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Over-expression of the cell death regulator BAX inhibitor-1 in barley confers reduced or enhanced susceptibility to distinct fungal pathogens

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Abstract

BAX inhibitor-1 (BI-1) is a conserved cell death regulator protein that inhibits mammalian BAX-induced cell death in yeast, animals and plants. Additionally, HvBI-1 suppresses defense responses and resistance to the powdery mildew fungus Blumeria graminis f.sp. hordei (Bgh) when over-expressed in single epidermal cells of barley. To test the potential of ectopic expression of BI-1 to influence fungal interactions with crop plants, we produced stable transgenic barley plants expressing a green fluorescing protein (GFP) fusion of HvBI-1 under control of the cauliflower mosaic virus 35S promoter. GFP-HvBI-1 plants were fertile and did not display obvious developmental alterations when compared to wild type parents. GFP-HvBI-1 plants were more resistant to single cell death induced by ballistic delivery of a mammalian proapototic BAX expression construct and more susceptible to biotrophic Bgh. Microscopic observation of the interaction phenotype revealed that enhanced susceptibility, i.e. a higher degree of successful establishment of haustoria in epidermal cells, was associated with a reduced frequency of hypersensitive cell death reactions. In contrast, young seedlings of GFP-HvBI-1 barley were more resistant to Fusarium graminearum than wild type or azygous controls. Hence the effect of GFP-HvBI-1 on the outcome of a particular plant–fungus interaction appeared dependent on the lifestyle of the pathogen.

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References

  • Bai Y, Pavan S, Zheng Z, Zappel NF, Reinstädler A, Lotti C, De Giovanni C, Ricciardi L, Lindhout P, Visser R, Theres K, Panstruga R (2008) Naturally occurring broad-spectrum powdery mildew resistance in a Central American tomato accession is caused by loss of mlo function. Mol Plant Microbe Interact 21:30–39

    Article  PubMed  CAS  Google Scholar 

  • Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705

    Article  PubMed  Google Scholar 

  • Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, Westphal L, Vogel J, Lipka V, Kemmerling B, Schulze-Lefert P, Somerville SC, Panstruga R (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38:716–720

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Dietrich RA, Richberg MH (1996) Death don′t have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8:1793–1807

    Article  PubMed  CAS  Google Scholar 

  • Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiss M, Waller F, 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

    Article  PubMed  CAS  Google Scholar 

  • Deshmukh SD, Kogel K-H (2007) Piriformospora indica protects barley from Fusarium root rot. J Plant Dis Prot 114:263–268

    Google Scholar 

  • 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. Mol Plant Pathol 7:543–552

    Article  CAS  Google Scholar 

  • Eichmann R, Schultheiss H, 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. Mol Plant-Microbe Interact 17:484–490

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Goswami RS, Kistler HC (2004) Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 5:515–525

    Article  CAS  Google Scholar 

  • Hückelhoven R (2004) BAX Inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis 9:299–307

    Article  PubMed  Google Scholar 

  • Hückelhoven R, Dechert C, Kogel K-H (2003) Over-expression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis. Proc Natl Acad Sci USA 100:5555–5560

    Article  PubMed  Google Scholar 

  • Hückelhoven R, Dechert C, Trujillo M, Kogel K-H (2001) Differential expression of putative cell death regulator genes in near-isogenic, resistant and susceptible barley lines inoculated with the powdery mildew fungus. Plant Mol Biol 47:739–748

    Article  PubMed  Google Scholar 

  • Hückelhoven R, Fodor J, Preis C, Kogel K-H (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with H2O2 but not with salicylic acid accumulation. Plant Physiol 119:1251–1260

    Article  PubMed  Google Scholar 

  • Hückelhoven R, 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

    Article  Google Scholar 

  • Ihara-Ohori Y, Nagano M, Muto S, Uchimiya H, Kawai-Yamada M (2007) Cell death suppressor Arabidopsis Bax Inhibitor-1 is associated with calmodulin binding and ion homeostasis. Plant Physiol 143:650–660

    Article  PubMed  CAS  Google Scholar 

  • Imani J, Baltruschat H, Stein E, Jia G, Vogelsberg J, Kogel K-H, Hückelhoven R (2006) Expression of barley BAX Inhibitor-1 in carrots confers resistance to Botrytis cinerea. Mol Plant Pathol 7:279–284

    Article  CAS  Google Scholar 

  • Jansen C, von Wettstein D, Schafer W, Kogel K-H, Felk A, Maier FJ (2005) Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc Natl Acad Sci USA 102:16892–16897

    Article  PubMed  CAS  Google Scholar 

  • Jarosch B, Kogel K-H, Schaffrath U (1999) The ambivalence of the barley Mlo locus: Mutations conferring resistance against powdery mildew (Blumeria graminis f.sp. hordei) enhance susceptibility to the rice blast fungus Magnaporte grisea. Mol Plant-Microbe Interact 12:508–514

    Article  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Jørgensen JH (1992) Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63:141–152

    Article  Google Scholar 

  • Kawai-Yamada M, Jin L, Yoshinaga K, Hirata A, Uchimiya H (2001) Mammalian Bax-induced plant cell death can be down-regulated by over-expression of Arabidopsis Bax Inhibitor-1 (AtBI-1). Proc Natl Acad Sci USA 98:12295–12300

    Article  PubMed  CAS  Google Scholar 

  • Kawai-Yamada M, Ohori Y, Uchimiya H (2004) Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell 16:21–32

    Article  PubMed  CAS  Google Scholar 

  • Koga H, Bushnell WR, Zeyen RJ (1990) Specificity of cell type and timing of events associated with papilla formation and the hypersensitive reaction in leaves of Hordeum vulgare attacked by Erysiphe graminis fsp hordei. Can J Bot 68:2344–2352

    Google Scholar 

  • Kumar J, Hückelhoven R, Beckhove U, Nagarajan S, Kogel K-H (2001) A compromised Mlo pathway affects the response of barley to the necrotrophic fungus Bipolaris sorokiniana (teleomorph: Cochliobolus sativus) and its toxins. Phytopathology 91:127–133

    Article  PubMed  CAS  Google Scholar 

  • Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848–853

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \( {\text{2}}^{{-\Updelta\Updelta} C_{\rm{T}}}\) Method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • McCallum BD, Tekauz A (2002) Influence of inoculation method and growth stage on fusarium head blight in barley. Can J Plant Pathol 24:77–80

    Google Scholar 

  • Nicholson P, Simpson DR, Weston G, Rezanoor HN, Lees AK, Parry DW, Joyce D (1998) Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereals using PCR assays. Physiol Mol Plant Pathol 53:17–37

    Article  CAS  Google Scholar 

  • Nirenberg HI (1981) A simplified method for identifying Fusarium spp. occuring on wheat. Can J Bot 59:1599–1609

    Google Scholar 

  • Peterhänsel C, Freialdenhoven A, Kurth J, Kolsch R, Schulze-Lefert P (1997) Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. Plant Cell 9:1397–1409

    Article  PubMed  Google Scholar 

  • Schultheiss H, Hensel G, Imani J, Broeders S, Kumlehn J, Kogel K-H, Sonnewald U, Hückelhoven R (2005) Ectopic expression of constitutively activated RACB in barley enhances susceptibility to powdery mildew and abiotic stress. Plant Physiol 139:353–362

    Article  PubMed  CAS  Google Scholar 

  • Schweizer P, Pokorny J, Abderhalden O, Dudler R (1999) A transient assay system for the functional assessment of defense-related genes in wheat. Mol Plant Microbe Interact 12:647–654

    Article  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Watanabe N, Lam E (2006) Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death. Plant J 45:884–894

    Article  PubMed  CAS  Google Scholar 

  • Watanabe N, Lam E (2008) BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis. J Biol Chem 283:3200–3210

    Article  PubMed  CAS  Google Scholar 

  • Xu Q, Reed JC (1998) Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol Cell 1:337–346

    Article  PubMed  CAS  Google Scholar 

  • Zierold U, Scholz U, Schweizer P (2005) Transcriptome analysis of mlo-mediated resistance in the epidermis of barley. Mol Plant Pathol 6:139–151

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Ministry of Science, Research and Technology of Iran for the Ph.D. scholarship of V.B. (Home address: University of Agricultural and Natural Recourses, College of Agriculture, Department of Plant Protection, Sari, Iran).

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Correspondence to Ralph Hückelhoven.

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Communicated by A. Graner.

V. Babaeizad and J. Imani contributed equally to this study.

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Babaeizad, V., Imani, J., Kogel, KH. et al. 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 (2009). https://doi.org/10.1007/s00122-008-0912-2

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  • DOI: https://doi.org/10.1007/s00122-008-0912-2

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