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The barley serine/threonine kinase gene Rpg1 providing resistance to stem rust belongs to a gene family with five other members encoding kinase domains

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Abstract

The barley (Hordeum vulgare L.) stem rust (Puccinia graminis f. sp. tritici) resistance gene Rpg1 encodes a serine/threonine protein kinase with two tandem kinase domains. The Rpg1 gene family was identified from the cv. Morex and consists of five additional members with divergent homology to Rpg1. All family members encode serine/threonine kinase-like proteins with at least one predicted catalytically active kinase domain. The five family members were sequenced from cDNA and genomic DNA and genetically mapped. The family member most closely related to Rpg1, ABC1037, is located on chromosome 1(7H) bin 01, very near (∼50 kb) but not co-segregating with Rpg1. Two others, ABC1036 and ABC1040, are closely related to each other and tightly linked on chromosome 7(5H) bin 07. ABC1041 mapped to chromosome 7(5H) bin 13, tightly linked to the rust resistance genes rpg4 and Rpg5 providing resistance to barley stem rust pathotype QCC and rye stem rust pathotype 92-MN-90, respectively, but segregated away in a high-resolution population. ABC1063 was localized to chromosome 4(4H) bin 6. An interesting Rpg1 allele that appears to be the result of unequal recombination between Rpg1 and ABC1037 was characterized. No known resistance loci cosegregated with any family members, however characterization of the Rpg1 family has provided insight into the evolution of this novel gene family and may present tools for understanding the functional domains of Rpg1. The genetic mapping, gene structures, and analysis of amino-acid sequences of the Rpg1 gene family members are presented.

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References

  • Behrmann I, Smyczek T, Heinrich P, Schmitz-Van de Leur H, Komyod W, Giese B, Muller-Newen G, Haan S, Haan C (2004) Janus kinase (JAK) subcellular localization revisited. J Biol Chem 279(34):35486–35493

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen J (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269

    Article  PubMed  CAS  Google Scholar 

  • Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, Chen J, Druka A, Steffenson B, Kleinhofs A (2002) The barley stem rust-resistance gene Rpg1 is a novel disease resistance gene with homology to receptor kinases. Proc Natl Acad Sci USA 99:9328–9333

    Article  PubMed  CAS  Google Scholar 

  • Cabrillac D, Delorme V, Garin J, Ruffio-Chable V, Giranton J, Dumas C, Gaude T, Cock J (1999) The S15 self-incompatibility haplotype in Brassica oleracea includes three S gene family members expressed in stigmas. Plant Cell 11:971–986

    Article  PubMed  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid Guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156

    Article  PubMed  CAS  Google Scholar 

  • Dodds P, Lawrence G, Ellis J (2001) Contrasting modes of evolution acting on the complex N locus for rust resistance in flax. Plant J 27:439–453

    Article  PubMed  CAS  Google Scholar 

  • Druka A, Kudrna D, Han F, Kilian A, Steffenson B, Frisch D, Tompkins J, Wing R, Kleinhofs A (2000) Physical mapping of the barley stem rust resistance gene rpg4. Mol Gen Genet 264:283–290

    Article  PubMed  CAS  Google Scholar 

  • Ellis J, Lawrence G, Finnegan E, Anderson P (1995) Contrasting complexity of two rust resistance loci in flax. Proc Natl Acad Sci USA 92:4185–4188

    Article  PubMed  CAS  Google Scholar 

  • Hanks S, Quinn A, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52

    PubMed  CAS  Google Scholar 

  • Horvath H, Rostoks N, Brueggeman R, Steffenson B, von Wettstein D, Kleinhofs A (2003) Genetically engineered stem rust resistance in barley using the Rpg1 gene. Proc Natl Acad Sci USA 100:364–369

    Article  PubMed  CAS  Google Scholar 

  • Kim Y, Lin N, Martin G (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589–598

    Article  PubMed  CAS  Google Scholar 

  • Kleinhofs A, Graner A (2001) An integrated map of the barley genome. In: Phillips RL, Vasil I (eds) DNA-based markers in plants, 2nd edn. Kluwer, Boston, pp 187–199

    Google Scholar 

  • Kleinhofs A, Kilian A, Saghai Maroof M, Biyashev R, Hayes P, Chen F, Lapitan N, Fenwick A, Blake T, Kanazin V, Ananiev E, Dahleen L, Kudrna D, Bollinger J, Knapp S, Liu B, Sorrells M, Heun M, Franckowiak J, Hoffman D, Skadsen R, Steffenson B (1993) A molecular, isozyme and morphological map of the barley (Hordeum vulgare) genome. Theor Appl Genet 86:705–712

    Article  CAS  Google Scholar 

  • Luo H, Roe P, Barber D, Hanratty W, Lee S, Roberts T, D’Andrea A, Dearolf C (1997) Mutation in the Jak kinase JH2 domain hyperactivates Drosophila and mammalian Jak-Stat pathways. Mol Cell Biol 17:1562–1571

    PubMed  CAS  Google Scholar 

  • Martin G, Brommonschenkel S, Chunwongse J, Frary A, Ganal M, Spivey R, Wu T, Earle E, Tanksley S (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436

    PubMed  CAS  Google Scholar 

  • Martin G, Frary A, Wu T, Brommonschenkel S, Chunwongse J (1994) Member of the Pto gene family confers sensitivity to fenthion resulting in rapid cell death. Plant Cell 6:1543–1552

    Article  PubMed  CAS  Google Scholar 

  • Martin G, Bogdanove A, Sessa G (2003) Understanding the function of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61

    Article  PubMed  CAS  Google Scholar 

  • Nirmala J, Brueggeman R, Maier C, Clay C, Rostoks N, Kannangara G, Wettstein D, Steffenson B, Kleinhofs A (2006) Sub-cellular localization and functions of the barley stem rust resistance receptor-like serine/threonine-specific protein kinase Rpg1. Proc Natl Acad Sci USA 103:7518–7523

    Article  PubMed  CAS  Google Scholar 

  • Pellegrini S, Dusanter-Fourt I (1997) The structure, regulation and function of the Janus kinases (JAKs) and the signal transducers and activators of transcription (STATs). Eur J Biochem 248:615–63

    Article  PubMed  CAS  Google Scholar 

  • Richter T, Ronald P (2000) The evolution of disease resistance genes. Plant Mol Biol 42:195–204

    Article  PubMed  CAS  Google Scholar 

  • Richter T, Pryor T, Bennetzen J, Hulbert S (1995) New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics 141:373–381

    PubMed  CAS  Google Scholar 

  • Ronald P, Albano B, Tabien R, Abenes L, Wu K, McCouch S, Tanksley S (1992) Genetics and physical analysis of the rice bacterial blight disease resistance locus, Xa21. Mol Gen Genet 236:113–120

    PubMed  CAS  Google Scholar 

  • Rosenberg E, Holmes M, Tenenholz T, Abd El Raouf Khalil A, Valerie K (2003) Mapping of transcription start sites by direct sequencing of SMARTTM RACE products. BioTechniques 34:482–486

    Google Scholar 

  • Rostoks N, Steffenson B, Kleinhofs A (2004) Structure and expression of the barley stem rust resistance gene Rpg1 messenger RNA. Phys Mol Plant Path 64:91–101

    Article  CAS  Google Scholar 

  • Saitou N Nei M (1987) The Neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Salmeron J., Oldroyd G, Rommens C, Scofield S, Kim H (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86:123–133

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Shao F, Goldstein C, Ade J, Stoutemyer M, Dixon J, Innes R (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–1233

    Article  PubMed  CAS  Google Scholar 

  • Shiu S-H, Bleeker A (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543

    Article  PubMed  CAS  Google Scholar 

  • Shiu S-H, Karlowski W, Pan R, Tzeng Y-H, Mayer K, Li W-H (2004) Comparitive analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 15:1220–1234

    Article  Google Scholar 

  • Song W, Wang G, Chen L, Kim H, Pi L, Gardner J, Wang B, Holsten T, Zhai W, Zhu L, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene Xa21. Science 270:1804–1806

    PubMed  CAS  Google Scholar 

  • Song W, Pi L, Wang G, Gardner J, Holsten T, Ronald P (1997) Evolution of the Rice Xa21 disease resistance gene family. Plant Cell 9:1279–1287

    Article  PubMed  CAS  Google Scholar 

  • Stein J, Howlett B, Boyes D, Nasrallah M, Nasrallah J (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci USA 88:8816–8820

    Article  PubMed  CAS  Google Scholar 

  • Stein J, Dixit R, Nasrallah M, Nasrallah J (1996) SRK, the stigma-specific S locus receptor kinase of Brassica, is targeted to the plasma membrane in transgenic tobacco. Plant Cell 8:429–445

    Article  PubMed  CAS  Google Scholar 

  • Swiderski M, Innes R (2001) The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J 26:101–112

    Article  PubMed  CAS  Google Scholar 

  • Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogal A, Hinata K (2000) The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403:913–916

    Article  PubMed  CAS  Google Scholar 

  • Yu Y, Tomkins J, Waugh R, Frisch D, Kudrna D, Kleinhofs A, Brueggeman R, Muehlbauer G, Wise R, Wing R (2000) A bacterial artificial chromosome library for barley (Hordeum vulgare L.) and the identification of clones containing putative resistance genes. Theor Appl Genet 101:1093–1099

    Article  CAS  Google Scholar 

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Acknowledgments

This is Scientific Paper No. 0302-06 from the College of Agricultural, Human, and Natural Sciences Research Center, Washington State University, Pullman, WA 99164, Project 0196. Research was supported by USDA-NRI grant # 2004-35301-14635 and the U.S. Barley Genome Project.

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Authors and Affiliations

  1. Department of Crop and Soil Sciences, Washington State University, Pullman, WA, 99164-6420, USA

    R. Brueggeman & A. Kleinhofs

  2. School of Molecular Biosciences, Washington State University, Pullman, WA, 99164-4234, USA

    T. Drader & A. Kleinhofs

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  1. R. Brueggeman
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  2. T. Drader
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  3. A. Kleinhofs
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Correspondence to R. Brueggeman.

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Communicated by B. Keller

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Brueggeman, R., Drader, T. & Kleinhofs, A. The barley serine/threonine kinase gene Rpg1 providing resistance to stem rust belongs to a gene family with five other members encoding kinase domains. Theor Appl Genet 113, 1147–1158 (2006). https://doi.org/10.1007/s00122-006-0374-3

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  • DOI: https://doi.org/10.1007/s00122-006-0374-3

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