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Meta-analysis of transcripts associated with race-specific resistance to stripe rust in wheat demonstrates common induction of blue copper-binding protein, heat-stress transcription factor, pathogen-induced WIR1A protein, and ent-kaurene synthase transcripts

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Abstract

Resistance to stripe rust in wheat is a preferred method of disease prevention. Race-specific all-stage resistance usually provides complete protection; thus an understanding of the molecular control of race-specific resistance is important. To build on previous studies of race-specific resistance controlled by the Yr5 gene, this study reports the construction and use of a custom oligonucleotide microarray to perform a meta-analysis of the transcriptional response involved in race-specific resistance conferred by Yr1, Yr5, Yr7, Yr8, Yr9, Yr10, Yr15, and Yr17. By profiling the response of eight resistance genes in a common background, we identified 28 transcripts significantly involved in the resistance phenotype across all genotypes. The most significant of these were annotated as blue copper-binding protein, heat-stress transcription factor, pathogen-induced WIR1A protein, and ent-kaurene synthase transcripts. Unique transcripts significant in each genotype were also identified, which highlighted some transcriptional events specific to certain genotypes. The approach was effective in narrowing down the list of candidate genes in comparison to studying individual genotypes. Annotation revealed key gene expression events involved in race-specific resistance. The results confirm the activity of known R-gene-mediated pathway race-specific resistance, including an oxidative burst that likely contributes to a hypersensitive response, as well as pathogenesis-related protein expression and activity of the phenylpropanoid pathway. However, several identified transcripts remained unknown and may prove interesting candidates for further characterization.

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References

  • Barrett T, Suzek TO, Troup DB, Wilhite SE, Ngau WC, Ledoux P, Rudnev D, Lash AE, Fujibuchi W, Edgar R (2005) NCBI GEO: mining millions of expression profiles—database and tools. Nucleic Acids Res 33:D562–D566

    Article  CAS  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300

    Google Scholar 

  • Bethke PC, Fath A, Spiegel YN, Hwang YS, Jones RL (2002) Abscisic acid, gibberellin and cell viability in cereal aleurone. Euphytica 126:3–11

    Article  CAS  Google Scholar 

  • Bindschedler L, Dewdney J, Blee K, Stone J, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies D, Ausubel F, Bolwell G (2006) Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J 47:851–863

    Article  CAS  PubMed  Google Scholar 

  • Boddu J, Cho S, Kruger W, Muehlbauer G (2006) Transcriptome analysis of the barley–Fusarium graminearum interaction. Mol Plant-Microbe Interact 19:407–417

    Article  CAS  PubMed  Google Scholar 

  • Boddu J, Cho S, Muehlbauer G (2007) Transcriptome analysis of trichothecene-induced gene expression in barley. Mol Plant–Microbe Interact 20:1364–1375

    Article  CAS  PubMed  Google Scholar 

  • Bouche N, Yellin A, Snedden W, Fromm H (2005) Plant-specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435–466

    Article  CAS  PubMed  Google Scholar 

  • Buckley M (2002) The spot user’s guide. CSIRO Mathematical and Information Sciences. http://www.cmis.csiro.au/IAP/Spot/spotmanual.htm

  • Bull J, Mauch F, Hertig C, Rebmann G, Dudler R (1992) Sequence and expression of a wheat gene that encodes a novel protein associated with pathogen defense. Mol Plant–Microbe Interact 5:516–519

    CAS  PubMed  Google Scholar 

  • Chen X (2005) Epidemiology and control of stripe rust (Puccinia striiformis f. sp. tritici) on wheat. Can J Plant Pathol 27:314–337

    Google Scholar 

  • Cliftona R, Millara A, Whelan J (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. BBA-Bioenergetics 1757:730–741

    Article  Google Scholar 

  • Coram T, Settles M, Chen X (2008a) Transcriptome analysis of high-temperature adult-plant resistance conditioned by Yr39 during the wheat–Puccinia striiformis f. sp. tritici interaction. Mol Plant Pathol 9:479–493

    Article  CAS  PubMed  Google Scholar 

  • Coram T, Wang M, Chen X (2008b) Transcriptome analysis of the wheat–Puccinia striiformis f. sp. tritici interaction. Mol Plant Pathol 9:157–169

    Article  CAS  PubMed  Google Scholar 

  • Dangl J, Jones J (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7:1243–1249. doi:10.1038/ni1410

    Article  CAS  PubMed  Google Scholar 

  • Dittrich H, Kutchan T (1991) Molecular cloning, expression, and induction of berberine bridge enzyme, an enzyme essential to the formation of benzophenanthridine alkaloids in the response of plants to pathogenic attack. Proc Natl Acad Sci U S A 88:9969–9973

    Article  CAS  PubMed  Google Scholar 

  • Dixon R, Achnine L, Kota P, Lui C, Reddy M, Wang L (2002) The phenylpropanoid pathway and plant defence—a genomics perspective. Mol Plant Pathol 3:371–390

    Article  CAS  PubMed  Google Scholar 

  • Gautier L, Cope L, Bolstad B, Irizarry R (2004) affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20:307–315

    Article  CAS  PubMed  Google Scholar 

  • Gentleman R, Carey V, Bates D, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn TWH, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini A, Sawitzki G, Smith C, Smyth G, Tierney L, Yang J, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80

    Article  PubMed  Google Scholar 

  • Gjetting T, Hagedorn P, Schweizer P, Thordal-Christensen H, Carver T, Lyngkjær M (2007) Single-cell transcript profiling of barley attacked by the powdery mildew fungus. Mol Plant–Microbe Interact 20:235–246

    Article  CAS  PubMed  Google Scholar 

  • Greenberg J (1997) Programmed cell death in plant–pathogen interactions. Annu Rev Plant Phys 48:525–545

    Article  CAS  Google Scholar 

  • Hammond-Kosack K, Parker J (2003) Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotech 14:177–193

    Article  CAS  PubMed  Google Scholar 

  • Hulbert S, Bai J, Fellers J, Pacheco M, Bowden R (2007) Gene expression patterns in near isogenic lines for wheat rust resistance gene Lr34/Yr18. Phytopathology 97:1083–1093

    Article  CAS  PubMed  Google Scholar 

  • Jansen C, Korell M, Eckey C, Biedenkopf D, Kogel K (2005) Identification and transcriptional analysis of powdery-mildew induced barley genes. Plant Sci 168:373–380

    Article  CAS  Google Scholar 

  • Jasinski M, Ducos E, Martinoia E, Boutry M (2003) The ATP-binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis. Plant Physiol 131:1169–1177

    Article  CAS  PubMed  Google Scholar 

  • Kong L, Anderson J, Ohm H (2005) Induction of wheat defense and stress-related genes in response to Fusarium graminearum. Genome 48:29–40

    Article  CAS  PubMed  Google Scholar 

  • Lamb C, Dixon R (1997) The oxidative burst in plant disease response. Annu Rev Plant Phys 48:251–275

    Article  CAS  Google Scholar 

  • Marcel T, Varshney R, Barbieri M, Jafary H, de Kock M, Graner A, Niks R (2007) A high-density consensus map of barley to compare the distribution of QTLs for partial resistance to Puccinia hordei and of defence gene homologues. Theor Appl Genet 114:487–500

    Article  CAS  PubMed  Google Scholar 

  • Mohammadi M, Kazemi H (2002) Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Sci 162:491–498

    Article  CAS  Google Scholar 

  • Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342

    Article  CAS  PubMed  Google Scholar 

  • Neu C, Keller B, Feuillet C (2003) Cytological and molecular analysis of the Hordeum vulgare–Puccinia triticina nonhost interaction. Mol Plant–Microbe Interact 16:626–633

    Article  CAS  PubMed  Google Scholar 

  • Pritsch C, Muehlbauer G, Bushnell W, Somers D, Vance C (2000) Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. Mol Plant–Microbe Interact 13:159–169

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Richards K, Schott E, Sharma Y, Davis K, Gardner R (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418

    Article  CAS  PubMed  Google Scholar 

  • Sculer M, Werck-Reichhart D (2003) Functional genomics of P450s. Annu Rev Plant Biol 54:629–667

    Article  Google Scholar 

  • Smyth G (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W (eds) Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York, pp 397–420

    Chapter  Google Scholar 

  • Van Ooijen G, Mayr G, Kasiem MMA, Albrecht M, Cornelissen BJC, Takken FLW (2008) Structure–function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59:1383–1397. doi:10.1093/jxb/ern045

    Article  PubMed  Google Scholar 

  • Wellings C, Singh R, McIntosh R, Pretorius Z (2004) The development and application of near isogenic lines for the wheat stripe (yellow) rust pathosystem. In 11th International Cereal Rusts and Powdery Mildew Conference. John Innes Centre, Norwich, p 39

    Google Scholar 

  • Yang KY, Im YJ, Chung GC, Cho BH (2002) Activity of the Arabidopsis blue copper-binding protein gene promoter in transgenic tobacco plants upon wounding. Plant Cell Rep 20:987–991. doi:10.1007/s00299-002-0436-1

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported in part by the US Department of Agriculture, Agricultural Research Service (project no. 5348-22000-014-00D), USDA-ARS Postdoctoral Program, and Washington Wheat Commission (project no. 13C-3061-3923). PPNS no. XXXX, Department of Plant Pathology, College of Agricultural, Human, and Natural Resources Research Center, project numbers WNP00823. The authors acknowledge Lisa Orfe and Dr. Douglas Call for printing the microarrays.

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Correspondence to Tristan E. Coram.

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Supplementary Table

The transcripts identified as uniquely significant (p < 0.10, fold change>2.0) for the incompatible interaction of each genotype in reference to mock-inoculated controls. Note that no unique transcripts were identified for genotypes Yr5 and Yr9. Functional categories were based on the Munich Information Center for Protein Sequence classifications and putative function shows the best significant BLASTX database hit from HarvEST. (DOC 125 kb)

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Coram, T.E., Huang, X., Zhan, G. et al. Meta-analysis of transcripts associated with race-specific resistance to stripe rust in wheat demonstrates common induction of blue copper-binding protein, heat-stress transcription factor, pathogen-induced WIR1A protein, and ent-kaurene synthase transcripts. Funct Integr Genomics 10, 383–392 (2010). https://doi.org/10.1007/s10142-009-0148-5

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  • DOI: https://doi.org/10.1007/s10142-009-0148-5

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