A candidate gene for fire blight resistance in Malus × robusta 5 is coding for a CC-NBS-LRR

Tree Genetics and Genomes

Volumn 9, Issue 1, 2013, Pages 237-251

  Fahrentrapp, Johannes ^a   Broggini, Giovanni A L ^a   Kellerhals, Markus ^b   Peil, Andreas ^c   Richter, Klaus ^c   Zini, Elena ^d   Gessler, Cesare ^a  

^a ETH ZURICH   (Switzerland)

^b AGROSCOPE   (Switzerland)

^c INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^d RESEARCH AND INNOVATION CENTRE   (Italy)

Author keywords

Apple breeding; Erwinia amylovora; Fine mapping; Positional cloning; QTL analysis; R gene

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); ERWINIA AMYLOVORA; MALUS; MALUS X DOMESTICA; PYRUS; PYRUS COMMUNIS;

EID: 84872654423     PISSN: 16142942     EISSN: 16142950     Source Type: Journal    
DOI: 10.1007/s11295-012-0550-3     Document Type: Article

References (72)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
3. Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12: 1871-1884.
4. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
5. Baldi P, Patocchi A, Zini E, Toller C, Velasco R, Komjanc M (2004) Cloning and linkage mapping of resistance gene homologues in apple. Theor Appl Genet 109: 231-239.
6. Barakat A, Han DT, Benslimane A-A, Rode A, Bernardi G (1999) The gene distribution in the genomes of pea, tomato and date palm. FEBS Lett 463: 139-142.
7. Bernardi G (2004) The organization of plant genomes. In: Bernardi G (ed) New comprehensive biochemistry. Elsevier, Amsterdam, pp 227-240.
8. Block A, Alfano JR (2011) Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr Opin Microbiol 14: 39-46.
9. Broggini GAL, Le Cam B, Parisi L, Wu C, Zhang HB, Gessler C, Patocchi A (2007) Construction of a contig of BAC clones spanning the region of the apple scab avirulence gene AvrVg. Fungal Genet Biol 44: 44-51.
10. Broggini GAL, Galli P, Parravicini G, Gianfranceschi L, Gessler C, Patocchi A (2009) HcrVf paralogs are present on linkage groups 1 and 6 of Malus. Genome 52: 129-138.
11. Calenge F, van der Linden CG, van de Weg E, Schouten HJ, van Arkel G, Denance C, Durel CE (2005) Resistance gene analogues identified through the NBS-profiling method map close to major genes and QTL for disease resistance in apple. Theor Appl Genet 110: 660-668.
12. Caplan J, Padmanabhan M, Dinesh-Kumar SP (2008) Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3: 126-135.
13. Chagne D, Carlisle C, Blond C, Volz R, Whitworth C, Oraguzie N, Crowhurst R, Allan A, Espley R, Hellens R, Gardiner S (2007) Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8: 212.
14. DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7: 1243-1249.
15. Durel CE, Denance C, Brisset MN (2009) Two distinct major QTL for resistance to fire blight co-localize on linkage group 12 in apple genotypes 'Evereste' and Malus floribunda clone 821. Genome 52: 139-147.
16. FAO (2009) Food and agricultural organization of the United Nations Statistical database. FAO, Rome.
17. Flor H (1971) Current status of gene-for-gene concept. Annu Rev Phytopathol 9: 275.
18. Frey JE, Frey B, Sauer C, Kellerhals M (2004) Efficient low-cost DNA extraction and multiplex fluorescent PCR method for marker-assisted selection in breeding. Plant Breed 123: 554-557.
19. Galli P, Patocchi A, Broggini GAL, Gessler C (2010) The Rvi15 (Vr2) apple scab resistance locus contains three TIR-NBS-LRR genes. Mol Plant Microbe Interact 23: 608-617.
20. Gardiner S, Norelli J, de Silva N, Fazio G, Peil A, Malnoy M, Horner M, Bowatte D, Carlisle C, Wiedow C, Wan Y, Bassett C, Baldo A, Celton J-M, Richter K, Aldwinckle H, Bus V (2012) Putative resistance gene markers associated with quantitative trait loci for fire blight resistance in Malus 'Robusta 5' accessions. BMC Genet 13: 25.
21. Gessler C (2011) Cisgenic disease resistant apples: a product with benefits for the environment, producer and consumer. Outlooks Pest Manag 22: 216-219.
22. Grant M, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes R, Dangl J (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843-846.
23. Hammond-Kosack KE, Jones JD (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48: 575-607.
24. Jones DA, Jones JDG (1997) The role of leucine-rich repeat proteins in plant defences. Adv Bot Res 24: 89-167.
25. Juniper BE, Mabberley DJ (2006) The story of the apple. Timber Press, Portland.
26. Kajava AV, Kobe B (2002) Assessment of the ability to model proteins with leucine-rich repeats in light of the latest structural information. Protein Sci 11: 1082-1090.
27. Kellerhals M, Székely T, Sauer C, Frey J, Patocchi A (2009) Pyramiding scab resistances in apple breeding. Erwerbs-Obstbau 51: 21-28.
28. Khan M, Zhao YF, Korban S (2011) Molecular mechanisms of pathogenesis and resistance to the bacterial pathogen Erwinia amylovora, causal agent of fire blight disease in Rosaceae. Plant Mol Biol Rep 30(2): 247-260.
29. Kobe B, Deisenhofer J (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19: 415-421.
30. Kruijt M, De Kock MJD, De Wit PJGM (2005) Receptor-like proteins involved in plant disease resistance. Mol Plant Pathol 6: 85-97.
31. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132.
32. Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, van De Weg E, Gessler C (2002) Development and characterisation of 140 new microsatellites in apple (Malus × domestica Borkh.). Mol Breed 10: 217-241.
33. Lupas A (1996) Prediction and analysis of coiled-coil structures. In: Russell FD (ed) Methods Enzymol. Academic, Waltham, pp 513-525.
34. Lupas A, van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252: 1162-1164.
35. 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.
36. McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40: 349-379.
37. McManus PS, Stockwell VO, Sundin GW, Jones AL (2002) Antibiotic use in plant agriculture. Annu Rev Phytopathol 40: 443-465.
38. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809-834.
39. Ngugi HK, Lehman B, Madden LV (2011) Multiple treatment meta-analysis of products evaluated for control of fire blight in the eastern United States. Phytopathology 101: 512-522.
40. Norelli JL, Aldwinckle HS (1986) Differential susceptibility of Malus spp cultivars Robusta 5, Novole, and Ottawa 523 to Erwinia amylovora. Plant Dis 70: 1017-1019.
41. Norelli JL, Aldwinckle HS, Beer SV (1988) Virulence of Erwinia amylovora strains to Malus sp. Novole plants grown in vitro and in the greenhouse. Phytopathology 78: 1292-1297.
42. Norelli JL, Farrell RE, Bassett CL, Baldo AM, Lalli DA, Aldwinckle HS, Wisniewski ME (2009) Rapid transcriptional response of apple to fire blight disease revealed by cDNA suppression subtractive hybridization analysis. Tree Genet Genomes 5: 27-40.
43. Pagni M, Ioannidis V, Cerutti L, Zahn-Zabal M, Jongeneel CV, Hau J, Martin O, Kuznetsov D, Falquet L (2007) MyHits: improvements to an interactive resource for analyzing protein sequences. Nucleic Acids Res 35: W433-W437.
44. Parravicini G (2010) Candidate genes for fire blight resistance in apple cultivar 'Evereste'. IBZ Plant Pathology, ETH, Zurich, p 149.
45. Parravicini G, Gessler C, Denance C, Lasserre-Zuber P, Vergne E, Brisset MN, Patocchi A, Durel CE, Broggini GAL (2011) Identification of serine/threonine kinase and nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes in the fire blight resistance quantitative trait locus of apple cultivar 'Evereste'. Mol Plant Pathol 12: 493-505.
46. Patocchi A, Vinatzer BA, Gianfranceschi L, Tartarini S, Zhang HB, Sansavini S, Gessler C (1999) Construction of a 550 kb BAC contig spanning the genomic region containing the apple scab resistance gene Vf. Mol Gen Genet 262: 884-891.
47. Paulin JP, Lachaud G, Lespinasse Y (1993) Role of the aggressiveness of strains of Erwinia amylovora in the experimental evaluation of susceptibility of apple cultivars to fire blight. Acta Hortic (ISHS) 338: 375-376.
48. Pedley KF, Martin GB (2003) Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu Rev Phytopathol 41: 215-243.
49. Peil A, Garcia-Libreros T, Richter K, Trognitz FC, Trognitz B, Hanke MV, Flachowsky H (2007) Strong evidence for a fire blight resistance gene of Malus robusta located on linkage group 3. Plant Breed 126: 470-475.
50. Peil A, Hanke MV, Flachowsky H, Richter K, Garcia-Libreros T, Celton JM, Gardiner S, Horner M, Bus V (2008) Confirmation of the fire blight QTL of Malus × robusta 5 on linkage group 3. Acta Hortic (ISHS) 793: 297-303.
51. Peil A, Flachowsky H, Hanke M-V, Richter K, Rode J (2011) Inoculation of Malus × robusta 5 progeny with a strain breaking resistance to fire blight reveals a minor QTL on LG5. Acta Hortic (ISHS) 896: 357-362.
52. Rairdan GJ, Collier SM, Sacco MA, Baldwin TT, Boettrich T, Moffett P (2008) The coiled-coil and nucleotide binding domains of the potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell 20: 739-751.
53. Richter K, Fischer C (2000) Stability of fire blight resistance in apple. Acta Hortic (ISHS) 538: 267-270.
54. Rozen S, Skaletsky H (1999) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
55. Salamov AA, Solovyev VV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10: 516-522.
56. Sanseverino W, Roma G, De Simone M, Faino L, Melito S, Stupka E, Frusciante L, Ercolano MR (2010) PRGdb: a bioinformatics platform for plant resistance gene analysis. Nucleic Acids Res 38: D814-D821.
57. Schouten HJ, Krens FA, Jacobsen E (2006) Cisgenic plants are similar to traditionally bred plants. EMBO Rep 7: 750-753.
58. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18: 233-234.
59. Söding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21: 951-960.
60. Szankowski I, Waidmann S, Degenhardt J, Patocchi A, Paris R, Silfverberg-Dilworth E, Broggini GAL, Gessler C (2009) Highly scab-resistant transgenic apple lines achieved by introgression of HcrVf2 controlled by different native promoter lengths. Tree Genet Genomes 5: 349-358.
61. Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci U S A 96: 14153-14158.
62. Taylor WR (1986) The classification of amino acid conservation. J Theor Biol 119: 205-218.
63. van der Biezen EA, Jones JD (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23: 454-456.
64. van der Hoorn RAL, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20: 2009-2017.
65. van der Zwet T (2006) Present worldwide distribution of fire blight and closely related diseases. Acta Hortic (ISHS) 704: 35-36.
66. van Ooijen JW, Voorrips RE (2001) JoinMap 3. 0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen.
67. 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.
68. Vanblaere T, Szankowski I, Schaart J, Schouten H, Flachowsky H, Broggini GAL, Gessler C (2011) The development of a cisgenic apple plant. J Biotechnol 154: 304-311.
69. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C-E, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42: 833-839.
70. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1: 945-951.
71. Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang Z-X, Kono I, Kurata N, Yano M, Iwata N, Sasaki T (1998) Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci U S A 95: 1663-1668.
72. Zhao YF, He SY, Sundin GW (2006) The Erwinia amylovora avrRpt2(EA) gene contributes to virulence on pear and AvrRpt2(EA) is recognized by Arabidopsis RPS2 when expressed in Pseudomonas syringae. Mol Plant Microbe Interact 19: 644-654.