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Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family

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Abstract

In hexaploid wheat, leaf rust resistance gene Lr1 is located at the distal end of the long arm of chromosome 5D. To clone this gene, an F1-derived doubled haploid population and a recombinant inbred line population from a cross between the susceptible cultivar AC Karma and the resistant line 87E03-S2B1 were phenotyped for resistance to Puccinia triticina race 1-1 BBB that carries the avirulence gene Avr1. A high-resolution genetic map of the Lr1 locus was constructed using microsatellite, resistance gene analog (RGA), BAC end (BE), and low pass (LP) markers. A physical map of the locus was constructed by screening a hexaploid wheat BAC library from cultivar Glenlea that is known to have Lr1. The locus comprised three RGAs from a gene family related to RFLP marker Xpsr567. Markers specific to each paralog were developed. Lr1 segregated with RGA567-5 while recombinants were observed for the other two RGAs. Transformation of the susceptible cultivar Fielder with RGA567-5 demonstrated that it corresponds to the Lr1 resistance gene. In addition, the candidate gene was also confirmed by virus-induced gene silencing. Twenty T 1 lines from resistant transgenic line T 0-938 segregated for resistance, partial resistance and susceptibility to Avr1 corresponding to a 1:2:1 ratio for a single hemizygous insertion. Transgene presence and expression correlated with the phenotype. The resistance phenotype expressed by Lr1 seemed therefore to be dependant on the zygosity status. T 3-938 sister lines with and without the transgene were further tested with 16 virulent and avirulent rust isolates. Rust reactions were all as expected for Lr1 thereby providing additional evidence toward the Lr1 identity of RGA567-5. Sequence analysis of Lr1 indicated that it is not related to the previously isolated Lr10 and Lr21 genes and unlike these genes, it is part of a large gene family.

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References

  • Altschul SF, Madden TL, Schaffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Ausemus ER, Harrington JB, Worzella WW et al (1946) A summary of genetic studies in hexaploid and tetraploid wheats. J Am Soc Agron 38:1082–1099

    Google Scholar 

  • Bai J, Pennill LA, Ning J et al (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12:1871–1884

    Article  PubMed  CAS  Google Scholar 

  • Bossolini E, Wicker T, Knober PA et al (2007) Comparison of orthologous loci from small grass genomes Brachypodium and rice: implications from wheat genomics and grass genome annotation. Plant J 49:704–717

    Article  PubMed  CAS  Google Scholar 

  • Brooks SA, Huang L, Herbel MN et al (2006) Structural variation and evolution of a defense-gene cluster in natural populations of Aegilops tauschii. Theor Appl Genet 112:618–626

    Article  PubMed  CAS  Google Scholar 

  • Burch-Smith TM, Anderson JC, Martin GB et al (2004) Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J 39:734–746

    Article  PubMed  CAS  Google Scholar 

  • Chiu W, Niwa Y, Zeng W et al (1996) Engineered GFP as a vital reporter for plants. Curr Biol 6:325–330

    Article  PubMed  CAS  Google Scholar 

  • Christensen AH, Quail PH (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Trans Res 5:213–218

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dyck PL, Samborski DJ (1968) Genetics of resistance to leaf rust in common wheat varieties. Webster, Loros, Brevit, Carina, Malakoff and Centenario. Can J Genet Cytol 10:7–17

    Google Scholar 

  • Dyck PL, Samborski DJ, Martens JW (1985) Inheritance of resistance to leaf rust and stem rust in the wheat cultivar Glenlea. Can J Plant Pathol 7:351–354

    Google Scholar 

  • Feuillet C, Messmer M, Schachermayr G et al (1995) Genetic and physical characterization of the LR1 leaf rust resistance locus in wheat (Triticum aestivum L.). Mol Gen Genet 248:553–562

    Article  PubMed  CAS  Google Scholar 

  • Feuillet C, Travella S, Stein N et al (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc Natl Acad Sci USA 100:15253–15258

    Article  PubMed  CAS  Google Scholar 

  • Flor HH (1956) The complementary genic systems in flax and flax rust. Adv Genet 8:29–54

    Article  Google Scholar 

  • Gallego F, Feuillet C, Messmer M et al (1998) Comparative mapping of the two wheat leaf rust resistance loci Lr1 and Lr10 in rice and barley. Genome 41:328–336

    Article  PubMed  CAS  Google Scholar 

  • Graham MA, Marek LF, Shoemaker RC (2002) Organization, expression and evolution of a disease resistance gene cluster in soybean. Genetics 162:1961–1977

    PubMed  CAS  Google Scholar 

  • Graner A, Siedler H, Jahoor A et al (1990) Assessment of the degree and the type of restriction fragment length polymorphism in barley (Hordeum vulgare). Theor Appl Genet 80:826–832

    Article  Google Scholar 

  • Holzberg S, Brosio P, Gross C et al (2002) Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J 30:315–327

    Article  PubMed  CAS  Google Scholar 

  • Huang L, Brooks SA, Li W et al (2003) Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics 164:655–664

    PubMed  CAS  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM et al (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312

    Article  PubMed  CAS  Google Scholar 

  • Iyer LM, Kumpatla SP, Chandrasekharan MB et al (2000) Transgene silencing in monocots. Plant Mol Biol 43:323–346

    Article  PubMed  CAS  Google Scholar 

  • Jordan MC (2000) Green fluorescent protein as a visual marker for wheat transformation. Plant Cell Rep 19:1069–1075

    Article  CAS  Google Scholar 

  • Keller B, Feuillet C, Yahiaoui N (2005) Map-based isolation of disease resistance genes from bread wheat: cloning in a supersize genome. Genet Res 85:93–100

    Article  PubMed  CAS  Google Scholar 

  • Kolmer JA (1996) Genetics of resistance to wheat leaf rust. Annu Rev Phytopathol 34:435–455

    Article  PubMed  CAS  Google Scholar 

  • Kolmer JA (2001) Physiologic specialization of Puccinia triticina in Canada in 1998. Plant Dis 85:155–158

    Article  Google Scholar 

  • Kolmer JA (2005) Tracking wheat rust on a continental scale. Curr Opinion Plant Biol 8:441–449

    Article  Google Scholar 

  • Kolmer JA, Dyck PL (1994) Gene expression in the Triticum aestivum-Puccinia recondita f. sp. tritici gene-for-gene system. Phytopatol 84:437–440

    Article  Google Scholar 

  • Kolmer JA, Liu JQ (2002) Inheritance of leaf rust resistance in the wheat cultivars AC Majestic, AC Splendor, and AC Karma. Can J Plant Pathol 24:327–331

    Article  Google Scholar 

  • Kuang H, Woo S-S, Meyers BC et al (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16:2870–2894

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J et al (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Laurie DA, Bennett MD (1986) Wheat × maize hybridization. Can J Genet Cytol 28:313–316

    Google Scholar 

  • Lehmann P (2002) Structure and evolution of plant disease resistance genes. J Appl Genet 43:403–414

    PubMed  Google Scholar 

  • Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet 20:116–122

    Article  PubMed  CAS  Google Scholar 

  • Ling H-Q, Qiu J, Singh RP et al (2004) Identification and genetic characterization of an Aegilops tauschii ortholog of the wheat leaf rust disease resistance gene Lr1. Theor Appl Genet 109:1133–1138

    Article  PubMed  CAS  Google Scholar 

  • Ling H-Q, Zhu Y, Keller B (2003) High-resolution mapping of the leaf rust disease resistance gene Lr1 in wheat and characterization of BAC clones from the Lr1 locus. Theor Appl Genet 106:875–882

    PubMed  CAS  Google Scholar 

  • Liu JQ, Kolmer JA (1998) Genetics of stem rust resistance in wheat cvs Pasqua and AC Taber. Phytopathology 88:171–176

    Article  CAS  PubMed  Google Scholar 

  • Long DL, Kolmer JA (1989) A North American system of nomenclature for Puccinia recondita f. sp. tritici. Phytopathology 79:525–529

    Google Scholar 

  • Luo MC, Thomas C, You FM et al (2003) High-throughput fingerprinting of bacterial artificial chromosomes using the snapshot labeling kit and sizing of restriction fragments by capillary electrophoresis. Genomics 82:378–389

    Article  PubMed  CAS  Google Scholar 

  • Lupas A (1996) Coiled coils: new structures and new functions. Trends Biochem Sci 21:375–382

    Article  PubMed  CAS  Google Scholar 

  • Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252:1162–1164

    Article  PubMed  CAS  Google Scholar 

  • Madsen LH, Collins NC, Rakwalska M et al (2003) Barley disease resistance gene analogs of the NBS-LRR class: identification and mapping. Mol Gen Genom 269:150–161

    CAS  Google Scholar 

  • Mains EB, Leighty CE, Johnston CO (1926) Inheritance of resistance to leaf rust Puccinia triticina Erikss., in crosses of common wheat, Triticum vulgare Vill. J Agric Res 32:931–972

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • McIntosh RA, Baker EP, Driscoll CS (1965) Cytogenetic studies in wheat I. Monosomic analysis of leaf rust resistance in cultivar Uruguay and Transfer. Aust J Biol Sci 18:971–977

    Google Scholar 

  • McVey DV (1989) Verification of infection-type data for identification of genes for resistance to leaf rust in some hard red spring wheats. Crop Sci 29:304–307

    Article  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Kozik A, Griego A et al (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Shen KA, Rohani P et al (1998) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 11:1833–1846

    Article  Google Scholar 

  • Nilmalgoda SN, Cloutier S, Walichnowski AZ (2003) Construction and characterization of a bacterial artificial chromosome library of hexaploid wheat (Triticum aestivum L.) and validation of genome coverage using locus-specific primers. Genome 46:870–878

    Article  PubMed  CAS  Google Scholar 

  • Radovanovic N, Cloutier S (2003) Gene-assisted selection for high molecular weight glutenin subunits in wheat doubled haploid breeding programs. Mol Breed 12:51–59

    Article  CAS  Google Scholar 

  • Samborski DJ (1973) Leaf rust of wheat in Canada in (1972). Can Plant Dis Surv 52:168–170

    Google Scholar 

  • Schachermayr GM, Messmer MM, Feuillet C et al (1995) Identification of molecular markers linked to the Agropyron elongatum-derived leaf rust resistance gene Lr24 in wheat. Theor Appl Genet 90:982–990

    Article  CAS  Google Scholar 

  • Scofield SR, Huang L, Brandt AS et al (2005) Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol 138:2165–2173

    Article  PubMed  CAS  Google Scholar 

  • Shen Q-H, Sajo Y, Mauch S (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315:1098–1103

    Article  PubMed  CAS  Google Scholar 

  • Simons K, Fellers JP, Trick HN et al (2005) Isolation and characterization of the major domestication gene Q in wheat. Proc Plant Ani Genome XIII meeting, 15–19 Jan 2005, San Diego, USA, p 97

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

    Article  PubMed  CAS  Google Scholar 

  • Sonnhammer EL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:1–10

    Article  Google Scholar 

  • Stam M, Mol JNM, Kooter JM (1997) The silence of genes in transgenic plants. Ann Bot 79:3–12

    Article  CAS  Google Scholar 

  • Stein N, Feuillet C, Wicker T et al (2000) Subgenome chromosome walking in wheat: a 450-kb physical contig in Triticum monococcum L. spans the Lr10 resistance locus in hexaploid wheat (Triticum aestivum L.). Proc Natl Acad Sci 97:13436–13441

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Upadhyaya NM, Ramm K, Gaudron J et al (1998) Can gfp replace uidA as a reporter gene to monitor transformation of cereals by biolistics or Agrobacterium? In: Larkin PJ (ed) Agricultural Biotechnology: Laboratory, Field and Market. Proceedings of the 4th Asia-Pacific conference on agricultural biotechnology, Darwin, 13–16 July, Canberra UTC publishing, pp 111–113

  • Van der Biezen EA, Jones JDG (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23:454–456

    Article  PubMed  Google Scholar 

  • Vaucheret H, Béclin C, Elmayan T et al (1998) Transgene-induced gene silencing in plants. Plant J 16:651–659

    Article  PubMed  CAS  Google Scholar 

  • Webb CA, Fellers JP (2006) Cereal rust fungi genomics and the pursuit of virulence and avirulence factors. FEMS Microbiol Lett 264:1–7

    Article  PubMed  CAS  Google Scholar 

  • Xie DX, Devos KM, Moore G et al (1993) RFLP-based genetic maps of the homoeologous group 5 chromosomes of bread wheat (Triticum aestivum L.). Theor Appl Genet 87:70–74

    Article  CAS  Google Scholar 

  • Xu Z, Deal KR, Li W et al (2002) Construction and characterization of five large-insert BAC and BiBAC libraries of Aegilops tauschii, the diploid donor of the wheat D genome. Proc Plant Ani Microbe Genomes X meeting, 12–16 Jan 2002, San Diego, USA, p 101

  • Yahiaoui N, Srichumpa P, Dudler R et al (2004) Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J 37:528–538

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G et al (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Loukoianov A, Blechl A et al (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644

    Article  PubMed  CAS  Google Scholar 

  • Zhang H-B, Zhao Z, Ding X et al (1995) Preparation of megabase-size DNA from plant nuclei. Plant J 7:175–184

    Article  CAS  Google Scholar 

  • Zhou T, Wang Y, Chen JQ et al (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genom 271:402–415

    Article  CAS  Google Scholar 

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Acknowledgements

The authors extend sincere thanks to Pat Seto-Goh, Elsa Reimer, Natasa Radovanovic, Andrzej Walichnowski, Danielle Deshaies, Marcy Zirino, Tao Fan, and Mark Gray for excellent technical support throughout the project. We would also like to thank Andrzej Walichnowski for manuscript review, Joanne Schiavoni for manuscript preparation, and Michael Shillinglaw for the figures. We wish to thank CSIRO Plant Industry (Canberra, Australia) for the gift of pMNK1005. We wish to thank Large Scale Biology Corporation, Vacaville, CA for providing us with the viral vector subunits. We thank Dr. Steve Scofield for introducing us into the VIGS approach in wheat and his help setting up the system. The work on VIGS and annotation of the BAC sequences, carried out at the University of Zürich (C.L., T.W., and B.K.) was supported by the Swiss National Science Foundation (SNF) grant 3100A0–105620. This remainder of the project was carried out at the Cereal Research Centre of Agriculture and Agri-Food Canada in Winnipeg and was funded by the Canadian Crop Genomics Initiative. This is AAFC contribution number 1951.

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  1. Catherine Feuillet

    Present address: Institut National de la Recherche Agronomique, Amélioration et Santé des Plantes, 234 Ave du Brézet, 63039, Clermont Ferrand, France

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  1. Cereal Research Centre, Agriculture and Agri-Food Canada, 195 Dafoe Road, R3T 2M9, Winnipeg, MB, Canada

    Sylvie Cloutier, Brent D. McCallum, Travis W. Banks & Mark C. Jordan

  2. Institute of Plant Biology, University of Zürich, Zollikerstr. 107, 8008, Zurich, Switzerland

    Caroline Loutre, Thomas Wicker, Catherine Feuillet & Beat Keller

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  1. Sylvie Cloutier
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Correspondence to Sylvie Cloutier.

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Cloutier, S., McCallum, B.D., Loutre, C. et al. Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol Biol 65, 93–106 (2007). https://doi.org/10.1007/s11103-007-9201-8

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