Durable resistance to the wheat rusts: Integrating systems biology and traditional phenotype-based research methods to guide the deployment of resistance genes

Euphytica

Volumn 179, Issue 1, 2011, Pages 69-79

  Lowe, Iago ^a   Cantu, Dario ^a   Dubcovsky, Jorge ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Breeding; Interactome; Partial resistance; Puccinia; Triticum aestivum

Indexed keywords

PUCCINIA; PUCCINIA GRAMINIS F. SP. TRITICI; TRITICUM AESTIVUM; UREDINALES;

EID: 79953752182     PISSN: 00142336     EISSN: 15735060     Source Type: Journal    
DOI: 10.1007/s10681-010-0311-z     Document Type: Article

References (87)

1. Ayliffe MA, Lagudah ES (2004) Molecular genetics of disease resistance in cereals. Ann Bot 94: 765-773.
2. Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A et al (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295: 2073-2076.
3. Benfey PN, Mitchell-Olds T (2008) From genotype to phenotype: systems biology meets natural variation. Science 320: 495-497.
4. Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45: 399-436.
5. Bent AF, Kunkel BN, Dahlbeck D, Brown KL et al (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856-1860.
6. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43: 545-580.
7. Brueggeman R, Rostoks N, Kudrna D, Kilian A et al (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.
8. Brueggeman R, Druka A, Nirmala J, Cavileer T et al (2008) The stem rust resistance gene Rpg5 encodes a protein with nucleotide-binding-site, leucine-rich, and protein kinase domains. Proc Natl Acad Sci USA 105: 14970-14975.
9. Caldwell RM, Schafer JF, Compton LE, Patterson FL (1958) Tolerance to cereal leaf rusts. Science 128: 714-715.
10. Cantu D, Govindarajulu M, Kozik A, Wang M et al (2010) Next generation sequencing provides rapid access to the genes of wheat stripe rust. Submitted.
11. Carter AH, Chen XM, Garland-Campbell K, Kidwell KK (2009) Identifying QTL for high-temperature adult-plant resistance to stripe rust (Puccinia striiformis f. sp tritici) in the spring wheat (Triticum aestivum L.) cultivar 'Louise'. Theor Appl Genet 119: 1119-1128.
12. Chen XM (2005) Epidemiology and control of stripe rust (Puccinia striiformis f. sp tritici) on wheat. Can J Plant Pathol 27: 314-337.
13. Chen XM (2007) Challenges and solutions for stripe rust control in the United States. Aust J Agr Res 58: 648-655.
14. Cheng P, Chen X (2008) Molecular mapping of a gene for resistance to stripe rust in spring wheat cultivar IDO377 s. Phytopathology 98: S38-s39.
15. Chhuneja P, Kaur S, Garg T, Ghai M et al (2008) Mapping of adult plant stripe rust resistance genes in diploid A genome wheat species and their transfer to bread wheat. Theor Appl Genet 116: 313-324.
16. Cloutier S, McCallum BD, Loutre C, Banks TW et al (2007) 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.
17. Cuomo CA, Guldener U, Xu JR, Trail F et al (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400-1402.
18. Cusick ME, Klitgord N, Vidal M, Hill DE (2005) Interactome: gateway into systems biology. Hum Mol Genet 14(Spec no 2): R171-R181.
19. Dedryver F, Paillard S, Mallard S, Robert O et al (2009) Characterization of genetic components involved in durable resistance to stripe rust in the bread wheat 'Renan'. Phytopathology 99: 968-973.
20. Ding XD, Richter T, Chen M, Fujii H et al (2009) A rice kinase-protein interaction map. Plant Physiol 149: 1478-1492.
21. Dou D, Kale SD, Wang X, Jiang RH et al (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20: 1930-1947.
22. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protocols 2: 953-971.
23. Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10: 71-78.
24. Fiehn O (2002) Metabolomics--the link between genotypes and phenotypes. Plant Mol Biol 48: 155-171.
25. Flor HH (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32: 653-659.
26. Flor HH (1956) The complementary gene systems in flax and flax rust. Adv Genet 8: 29-54.
27. Fu D, Uauy C, Blechl A, Dubcovsky J (2007) RNA interference for wheat functional gene analysis. Transgenic Res 16: 689-701.
28. Fu D, Uauy C, Distelfeld A, Blechl A et al (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323: 1357-1360.
29. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43: 205-227.
30. Guo Q, Zhang ZJ, Xu YB, Li GH et al (2008) Quantitative trait loci for high-temperature adult-plant and slow-rusting resistance to Puccinia striiformis f. sp. tritici in wheat cultivars. Phytopathology 98: 803-809.
31. Hahn M, Mendgen K (1997) Characterization of in planta-induced rust genes isolated from a haustorium-specific cDNA library. Mol Plant Microbe Interact 10: 427-437.
32. Hovmoller MS, Yahyaoui AH, Milus EA, Justesen AF (2008) Rapid global spread of two aggressive strains of a wheat rust fungus. Mol Ecol 17: 3818-3826.
33. Huang L, Brooks S, Li W, Fellers J et al (2009) Evolution of new disease specificity at a simple resistance locus in a crop-weed complex: reconstitution of the Lr21 gene in wheat. Genetics 182: 595-602.
34. Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39: 285-312.
35. Ideker T, Galitski T, Hood L (2001) A new approach to decoding life: systems biology. Annu Rev Genomics Hum Genet 2: 343-372.
36. International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodiumdistachyon. Nature 463: 763-768.
37. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436: 793-800.
38. Jin Y, Steffenson BJ, Fetch T (1994) Sources of resistance to pathotype QCC of Puccinia graminis f. sp. tritici in barley. Crop Sci 34: 285-288.
39. Jin Y, Szabo LJ, Pretorius ZA, Singh RP et al (2008) Detection of virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp tritici. Plant Dis 92: 923-926.
40. Jin Y, Szabo LJ, Rouse MN, Fetch T et al (2009) Detection of virulence to resistanc gene Sr36 within the TTKS race lineage of Puccinia graminis f. sp. tritici. Plant Dis 93: 367-370.
41. Johnson R (1978) Practical breeding for durable resistance to rust diseases in self-pollinating cereals. Euphytica 27: 529-540.
42. Johnson R (1981) Durable resistance, definition of, genetic control, and attainment in plant breeding. Phytopathology 71: 567-568.
43. Johnson R (1984) A critical analysis of durable resistance. Annu Rev Phytopathol 22: 309-330.
44. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329.
45. Kale SD, Gu B, Capelluto DGS, Dou D et al (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142: 284-295.
46. Kämper J, Kahmann R, Bolker M, Ma LJ et al (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
47. 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.
48. Kitano H (2002) Systems biology: a brief overview. Science 295: 1662-1664.
49. Kloppers FJ, Pretorius ZA (1997) Effects of combinations amongst genes Lr13, Lr34 and Lr37 on components of resistance in wheat to leaf rust. Plant Pathol 46: 737-750.
50. Kolmer JA (1996) Genetics of resistance to wheat leaf rust. Annu Rev Phytopathol 34: 435-455.
51. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP et al (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323: 1360-1363.
52. Lu Y, Lan C, Liang S, Zhou X et al (2009) QTL mapping for adult-plant resistance to stripe rust in Italian common wheat cultivars Libellula and Strampelli. Theor Appl Genet 119: 1349-1359.
53. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ et al (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373.
54. Markell SG, Milus EA (2008) Emergence of a novel population of Puccinia striiformis f. sp. tritici in Eastern United States. Phytopathology 98: 632-639.
55. Martens JW, Dunsmore KM, Harder DE (1989) Incidence and virulence of Puccinia graminis in Canada on wheat and barley in 1988. Plant Pathol 11: 424-430.
56. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A et al (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262: 1432-1436.
57. Melichar JP, Berry S, Newell C, MacCormack R, Boyd LA (2008) QTL identification and microphenotype characterisation of the developmentally regulated yellow rust resistance in the UK wheat cultivar Guardian. Theor Appl Genet 117: 391-399.
58. Metzker ML (2010) Sequencing technologies--the next generation. Nat Rev Genet 11: 31-46.
59. Milus EA, Kristensen K, Hovmoller MS (2009) Evidence for increased aggressiveness in a recent widespread strain of Puccinia striiformis f. sp. tritici causing stripe rust of wheat. Phytopathology 99: 89-94.
60. Mindrinos M, Katagiri F, Yu GL, Ausubel FM (1994) The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089-1099.
61. Morsy M, Gouthu S, Orchard S, Thorneycroft D et al (2008) Charting plant interactomes: possibilities and challenges. Trends Plant Sci 13: 183-191.
62. Mustacchi R, Hohmann S, Nielsen J (2006) Yeast systems biology to unravel the network of life. Yeast 23: 227-238.
63. Oh SK, Young C, Lee M, Oliva R et al (2009) In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 21: 2928-2947.
64. Park CJ, Peng Y, Chen X, Dardick C et al (2008) Rice XB15, a protein phosphatase 2C, negatively regulates cell death and Xa21-mediated innate immunity. PLoS Biol 6: e231.
65. Paux E, Sourdille P, Salse J, Saintenac C et al (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322: 101-104.
66. Peng Y, Bartley LE, Chen X, Dardick C et al (2008) OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant 1: 446-458.
67. Pretorius ZA, Singh RP, Wagoire WW, Payne TS (2000) Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis 84: 203.
68. Rohila JS, Chen M, Chen S, Chen J et al (2006) Protein-protein interactions of tandem affinity purification-tagged protein kinases in rice. Plant J 46: 1-13.
69. Rosewarne GM, Singh RP, Huerta-Espino J, Rebetzke GJ (2008) Quantitative trait loci for slow-rusting resistance in wheat to leaf rust and stripe rust identified with multi-environment analysis. Theor Appl Genet 116: 1027-1034.
70. Rubiales D, Niks RE (1995) Characterization of Lr34, a major gene conferring nonhypersensitive resistance to wheat leaf rust. Plant Dis 79: 1208-1212.
71. Santra DK, Chen XM, Santra M, Campbell KG, Kidwell KK (2008) Identification and mapping QTL for high-temperature adult-plant resistance to stripe rust in winter wheat (Triticum aestivum L.) cultivar 'Stephens'. Theor Appl Genet 117: 793-802.
72. Scofield SR, Huang L, Brandt AS, Gill BS (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.
73. Seo NS, Lee SK, Song MY, Suh JP et al (2008) The HSP90-SGT1-RAR1 molecular chaperone complex: a core modulator in plant immunity. J Plant Biol 51: 1-10.
74. Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60: 139-164.
75. Singh RP (1992) Association between gene Lr34 for leaf rust resistance and leaf tip necrosis in wheat. Crop Sci 32: 874-878.
76. Singh RP, McIntosh RA (1984a) Complementary genes for reaction to Puccinia recondita tritici in Triticum aestivum. I: Genetic and linkage studies. Can J Genet Cytol 26: 723-735.
77. Singh RP, McIntosh RA (1984b) Complementary genes for reaction to Puccinia recondita tritici in Triticum aestivum. II: Cytogenetic studies. Can J Genet Cytol 26: 736-742.
78. Singh RP, Huerta-Espino J, Rajaram S (2000) Achieving near-immunity to leaf and stripe rusts in wheat by combining slow rusting resistance genes. Acta Phytopathol et Entomol Hungarica 35: 133-139.
79. Singh RP, Hodson DP, Jin Y, Huerta-Espino J et al (2006) Current status, likely migration and strategies to mitigate the threat to wheat production from race Ug99 (TTKS) of stem rust pathogen. CAB Rev 1: 1-13.
80. Song WY, Wang GL, Chen LL, Kim HS et al (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270: 1804-1806.
81. Tsunezuka H, Fujiwara M, Kawasaki T, Shimamoto K (2005) Proteome analysis of programmed cell death and defense signaling using the rice lesion mimic mutant cdr2. Mol Plant Microbe Interact 18: 52-59.
82. Uauy C, Paraiso F, Colasuonno P, Tran RK et al (2009) A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol 9: 115-128.
83. van Norman JM, Benfey PN (2009) Arabidopsis thaliana as a model organism in systems biology. Wiley Interdiscip Rev Syst Biol Med 1: 372-379.
84. Wang YS, Pi LY, Chen X, Chakrabarty PK et al (2006) Rice Xa21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18: 3635-3646.
85. Wroblewski T, Caldwell KS, Piskurewicz U, Cavanaugh KA et al (2009) Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Physiol 150: 1733-1749.
86. Yin C, Chen X, Wang X, Han Q et al (2009) Generation and analysis of expression sequence tags from haustoria of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. BMC Genomics 10: 626.
87. Zhou F, Kurth J, Wei F, Elliott C et al (2001) Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1-independent signaling pathway. Plant Cell 13: 337-350.