Co-immunoprecipitation-based identification of putative BAX INHIBITOR-1-interacting proteins involved in cell death regulation and plant-powdery mildew interactions

Molecular Plant Pathology

Volumn 14, Issue 8, 2013, Pages 791-802

  Weis, Corina ^a   Pfeilmeier, Sebastian ^a   Glawischnig, Erich ^a   Isono, Erika ^a   Pachl, Fiona ^a   Hahne, Hannes ^a   Kuster, Bernhard ^a   Eichmann, Ruth ^a,b   Hückelhoven, Ralph ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNARIA ALTERNATA; ANIMALIA; ARABIDOPSIS; ERYSIPHALES; ERYSIPHE CRUCIFERARUM; FUNGI;

ARABIDOPSIS PROTEIN; ATBI 1 PROTEIN, ARABIDOPSIS; ATBI-1 PROTEIN, ARABIDOPSIS; CYP83A1 PROTEIN, ARABIDOPSIS; CYTOCHROME P450; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MEMBRANE PROTEIN; PEPTIDE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; ASCOMYCETES; CELL DEATH; CHEMISTRY; CYTOLOGY; ENDOPLASMIC RETICULUM; HOST PATHOGEN INTERACTION; IMMUNOPRECIPITATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN BINDING; STAINING;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; CELL DEATH; CYTOCHROME P-450 ENZYME SYSTEM; ENDOPLASMIC RETICULUM; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; STAINING AND LABELING;

EID: 84883447011     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12050     Document Type: Article

References (85)

1. Adas, F., Salaün, J.P., Berthou, F., Picart, D., Simon, B. and Amet, Y. (1999) Requirement for omega and (omega;-1)-hydroxylations of fatty acids by human cytochromes P450 2E1 and 4A11. J. Lipid Res. 40, 1990-1997.
2. Ahn, C.S., Lee, J.H., Reum Hwang, A., Kim, W.T. and Pai, H.S. (2006) Prohibitin is involved in mitochondrial biogenesis in plants. Plant J. 46, 658-667.
3. Babaeizad, V., Imani, J., Kogel, K.H., Eichmann, R. and Hückelhoven, R. (2009) Over-expression of the cell death regulator BAX inhibitor-1 in barley confers reduced or enhanced susceptibility to distinct fungal pathogens. Theor. Appl. Genet. 118, 455-463.
4. Bak, S. and Feyereisen, R. (2001) The involvement of two P450 enzymes, CYP83B1 and CYP83A1, in auxin homeostasis and glucosinolate biosynthesis. Plant Physiol. 127, 108-118.
5. Bak, S., Beisson, F., Bishop, G., Hamberger, B., Höfer, R., Paquette, S. and Werck-Reichhart, D. (2011) Cytochromes P450. Arabidopsis Book, 9, e0144.
6. Bilodeau, P., Udvardi, M.K., Peacock, W.J. and Dennis, E.S. (1999) A prolonged cold treatment-induced cytochrome P450 gene from Arabidopsis thaliana. Plant Cell Environ. 22, 791-800.
7. Bolduc, N., Ouellet, M., Pitre, F. and Brisson, L.F. (2003) Molecular characterization of two plant BI-1 homologues which suppress Bax-induced apoptosis in human 293 cells. Planta, 216, 377-386.
8. Carrara, G., Saraiva, N., Johnson, B.F., Gubser, C. and Smith, G.L. (2012) A six transmembrane topology for Golgi Anti-Apoptotic Protein (GAAP) and Bax Inhibitor 1 (BI-1) provides a model for the Transmembrane Bax Inhibitor Containing Motif (TMBIM) family. J. Biol. Chem. 287, 15896-15905.
9. Chen, J.C., Jiang, C.Z. and Reid, M.S. (2005) Silencing a prohibitin alters plant development and senescence. Plant J. 44, 16-24.
10. Chen, S., Glawischnig, E., Jørgensen, K., Naur, P., Jørgensen, B., Olsen, C.E., Hansen, C.H., Rasmussen, H., Pickett, J.A. and Halkier, B.A. (2003) CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J. 33, 923-937.
11. Christians, M.J. and Larsen, P.B. (2007) Mutational loss of the prohibitin AtPHB3 results in an extreme constitutive ethylene response phenotype coupled with partial loss of ethylene-inducible gene expression in Arabidopsis seedlings. J. Exp. Bot. 58, 2237-2248.
12. Cowling, R.T. and Birnboim, H.C. (1998) Preliminary characterization of the protein encoded by human testis-enhanced gene transcript (TEGT). Mol. Membr. Biol. 15, 177-187.
13. De Brito, O.M. and Scorrano, L. (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature, 456, 605-610.
14. Deshmukh, S., Hückelhoven, R., Schäfer, P., Imani, J., Sharma, M., Weiss, M., Waller, F. and Kogel, K.H. (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc. Natl. Acad. Sci. USA, 103, 18450-18457.
15. Dettmer, J., Schubert, D., Calvo-Weimar, O., Stierhof, Y.D., Schmidt, R. and Schumacher, K. (2005) Essential role of the V-ATPase in male gametophyte development. Plant J. 41, 117-124.
16. +-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell, 18, 715-730.
17. Di, C., Xu, W., Su, Z. and Yuan, J.S. (2010) Comparative genome analysis of PHB gene family reveals deep evolutionary origins and diverse gene function. BMC Bioinformatics, 11, S22.
18. Dietz, K.J., Tavakoli, N., Kluge, C., Mimura, T., Sharma, S.S., Harris, G.C., Chardonnens, A.N. and Golldack, D. (2001) Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J. Exp. Bot. 52, 1969-1980.
19. Eichmann, R. and Schäfer, P. (2012) The endoplasmic reticulum in plant immunity and cell death. Front. Plant Sci. 3, 200. doi: 10.3389/fpls.2012.00200.
20. Eichmann, R., Dechert, C., Kogel, K.-H. and Hückelhoven, R. (2006) Transient over-expression of barley BAX Inhibitor-1 weakens oxidative defence and MLA12-mediated resistance to Blumeria graminis f.sp. hordei. Mol. Plant Pathol. 7, 543-552.
21. Eichmann, R., Bischof, M., Weis, C., Shaw, J., Lacomme, C., Schweizer, P., Duchkov, D., Hensel, G., Kumlehn, J. and Hückelhoven, R. (2010) BAX INHIBITOR-1 is required for full susceptibility of barley to powdery mildew. Mol. Plant-Microbe Interact. 23, 1217-1227.
22. Finer, J.J., Vain, P., Jones, M.W. and McMullen, M.D. (1992) Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Rep. 11, 323-328.
23. Finni, C., Andersen, C.H., Borch, J., Gjetting, S., Christensen, A.B., de Boer, A.H., Thordal-Christensen, H. and Collinge, D.B. (2002) Do 14-3-3 proteins and plasma membrane H+-AtPases interact in the barley epidermis in response to the barley powdery mildew fungus? Plant Mol. Biol. 49, 137-147.
24. Haseloff, J., Siemering, K.R., Prasher, D.C. and Hodge, S. (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. USA, 94, 2122-2127.
25. Hemm, M.R., Ruegger, M.O. and Chapple, C. (2003) The Arabidopsis ref2 mutant is defective in the gene encoding CYP83A1 and shows both phenylpropanoid and glycosinolate phenotypes. Plant Cell, 15, 179-194.
26. Hemrajani, C., Berger, C.N., Robinson, K.S., Marchès, O., Mousnier, A. and Frankel, G. (2010) NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection. Proc. Natl. Acad. Sci. USA, 107, 3129-3134.
27. Höfle, C., Loehrer, M., Schaffrath, U., Frank, M., Schultheiss, H. and 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.
28. Hopkins, R.J., Van Dam, N.M. and Van Loon, J.J. (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54, 57-83.
29. Hoppins, S., Lackner, L. and Nunnari, J. (2007) The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76, 751-780.
30. Hückelhoven, R. (2004) BAX Inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis, 9, 299-307.
31. Hückelhoven, R. and Kogel, K.-H. (1998) Tissue-specific superoxide generation at interaction sites in resistant and susceptible near-isogenic barley lines attacked by the powdery mildew fungus (Erysiphe graminis f. sp. hordei). Mol. Plant-Microbe Interact. 11, 292-300.
32. Hückelhoven, R., Dechert, C. and Kogel, K.-H. (2003) Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis. Proc. Natl. Acad. Sci. USA, 100, 5555-5560.
33. Ihara-Ohori, Y., Nagano, M., Muto, S., Uchimiya, H. and Kawai-Yamada, M. (2007) Cell death suppressor Arabidopsis Bax Inhibitor-1 is associated with calmodulin binding and ion homeostasis. Plant Physiol. 143, 650-660.
34. Imani, J., Baltruschat, H., Stein, E., Jia, G., Vogelsberg, J., Kogel, K.H. and Hückelhoven, R. (2006) Expression of barley BAX Inhibitor-1 in carrots confers resistance to Botrytis cinerea. Mol. Plant Pathol. 7, 279-284.
35. Ishikawa, T., Watanabe, N., Nagano, M., Kawai-Yamada, M. and Lam, E. (2011) Bax inhibitor-1: a highly conserved endoplasmic reticulum-resident cell death suppressor. Cell Death Differ. 18, 1271-1278.
36. Iwasawa, R., Mahul-Mellier, A.L., Datler, C., Pazarentzos, E. and Grimm, S. (2011) Fis1 and Bap31 bridge the mitochondria-ER interface to establish a platform for apoptosis induction. EMBO J. 30, 556-568.
37. Johnson, M.A., von Besser, K., Zhou, Q., Smith, E., Aux, G., Patton, D., Levin, J.Z. and Preuss, D. (2004) Arabidopsis hapless mutations define essential gametophytic functions. Genetics, 168, 971-982.
38. Kang, J.S., Frank, J., Kang, C.H., Kajiura, H., Vikram, M., Ueda, A., Kim, S., Bahk, J.D., Triplett, B., Fujiyama, K., Lee, S.Y., von Schaewen, A. and Koiwa, H. (2008) Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proc. Natl. Acad. Sci. USA, 105, 5933-5938.
39. Kawai, M., Panb, L., Reed, J.C. and 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 Lett. 464, 143-147.
40. Kawai-Yamada, M., Jin, L., Yoshinaga, K., Hirata, A. and Uchimiya, H. (2001) Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax Inhibitor-1 (AtBI-1). Proc. Natl. Acad. Sci. USA, 98, 12295-12300.
41. Kawai-Yamada, M., Ohori, Y. and Uchimiya, H. (2004) Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell, 16, 21-32.
42. Kawai-Yamada, M., Hori, Z., Ogawa, T., Ihara-Ohori, Y., Tamura, K., Nagano, M., Ishikawa, T. and Uchimiya, H. (2009) Loss of calmodulin binding to Bax inhibitor-1 affects Pseudomonas-mediated hypersensitive response-associated cell death in Arabidopsis thaliana. J. Biol. Chem. 284, 27998-28003.
43. Keinath, N.F., Kierszniowska, S., Lorek, J., Bourdais, G., Kessler, S.A., Shimosato-Asano, H., Grossniklaus, U., Schulze, W.X., Robatzek, S. and Panstruga, R. (2010) PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J. Biol. Chem. 285, 39140-39149.
44. Kelleher, D.J. and Gilmore, R. (2006) An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology, 16, 47R-62R.
45. Kim, H.R., Lee, G.H., Cho, E.Y., Chae, S.W., Ahn, T. and Chae, H.J. (2009) Bax inhibitor 1 regulates ER-stress-induced ROS accumulation through the regulation of cytochrome P450 2E1. J. Cell Sci. 122, 1126-1133.
46. Kiviluoto, S., Schneider, L., Luyten, T., Vervliet, T., Missiaen, L., De Smedt, H., Parys, J.B., Methner, A. and Bultynck, G. (2012) Bax Inhibitor-1 is a novel IP3 receptor-interacting and -sensitizing protein. Cell Death Dis. 3, e367.
47. Knauer, R. and Lehle, L. (1999) The oligosaccharyltransferase complex from yeast. Biochim. Biophys. Acta, 1426, 259-273.
48. Koiwa, H., Li, F., McCully, M.G., Mendoza, I., Koizumi, N., Manabe, Y., Nakagawa, Y., Zhu, J., Rus, A., Pardo, J.M., Bressan, R.A. and Hasegawa, P.M. (2003) The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell, 15, 2273-2284.
49. Kornmann, B., Currie, E., Collins, S.R., Schuldiner, M., Nunnari, J., Weissman, J.S. and Walter, P. (2009) An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science, 325, 477-481.
50. Lee, G.H., Ahn, T., Kim, D.S., Park, S.J., Lee, Y.C., Yoo, W.H., Jung, S.J., Yang, J.S., Kim, S., Muhlrad, A., Seo, Y.R., Chae1, S.W., Kim, H.R. and Chae, H.J. (2010) Bax inhibitor 1 increases cell adhesion through actin polymerization: involvement of calcium and actin binding. Mol. Cell. Biol. 30, 1800-1813.
51. Lee, G.H., Kim, H.R. and Chae, H.J. (2012) Bax inhibitor-1 regulates the expression of P450 2E1 through enhanced lysosome activity. Int. J. Biochem. Cell Biol. 44, 600-611.
52. Liu, J.X. and Howell, S.H. (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell, 22, 2930-2942.
53. Merkle, T. (2003) Nucleo-cytoplasmic partitioning of proteins in plants: implications for the regulation of environmental and developmental signalling. Curr. Genet. 44, 231-260.
54. Mikkelsen, M.D., Petersen, B.L., Glawischnig, E., Jensen, A.B., Andreasson, E. and Halkier, B.A. (2003) Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiol. 131, 298-308.
55. Millar, A.H., Sweetlove, L.J., Giegé, P. and Leaver, C.J. (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol. 127, 1711-1727.
56. Nafisi, M., Sønderby, I.E., Hansen, B.G., Geu-Flores, F., Nour-Eldin, H.H., Nørholm, M.H.H., Jensen, N.B., Li, J. and Halkier, B. (2006) Cytochromes P450 in the biosynthesis of glucosinolates and indole alkaloids. Phytochem. Rev. 5, 331-346.
57. Nagano, M., Ihara-Ohori, Y., Imai, H., Inada, N., Fujimoto, M., Tsutsumi, N., Uchimiya, H. and Kawai-Yamada, M. (2009) Functional association of cell death suppressor, Arabidopsis Bax inhibitor-1, with fatty acid 2-hydroxylation through cytochrome b. Plant J. 58, 122-134.
58. Nagano, M., Takahara, K., Fujimoto, M., Tsutsumi, N., Uchimiya, H. and Kawai-Yamada, M. (2012) Arabidopsis sphingolipid fatty acid 2-hydroxylases (AtFAH1 and AtFAH2) are functionally differentiated in fatty acid 2-hydroxylation and stress responses. Plant Physiol. 159, 1138-1148.
59. Naur, P., Petersen, B.L., Mikkelsen, M.D., Bak, S., Rasmussen, H., Olsen, C.E. and Halkier, B.A. (2003) CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol. 133, 63-72.
60. Nelson, B.K., Cai, X. and Nebenfuhr, A. (2007) A multicolored set of invivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136.
61. Nijtmans, L.G., de Jong, L., Artal Sanz, M., Coates, P.J., Berden, J.A., Back, J.W., Muijsers, A.O., Van der Spek, H. and Grivell, L. (2000) Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J. 19, 2444-2451.
62. Opalski, K.S., Schultheiss, H., Kogel, K.-H. and Hückelhoven, R. (2005) The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f.sp. hordei. Plant J. 41, 291-303.
63. Pröls, R. and Roitsch, T. (2009) Extracellular invertase LIN6 of tomato: a pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm. J. Exp. Bot. 60, 1555-1567.
64. Reintanz, B., Lehnen, M., Reichelt, M., Gershenzon, J., Kowalczyk, M., Sandberg, G., Godde, M., Uhl, R. and Palme, K. (2001) Bus, a Bushy Arabidopsis cyp79f1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell, 13, 351-367.
65. Reitz, M.U., Bissue, J.K., Zocher, K., Attard, A., Hückelhoven, R., Becker, K., Imani, J., Eichmann, R. and Schäfer, P. (2012) The subcellular localization of tubby-like proteins and participation in stress signaling and root colonization by the mutualist Piriformospora indica. Plant Physiol. 160, 349-364.
66. Reuber, T.L., Plotnikova, J.M., Dewdney, J., Rogers, E.E., Wood, W. and Ausubel, F.M. (1998) Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16, 473-485.
67. Robinson, K.S., Clements, A., Williams, A.C., Berger, C.N. and Frankel, G. (2011) Bax inhibitor 1 in apoptosis and disease. Oncogene, 30, 2391-2400.
68. Rothbauer, U., Zolghadr, K., Muyldermans, S., Schepers, A., Cardoso, C.M. and Leonhardt, H. (2008) A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Mol. Cell. Proteomics, 7, 282-289.
69. Ruegger, M. and Chapple, C. (2001) Mutations that reduce sinapoylmalate accumulation in Arabidopsis thaliana define loci with diverse roles in phenylpropanoid metabolism. Genetics, 159, 1741-1749.
70. Saijo, Y. (2010) ER quality control of immune receptors and regulators in plants. Cell. Microbiol. 12, 716-724.
71. Sanchez, P., De Torres Zabala, M. and 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. Plant J. 21, 393-399.
72. Schuler, M.A. and Werck-Reichhart, D. (2003) Functional genomics of P450s. Annu. Rev. Plant Biol. 54, 629-667.
73. Schweizer, P., Pokorny, J., Abderhalden, O. and Dudler, R. (1999) A transient assay system for the functional assessment of defense-related genes in wheat. Mol. Plant-Microbe Interact. 12, 647-654.
74. Siemering, K.R., Golbik, R., Sever, R. and Haseloff, J. (1996) Mutations that suppress the thermosensitivity of green fluorescent protein. Curr. Biol. 6, 1653-1663.
75. Siminszky, B., Corbin, F.T., Ward, E.R., Fleischmann, T.J. and Dewey, R.E. (1999) Expression of a soybean cytochrome P450 monooxygenase cDNA in yeast and tobacco enhances the metabolism of phenylurea herbicides. Proc. Natl. Acad. Sci. USA, 96, 1750-1755.
76. Van Aken, O., Pecenkova, T., Van De Cotte, B., De Rycke, R., Eeckhout, D., Fromm, H., De Jaeger, G., Witters, E., Beemster, G.B., Inze, D. and Van Breusegem, F. (2007) Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development. Plant J. 5, 850-864.
77. Van Aken, O., Whelan, J. and Van Breusegem, F. (2010) Prohibitins: mitochondrial partners in development and stress response. Trends Plant Sci. 15, 275-282.
78. Walter, L., Dirks, B., Rothermel, E., Heyens, M., Szpirer, C., Levan, G. and Gunther, E. (1994) A novel, conserved gene of the rat that is developmentally regulated in the testis. Mamm. Genome, 5, 216-221.
79. Watanabe, N. and Lam, E. (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J. 45, 884-894.
80. Watanabe, N. and Lam, E. (2008) BAX INHIBITOR-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis. J. Biol. Chem. 283, 3200-3210.
81. Wiermer, M., Palma, K., Zhang, Y. and Li, X. (2007) Should I stay or should I go? Nucleocytoplasmic trafficking in plant innate immunity. Cell. Microbiol. 9, 1880-1890.
82. Xu, Q. and Reed, J.C. (1998) Bax Inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol. Cell, 1, 337-346.
83. Yang, Y., Li, R. and Qi, M. (2000) Invivo analysis of plant promoters and transcription factors by agro infiltration of tobacco leaves. Plant J. 22, 543-551.
84. Yoshinaga, K., Arimura, S., Hirata, A., Niwa, Y., Yun, D.J., Tsutsumi, N., Uchimiya, H. and Kawai-Yamada, M. (2005) Mammalian Bax initiates plant cell death through organelle destruction. Plant Cell Rep. 24, 408-417.
85. Zhou, F., Andersen, C.H., Burhenne, K., Fischer, P.H., Collinge, D.B. and Thordal-Christensen, H. (2000) Proton extrusion is an essential signalling component in the HR of epidermal single cells in the barley-powdery mildew interaction. Plant J. 23, 245-254.