The Barley Stem Rust-resistance Gene Rpg1 is a Novel Disease-resistance Gene with Homology to Receptor Kinases

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2002 Jun 22

PMID 12077318

Citations 156

Authors

R Brueggeman

N Rostoks

D Kudrna

A Kilian

F Han

J Chen

A Druka

B Steffenson

A Kleinhofs

Affiliations

Soon will be listed here.

Abstract

Stem rust caused by Puccinia graminis f. sp. tritici was among the most devastating diseases of barley in the northern Great Plains of the U.S. and Canada before the deployment of the stem rust-resistance gene Rpg1 in 1942. Since then, Rpg1 has provided durable protection against stem rust losses in widely grown barley cultivars (cvs.). Extensive efforts to clone Rpg1 by synteny with rice provided excellent flanking markers but failed to yield the gene because it does not seem to exist in rice. Here we report the map-based cloning and characterization of Rpg1. A high-resolution genetic map constructed with 8,518 gametes and a 330-kb bacterial artificial chromosome contig physical map positioned the gene between two crossovers approximately 0.21 centimorgan and 110 kb apart. The region including Rpg1 was searched for potential candidate genes by sequencing low-copy probes. Two receptor kinase-like genes were identified. The candidate gene alleles were sequenced from resistant and susceptible cvs. Only one of the candidate genes showed a pattern of apparently functional gene structure in the resistant cvs. and defective gene structure in the susceptible cvs. identifying it as the Rpg1 gene. Rpg1 encodes a receptor kinase-like protein with two tandem protein kinase domains, a novel structure for a plant disease-resistance gene. Thus, it may represent a new class of plant resistance genes.

Citing Articles

Tandem kinase proteins across the plant kingdom.

Reveguk T, Fatiukha A, Potapenko E, Reveguk I, Sela H, Klymiuk V Nat Genet. 2025; 57(1):254-262.

PMID: 39779952 DOI: 10.1038/s41588-024-02032-x.

Mapping and Candidate Gene Analysis of an All-Stage Stem Rust Resistance Gene in Durum Wheat Landrace PI 94701.

Li H, Li K, Li H, Yang C, Perera G, Wang G Plants (Basel). 2024; 13(16).

PMID: 39204633 PMC: 11359134. DOI: 10.3390/plants13162197.

Allelic variability in the Rpp1 locus conferring resistance to Asian soybean rust revealed by genome-wide association.

Aoyagi L, Ferreira E, Gregorio da Silva D, Dos Santos A, Avelino B, Lopes-Caitar V BMC Plant Biol. 2024; 24(1):743.

PMID: 39095733 PMC: 11297723. DOI: 10.1186/s12870-024-05454-1.

A kinase fusion protein from Aegilops longissima confers resistance to wheat powdery mildew.

He H, Chen Z, Fan R, Zhang J, Zhu S, Wang J Nat Commun. 2024; 15(1):6512.

PMID: 39095395 PMC: 11297308. DOI: 10.1038/s41467-024-50909-6.

Association mapping with a diverse population of Puccinia graminis f. sp. tritici identified avirulence loci interacting with the barley Rpg1 stem rust resistance gene.

Upadhaya A, Upadhaya S, Brueggeman R BMC Genomics. 2024; 25(1):751.

PMID: 39090588 PMC: 11295639. DOI: 10.1186/s12864-024-10670-y.

References

Walker J . Structure and function of the receptor-like protein kinases of higher plants. Plant Mol Biol. 1994; 26(5):1599-609. DOI: 10.1007/BF00016492. View

Hanks S, Quinn A, Hunter T . The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988; 241(4861):42-52. DOI: 10.1126/science.3291115. View

Kilian A, Kudrna D, Kleinhofs A, Yano M, Kurata N, Steffenson B . Rice-barley synteny and its application to saturation mapping of the barley Rpg1 region. Nucleic Acids Res. 1995; 23(14):2729-33. PMC: 307098. DOI: 10.1093/nar/23.14.2729. View

Rane S, Reddy E . JAK3: a novel JAK kinase associated with terminal differentiation of hematopoietic cells. Oncogene. 1994; 9(8):2415-23. View

Richter T, Ronald P . The evolution of disease resistance genes. Plant Mol Biol. 2000; 42(1):195-204. View

Fisher T, Blenis J . Evidence for two catalytically active kinase domains in pp90rsk. Mol Cell Biol. 1996; 16(3):1212-9. PMC: 231103. DOI: 10.1128/MCB.16.3.1212. View

Torii K . Receptor kinase activation and signal transduction in plants: an emerging picture. Curr Opin Plant Biol. 2000; 3(5):361-7. DOI: 10.1016/s1369-5266(00)00097-2. View

Scofield , Tobias , Rathjen , Chang , Lavelle , Michelmore . Molecular Basis of Gene-for-Gene Specificity in Bacterial Speck Disease of Tomato. Science. 1996; 274(5295):2063-5. DOI: 10.1126/science.274.5295.2063. View

Rostoks N, Park Y, Ramakrishna W, Ma J, Druka A, Shiloff B . Genomic sequencing reveals gene content, genomic organization, and recombination relationships in barley. Funct Integr Genomics. 2002; 2(1-2):51-9. DOI: 10.1007/s10142-002-0055-5. View

10.

van der Knaap E, Song W, Ruan D, Sauter M, Ronald P, Kende H . Expression of a gibberellin-induced leucine-rich repeat receptor-like protein kinase in deepwater rice and its interaction with kinase-associated protein phosphatase. Plant Physiol. 1999; 120(2):559-70. PMC: 59295. DOI: 10.1104/pp.120.2.559. View

11.

Martin G, Brommonschenkel S, Chunwongse J, Frary A, Ganal M, Spivey R . Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science. 1993; 262(5138):1432-6. DOI: 10.1126/science.7902614. View

12.

Devereux J, Haeberli P, SMITHIES O . A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984; 12(1 Pt 1):387-95. PMC: 321012. DOI: 10.1093/nar/12.1part1.387. View

13.

Hulbert S, Webb C, Smith S, Sun Q . Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol. 2001; 39:285-312. DOI: 10.1146/annurev.phyto.39.1.285. View

14.

Kilian A, Chen J, Han F, Steffenson B, Kleinhofs A . Towards map-based cloning of the barley stem rust resistance genes Rpg1 and rpg4 using rice as an intergenomic cloning vehicle. Plant Mol Biol. 1997; 35(1-2):187-95. View

15.

Kawchuk L, Hachey J, Lynch D, Kulcsar F, van Rooijen G, Waterer D . Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci U S A. 2001; 98(11):6511-5. PMC: 33499. DOI: 10.1073/pnas.091114198. View

16.

Kleinhofs A, Kilian A, Saghai Maroof M, Biyashev R, Hayes P, Chen F . A molecular, isozyme and morphological map of the barley (Hordeum vulgare) genome. Theor Appl Genet. 2013; 86(6):705-12. DOI: 10.1007/BF00222660. View

17.

Rostoks N, Zale M, Soule J, Brueggeman R, Druka A, Kudrna D . A barley gene family homologous to the maize rust resistance gene Rp1-D. Theor Appl Genet. 2003; 104(8):1298-1306. DOI: 10.1007/s00122-002-0902-8. View

18.

Stein J, Howlett B, Boyes D, Nasrallah M, Nasrallah J . Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci U S A. 1991; 88(19):8816-20. PMC: 52601. DOI: 10.1073/pnas.88.19.8816. View

19.

Stein J, Dixit R, Nasrallah M, Nasrallah J . SRK, the stigma-specific S locus receptor kinase of Brassica, is targeted to the plasma membrane in transgenic tobacco. Plant Cell. 1996; 8(3):429-45. PMC: 161111. DOI: 10.1105/tpc.8.3.429. View

20.

Sessa G, Martin G . Signal recognition and transduction mediated by the tomato Pto kinase: a paradigm of innate immunity in plants. Microbes Infect. 2000; 2(13):1591-7. DOI: 10.1016/s1286-4579(00)01315-0. View