hannun YA, Obeid LM. 2002. The ceramide-centric universe of lipidmediated cell regulation: stress encounters of the lipid kind. Journal of Biological Chemistry 277, 25847-25850.
19. Heath MC. 2000. Hypersensitive response-related death. Plant Molecular Biology, 44, 321-344.
20. Hein I, Barciszewska-Pacak M, Hrubikova K, Williamson S, Dinesen M, Soenderby IE, Sundar S, Jarmolowski A, Shirasu K, Lacomme C. 2005. Virus-induced gene silencing based functional characterization of genes associated with powdery mildew resistance in barley. Plant Physiology 38, 2155-2164.
21. Hengartner M, Horvitz HR. 1994. C. elegans cell survival gene ced-9 encodes a functional homologue of the mammalian protooncogene bcl-2. Cell 76, 665-676.
22. Hoeberichts FA, Woltering EJ. 2003. Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. BioEssays 25, 47-57.
23. Hoefle C, Loehrer M, Schaffrath U, Frank M, Schultheiss H, Hückelhoven R. 2009. Transgenic suppression of cell death limits penetration success of the soybean rust fungus Phakopsora pachyrhizi into epidermal cells of barley. Phytopathology 99, 220-226.
24. Holzberg S, Brosio P, Gross C, Pogue GP. 2002. Barley stripe mosaic virus-induced gene silencing in a monocot plant. The Plant Journal 30, 315-327.
25. Hückelhoven R. 2004. BAX inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis 9, 299-307.
26. Hückelhoven R, Dechert C, Kogel KH. 2003. Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis. Proceedings of the National Academy of Sciences, USA 100, 5555-5560.
27. Hückelhoven R, Dechert C, Trujillo M, Kogel KH. 2001. Differential expression of putative cell death regulator genes in nearisogenic, resistant and susceptible barley lines during interaction with the powdery mildew fungus. Plant Molecular Biology 47, 739-748.
28. Isbat M, Zebab N, Kima SR, Hong CB. 2009. A BAX inhibitor- 1gene in Capsicum annuum is induced under various abiotic stresses and endows multi-tolerance in transgenic tobacco. Journal of Plant Physiology 166, 1685-1693.
29. Kang ZS, Li ZQ. 1984. Discovery of a normal T. type new pathogenic strain to Lovrin10. Acta Cllegii Septentrionali Occidentali Agriculturae 4, 18-28 (in Chinese).
30. Kawai M, Pan L, Reed JC, Uchimiya H. 1999. Evolutionally conserved plant homologue of the Bax inhibitor-1 (BI-1) gene capable of suppressing Bax-induced cell death in yeast. FEBS Letters 464, 143-147.
31. Kawai-Yamada M, Hori Z, Ogawa T, Ihara-Ohori Y, Tamura K, Nagano M, Ishikawa T, Uchimiya H. 2009. Loss of calmodulin binding to Bax inhibitor-1 affects pseudomonas-mediated hypersensitive response-associated cell death in Arabidopsis thaliana. Journal of Biological Chemistry 284, 27998-28003.
32. Kawai-Yamada M, Jin U, Yoshinaga K, Hirata A, Uchimiya H. 2001. Mammalian Bax-induced plant cell death can be downregulated by overexpression of Arabidopsis Bax inhibitor-1 (AtBI- 1). Proceedings of the National Academy of Sciences, USA 98, 12295-12300.
33. Kawai-Yamada M, Ohmori Y, Uchimiya H. 2004. Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. The Plant Cell 16, 21-32.
34. Kroemer G. 1997. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Medicine 3, 614-620.
35. Lacomme C, Santa CS. 1999. Bax-induced cell death in tobacco is similar to the hypersensitive response. Proceedings of the National Academy of Sciences, USA 96, 7956-7961.
36. Lam E, Kato N, Lawton M. 2001. Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411, 848-853.
37. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251-275.
38. Liang H, Yao N, Song JT, Luo S, Lu H, Greenberg JT. 2003. Ceramides modulate programmed cell death in plants. Genes and Development 17, 2636-2641.
39. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408.
40. Madeo F, Frohlich E, Ligr M, Grey M, Sigrist SJ, Wolf DH, Frohlich KU. 1999. Oxygen stress: a regulator of apoptosis in yeast. Journal of Cell Biology 145, 757-767.
41. Madeo F, Herker E, Wissing S, Jungwirth H, Eisenberg T, Frohlich KU. 2004. Apoptosis in yeast. Current Opinion in Microbiology 7, 655-660.
42. Matsumura H, Nirasawa S, Kiba A, Urasaki N, Saitoh H, Ito M, Kawai-Yamada M, Uchimiya H, Terauchi R. 2003. Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L.) cells. The Plant Journal 33, 425-434.
43. Mitsuhara I, Malik KA, Miura M, Ohashi Y. 1999. Animal cell-death suppressors Bcl-XL and Ced-9 inhibit cell death in tobacco cells. Current Biology 9, 775-778.
44. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405-410.
45. Nei M, Kumar S. 2000. Molecular evolution and phylogenetics. New York: Oxford University Press
46. Parlevliet JE, Kievit C. 1986. Development of barley leaf rust, Puccinia hordei infections in barley. I. Effect of partial resistance and plant stage. Euphytica 35, 953-959.
47. Pogue GP, Lindbo JA, Dawson WO, Turpen TH. 1998. Tobamovirus transient expression vectors: tools for plant biology and high-level expression of foreign proteins in plants. In: SB Gelvin, RA Schilperoot, eds, Plant molecular biology manual. Dordrecht: Kluwer Academic, pp 1-27.
48. Qutob D, Kamoun S, Gijzen M. 2002. Expression of a Phytophthora sojae necrosis inducing protein occurs during transition from biotrophy to necrotrophy. The Plant Journal 32, 361-373.
49. Richberg MH, Aviv DH, Dangl JL. 1998. Dead cells to tell tales. Current Opinion of Plant Biology 1, 480-485.
50. Ryerson DE, Heath MC. 1996. Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. The Plant Cell 8, 393-402.
51. Sanchez P, de Torres Zebala M, Grant M. 2000. AtBI-1, a plant homologue of Bax inhibitor-1, suppresses Bax-induced cell death in yeast and is rapidly upregulated during wounding and pathogen challenge. The Plant Journal 21, 393-399.
52. Scofield SR, Huang L, Brandt AS, Gill BS. 2005. Development of a virus-induced gene silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiology 138, 2165-2173.
53. Stakman EC. 1915. Relation between Puccinia graminis and plants highly resistant to its attack. Journal of Agricultural Research 4, 193-201.
54. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 11, 4673-4680.
55. Van Loon LC. 1997. Induced resistance in plants and the role of pathogenesis-related proteins. European Journal of Plant Pathology 103, 753-765.
56. Van Loon LC, Van Strien EA. 1999. The families of pathogenesisrelated proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology 55, 85-97.
57. Wang CF, Huang LL, Buchenauer H, Han QM, Zhang HC, Kang ZS. 2007. Histochemical studies on the accumulation of reactive oxygen species (O2- and H2O2) in the incompatible and compatible interaction of wheat-Puccinia striiformis f. sp. tritici. Physiological and Molecular Plant Pathology 71, 230-239.
58. Wang XJ, Liu W, Chen XM, et al. 2010. Differential gene expression in incompatible interaction between wheat and stripe rust fungus revealed by the cDNA-AFLP and comparison to compatible interaction. BMC Plant Biology 10, 9.
59. Wang XJ, Tang CL, Zhang HC, Xu JR, Liu B, LV J, Han DJ, Huang LL, Kang ZS. 2011. TaDAD2, a negative regulator of programmed cell death, is important for the interaction between wheat and the stripe rust fungus. Molecular Plant-Microbe Interactions 24, 79-90.
60. Wang XJ, Tang CL, Zhang G, et al. 2009. cDNA-AFLP analysis reveals differential gene expression in compatible interaction of wheat challenged with Puccinia striiformis f. sp. tritici. BMC Genomics 10, 289.
61. Xu P, Rogers SJ, Roossinck MJ. 2004. Expression of antiapoptotic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress. Proceedings of the National Academy of Sciences, USA 101, 15805-15810.
62. Xu Q, Reed JC. 1998. Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Molecular Cell 1, 337-346.
63. Yoshinaga K, Arimura S-I, Hirata A, Niwa Y, Yun D-J, Tsutsumi N, Uchimiya H, Kawai-Yamada M. 2005. Mammalian Bax initiates plant cell death through organelle destruction. Plant Cell Reports 24, 408-417.
64. Yu LH, Kawai-Yamada M, Naito M, Watanabe K, Reed JC, Uchimiya H. 2002. Induction of mammalian cell death by a plant Bax inhibitor. FEBS Letters 512, 308-312.
65. Yuan JY, Shaham S, Ledoux S, Ellis HM, Horvitz R. 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 converting enzyme. Cell 75, 641-652.