Skip to main content
Log in

Detection of physically interacting proteins with the CC and NB-ARC domains of a putative yellow rust resistance protein, Yr10, in wheat

  • Published:
Journal of Plant Diseases and Protection Aims and scope Submit manuscript

Abstract

Gene-for-gene (GFG) resistance is a potent defense mechanism in plants, that is mediated by resistance (R) proteins. In GFG resistance, pathogen effector or avirulence (Avr) proteins are recognised by R-proteins which initiate a series of signal transduction events that lead to hypersensitive cell death. In cereals, many R-proteins are comprised of an N-terminal coiled-coiled (CC) domain, a Nucleotide Binding (NB) domain and a Leucine Rich Repeats (LRR) region associated with effector recognition. NB-LRR immunity proteins are highly conserved across plant and animal taxa. To advance understating of signal transduction events in cereals, we exploited the high level of protein conservation to first identify yeast gene products interacting with the CC and NB domains of the candidate yellow rust R-protein (Yr10). Screening revealed proteins having mostly apoptosis related functions (Signal Recognition Particle 72kDa (SRP72); Chromosome SEgregation 1 (CSE1); ARrest Defective 1 (ARD1), translation initiation control in response to stress conditions (General Control Nonderepressible 2 (GCN2)), and a HSP90 co-chaperone (Cyclosporin-sensitive proline rotamase 7 (CPR7)). We then identified the close homologues of the interactors in barley and show that they were induced at 6h and/or 12 h after infection in Mla3 mediated Powdery Mildew (Blumeria graminis f.sp. hordei, Bgh) disease resistance, suggesting their involvement in pathogen response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arnesen T, Anderson D, Baldersheim C, Lanotte M, Varhaug JE & Lillehaug JR, 2005. Identification and characterization of the human ARD1-NATH protein acetyltransferase complex. Biochem J 386, 433–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K & Schulze-Lefert P, 2002. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295, 2073–6.

    Article  CAS  PubMed  Google Scholar 

  • Berardini TZ, Bollman K, Hui S & Poethig RS, 2001. Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science 291, 2405–07.

    Article  CAS  PubMed  Google Scholar 

  • Brinkmann U, 1998. CAS, the human homologue of the yeast chromosome-segregation gene CSE1, in proliferation, apoptosis, and cancer. Am J Hum Genet 62, 509–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemens MJ, 1997. PKR — a protein kinase regulated by doublestranded RNA. Int J Biochem Cell Biol 29, 945–949.

    Article  CAS  PubMed  Google Scholar 

  • Chen JJ, 2007. Regulation of protein synthesis by the heme-regulated eIF2alpha kinase: relevance to anemias. Blood 109, 2693–2699.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chang L-Y, Yang WY & Roth D, 2000. Functional complementation by wheat eIF2α in the yeast GCN2-mediated pathway. Biochem Bioph Res Co 279, 468–74.

    Article  CAS  Google Scholar 

  • Dangl JL & Jones JDG, 2001. Plant pathogens and integrated defense responses to infection. Nature 411, 826–833.

    Article  CAS  PubMed  Google Scholar 

  • Donze O & Picard D, 1999. Hsp90 binds and regulates the ligand-inducible a subunit of eukaryotic translation initiation factor kinase Gcn2. Mol Cell Biol 19, 8422–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duina AA, Kalton HM & Gaber RF, 1998. Requirement for Hsp90 and a CyP-40-type cyclophilin in negative regulation of the heat shock response. J Biol Chem 273, 18974–78.

    Article  CAS  PubMed  Google Scholar 

  • Duttweiler HM, 1996. A highly sensitive and non-lethal beta-galactosidase plate assay for yeast. Trends Genet 12, 340–341.

    Article  CAS  PubMed  Google Scholar 

  • Finlayson SD, Fleming C, Berry DR & Johnston JR, 1991. An improved lithium acetate method for yeast transformation. Biotech Tech 5, 13–18.

    Article  CAS  Google Scholar 

  • Halford NG, 2006. Regulation of carbon and amino acid metabolism, roles of sucrose nonfermenting-1-related protein kinase-1 and general control nonderepressible-2-related protein kinase. Adv Bot Res 43, 93–142.

    Article  CAS  Google Scholar 

  • Harding HP, Calfon M, Urano F, Novoa I & Ron D, 2002. Transcriptional and translational control in the Mammalian unfolded protein response. Annu Rev Cell Dev Biol 18, 575–599.

    Article  CAS  PubMed  Google Scholar 

  • Holt BF, Belkhadir Y & Dangl J, 2005. Antagonistic control of disease resistance protein stability in the plant immune system. Science 309, 929–932.

    Article  CAS  PubMed  Google Scholar 

  • Torres MA, Jones JDG & Dangl JL, 2006. ROS signaling in response to pathogens. Plant Physiol 141, 373–378.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H, Jiang X, Du F & Wang X, 2008. PHAPI, CAS, and Hsp70 Promote Apoptosome Formation by Preventing Apaf-1 Aggregation and Enhancing Nucleotide Exchange on Apaf-1. Mol Cell 30, 239–247.

    Article  CAS  PubMed  Google Scholar 

  • Kitagawa K, Skowyra D, Elledge SJ, Harper JW & Hieter P, 1999. SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol Cell 4, 21–33.

    Article  CAS  PubMed  Google Scholar 

  • Lageix S, Lanet E, Pouch-Pélissier M-N, Espagnol M-C, Robaglia C, Deragon J-M & Pélissier T, 2008. Arabidopsis eIF2α kinase GCN2 is essential for growth in stress conditions and is activated by wounding. BMC Plant Biol 8, 1–9.

    Article  Google Scholar 

  • Laroche A, Eudes F, Frick MM, Huel R, Nykiforuk CL, Conner RL, Kuzyk A, Acharya S & Jordan M, 2002. A wheat resistance gene against stripe rust. Can J Plant Pathol 24, 504–507.

    Article  Google Scholar 

  • Laroche A, Nykiforuk CL, Huel R, Frick MM, Conner RL, Kuzyk A, Eudes F, Acharya S & Jordan M, 2000. Identification of a candidate gene for the wheat stripe rust resistance locus Yr10. In International Plant Molecular Biology Meeting, Quebec, Canada, S22–S55.

    Google Scholar 

  • Liu Y, Burch-Smith T, Schiff M, Feng S & Dinesh-Kumar SP, 2004. Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 279, 2101–8.

    Article  CAS  PubMed  Google Scholar 

  • Mascarenhas C, Edwards-Ingram LC, Zeef L, Shenton D, Ashe MP & Grant CM, 2008. Gcn4 Is Required for the Response to Peroxide Stress in the Yeast Saccharomyces cerevisiae. Mol Biol Cell 19, 2995–3007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayr C, Richter K, Lilie H & Buchner J, 2000. Cpr6 and Cpr7, two closely related Hsp90-associated immunophilins from Saccharomyces cerevisiae, differ in their functional properties. J Biol Chem 275, 34140–46.

    Article  CAS  PubMed  Google Scholar 

  • Park EC & Szostack JW, 1992. ARD1 and NAT1 proteins form a complex that has N-terminal acetyltransferase activity. EMBO J 11, 2087–93.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ren Y-G, Wagner KW, Knee DA, Aza-Blanc P, Nasoff M & Deveraux QL, 2004. Differential Regulation of the TRAIL Death Receptors DR4 and DR5 by the Signal Recognition Particle. Mol Biol Cell 15, 5064–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samuel CE, 1993. The eIF2α protein kinases, regulators of translation in eukaryotes from yeasts to humans. J Biol Chem 268, 7603–8.

    CAS  PubMed  Google Scholar 

  • Serebriskii I, Khazak V & Golemis EA, 1999. A Two-hybrid dual bait system to discriminate specificity of protein interactions. J Biol Chem 274, 17080–87.

    Article  Google Scholar 

  • Shirasu K, Lahaye T, Tan MW, Zhou F, Azevedo C & Schulze-Lefert P, 1999. A novel class of eukaryotic zinc binding protein is required for disease resistance signaling in barley and development in C. elegans. Cell 99, 355–366.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi A, Casais C, Ichimura K & Shirasu K, 2003. HSP90 interacts with RAR1 and SGT1 and is essential for RPS2- mediated disease resistance in Arabidopsis. Proc Nat Acad Sci USA 100, 11777–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Utz PJ, Hottelet M, Le TM, Kim SJ, Geiger ME, van Venrooij WJ & Anderson P, 1998. The 72-kDa component of signal recognition particle is cleaved during apoptosis. J Biol Chem 273, 35362–70.

    Article  CAS  PubMed  Google Scholar 

  • Vandessompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A & Speleman F, 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3, research 00341–003411.

    Article  Google Scholar 

  • Zhang Y, Dickinson JR, Paul MJ & Halford NG, 2003. Molecular cloning of an Arabidopsis homologue of GCN2, a protein kinase involved in co-ordinated response to amino acid starvation. Planta 217, 668–75.

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang Y, Kanyuka K, Parry MAJ, Powers SJ & Halford NG, 2008. GCN2-dependent phosphorylation of eukaryotic translation initiation factor-2α in Arabidopsis. J Exp Bot 59, 3131–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mahinur S. Akkaya.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yildirim-Ersoy, F., Ridout, C.J. & Akkaya, M.S. Detection of physically interacting proteins with the CC and NB-ARC domains of a putative yellow rust resistance protein, Yr10, in wheat. J Plant Dis Prot 118, 119–126 (2011). https://doi.org/10.1007/BF03356391

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03356391

Keywords

Navigation