Exploiting regulatory variation to identify genes underlying quantitative resistance to the wheat stem rust pathogen Puccinia graminis f. sp. tritici in barley
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- 作者：Arnis Druka (1)
Elena Potokina (2)
Zewei Luo (2)
Nicola Bonar (1)
Ilze Druka (1) (3)
Ling Zhang (4)
David F. Marshall (1)
Brian J. Steffenson (5)
Timothy J. Close (6)
Roger P. Wise (7)
Andris Kleinhofs (4)
Robert W. Williams (8)
Michael J. Kearsey (2)
Robbie Waugh (1) - 刊名：Theoretical and Applied Genetics
- 出版年：2008
- 出版时间：July 2008
- 年：2008
- 卷：117
- 期：2
- 页码：261-272
- 全文大小：1249KB
- 参考文献：1. Badigannavar AM, Kale DM, Eapen S, Murty GS (2002) Inheritance of disease lesion mimic leaf trait in groundnut. J Hered 93:50-2 jhered/93.1.50">CrossRef
2. Balague C, Lin B, Alcon C, Flottes G, Malmstrom S, Kohler C, Neuhaus G, Pelletier G, Gaymard F, Roby D (2003) HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15:365-79 CrossRef
3. Bonfield JK, Smith K, Staden R (1995) A new DNA sequence assembly program. Nucleic Acids Res 23:4992-999 CrossRef
4. 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 99:9328-333 CrossRef
5. Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der LT, Diergaarde P, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley / Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695-05 CrossRef
6. Bystrykh L, Weersing E, Dontje B, Sutton S, Pletcher MT, Wiltshire T, Su AI, Vellenga E, Wang J, Manly KF, Lu L, Chesler EJ, Alberts R, Jansen RC, Williams RW, Cooke MP, de Haan G (2005) Uncovering regulatory pathways that affect hematopoietic stem cell function using ‘genetical genomics- Nat Genet 37:225-32 CrossRef
7. Chesler EJ, Wang J, Lu L, Qu Y, Manly KF, Williams RW (2003) Genetic correlates of gene expression in recombinant inbred strains: a relational model system to explore neurobehavioral phenotypes. Neuroinformatics 1:343-57 CrossRef
8. Chesler EJ, Lu L, Shou S, Qu Y, Gu J, Wang J, Hsu HC, Mountz JD, Baldwin NE, Langston MA, Threadgill DW, Manly KF, Williams RW (2005) Complex trait analysis of gene expression uncovers polygenic and pleiotropic networks that modulate nervous system function. Nat Genet 37:233-42 CrossRef
9. Cho S, Garvin DF, Muehlbauer GJ (2005) Transcriptome analysis and physical mapping of barley genes in wheat–barley chromosome addition lines. Genetics 172:1277-285 CrossRef
10. Dalle-Donne I, Rossi R, Milzani A, Di Simplicio P, Colombo R (2001) The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radic Biol Med 31:1624-632 CrossRef
11. Damerval C, Maurice A, Josse JM, De Vienne D (1994) Quantitative trait loci underlying gene product variation: a novel perspective for analyzing regulation of genome expression. Genetics 137:289-01
12. Davidson SM, Loones MT, Duverger O, Morange M (2002) The developmental expression of small HSP. Prog Mol Subcell Biol 28:103-28
13. Day T, Greenfield SA (2003) A peptide derived from acetylcholinesterase induces neuronal cell death: characterisation of possible mechanisms. Exp Brain Res 153:334-42 CrossRef
14. Decook R, Lall S, Nettleton D, Howell SH (2005) Genetic regulation of gene expression during shoot development in Arabidopsis. Genetics 172:1155-164 CrossRef
15. Dixon AL, Liang L, Moffatt MF, Chen W, Heath S, Wong KC, Taylor J, Burnett E, Gut I, Farrall M, Lathrop GM, Abecasis GR, Cookson WO (2007) A genome-wide association study of global gene expression. Nat Genet 39:1202-207 CrossRef
16. Druka A, Kudrna D, Han F, Kilian A, Steffenson B, Frisch D, Tomkins J, Wing R, Kleinhofs A (2000) Physical mapping of the barley stem rust resistance gene / rpg4. Mol Gen Genet 264:283-90 CrossRef
17. Druka A, Rostoks N, Whitelaw C, Brueggeman R, Zhang L, Kleinhofs A (2004) Comparative sequence analysis of the barley chromosome 7 (5HL) / rpg4 region and a syntenous rice chromosome 3 region. Plant and animal genomes XII conference, p 344. http://www.intl-pag.org/12/abstracts/P5a_PAG12_344.html
18. Druka A, Muehlbauer G, Druka I, Caldo R, Baumann U, Rostoks N, Schreiber A, Wise R, Close T, Kleinhofs A, Graner A, Schulman A, Langridge P, Sato K, Hayes P, McNicol J, Marshall D, Waugh R (2006) An atlas of gene expression from seed to seed through barley development. Funct Integr Genomics 6:202-11 CrossRef
19. Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971-974 CrossRef
20. de Haan G, Gerrits A, Bystrykh L (2006) Modern genome-wide genetic approaches to reveal intrinsic properties of stem cells. Curr Opin Hematol 13:249-53 CrossRef
21. Haussuhl K, Andersson B, Adamska I (2001) A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO J 20:713-22 j/20.4.713">CrossRef
22. Hayes P, Szucs P (2006) Disequilibrium and association in barley: thinking outside the glass. Proc Natl Acad Sci USA 103:18385-8386 CrossRef
23. 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 100:364-69 CrossRef
24. Hu G, Yalpani N, Briggs SP, Johal GS (1998) A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10:1095-105 CrossRef
25. Hubner N, Wallace CA, Zimdahl H, Petretto E, Schulz H, Maciver F, Mueller M, Hummel O, Monti J, Zidek V, Musilova A, Kren V, Causton H, Game L, Born G, Schmidt S, Muller A, Cook SA, Kurtz TW, Whittaker J, Pravenec M, Aitman TJ (2005) Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat Genet 37:243-53 CrossRef
26. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15 CrossRef
27. Jordan MC, Somers DJ, Banks TW (2007) Identifying regions of the wheat genome controlling seed development by mapping expression quantitative trait loci. Plant Biotechnol J 5:442-53 j.1467-7652.2007.00253.x">CrossRef
28. Jung YH, Rakwal R, Agrawal GK, Shibato J, Kim JA, Lee MO, Choi PK, Jung SH, Kim SH, Koh HJ, Yonekura M, Iwahashi H, Jwa NS (2006) Differential expression of defense/stress-related marker proteins in leaves of a unique rice blast lesion mimic mutant ( / blm). J Proteome Res 5:2586-598 CrossRef
29. Kelleher DJ, Gilmore R (1997) DAD1, the defender against apoptotic cell death, is a subunit of the mammalian oligosaccharyltransferase. Proc Natl Acad Sci USA 94:4994-999 CrossRef
30. Kerns RT, Ravindranathan A, Hassan S, Cage MP, York T, Sikela JM, Williams RW, Miles MF (2005) Ethanol-responsive brain region expression networks: implications for behavioral responses to acute ethanol in DBA/2J versus C57BL/6J mice. J Neurosci 25:2255-266 CrossRef
31. Kilian A, Kudrna DA, Kleinhofs A, Yano M, Kurata N, Steffenson B, Sasaki T (1995) Rice–barley synteny and its application to saturation mapping of the barley / Rpg1 region. Nucleic Acids Res 23:2729-733 CrossRef
32. Kilian A, Chen J, Han F, Steffenson B, Kleinhofs A (1997) Towards map-based cloning of the barley stem rust resistance genes / Rpg1 and / rpg4 using rice as an intergenomic cloning vehicle. Plant Mol Biol 35:187-95 CrossRef
33. Kirst M, Basten CJ, Myburg AA, Zeng ZB, Sederoff RR (2005) Genetic architecture of transcript-level variation in differentiating xylem of a eucalyptus hybrid. Genetics 169:2295-303 CrossRef
34. Kleinhofs A, Graner A (2001) An integrated map of the barley genome. In: Phillips R, Vasil I (eds) DNA-based markers in plants. Kluwer, Dordrecht, pp 187-99
35. Kleinhofs A, Kilian A, Saghai Maroof MA, Biyashev RM, Hayes P, Chen FQ, Lapitan N, Fenwick A, Blake TK, Kanazin V, Ananiev E, Dahleen L, Kudrna D, Bollinger J, Knapp SJ, Liu B, Sorrells M, Heun M, Franckowiak JD, Hoffman D, Skadsen R, Steffenson BJ (1993) A molecular, isozyme and morphological map of the barley ( / Hordeum vulgare) genome. Theor Appl Genet 86:705-12 CrossRef
36. Kliebenstein DJ, West MA, van Leeuwen H, Loudet O, Doerge RW, St Clair DA (2006) Identification of QTLs controlling gene expression networks defined a priori. BMC Bioinformatics 7:308 CrossRef
37. Kolmer JA (2005) Tracking wheat rust on a continental scale. Curr Opin Plant Biol 8:441-49 j.pbi.2005.05.001">CrossRef
38. Liang P, MacRae TH (1997) Molecular chaperones and the cytoskeleton. J Cell Sci 110(Pt 13):1431-440
39. Luo ZW, Potokina E, Druka A, Wise R, Waugh R, Kearsey M (2007) SFP genotyping from Affymetrix arrays is robust but largely detects / cis-acting expression regulators. Genetics 176:789-00 CrossRef
40. Manly KF, Olson JM (1999) Overview of QTL mapping software and introduction to map manager QT. Mamm Genome 10:327-34 CrossRef
41. Mariappan D, Winkler J, Parthiban V, Doss MX, Hescheler J, Sachinidis A (2006) Dietary small molecules and large-scale gene expression studies: an experimental approach for understanding their beneficial effects on the development of malignant and non-malignant proliferative diseases. Curr Med Chem 13:1481-489 CrossRef
42. Matthews DB, Bhave SV, Belknap JK, Brittingham C, Chesler EJ, Hitzemann RJ, Hoffmann PL, Lu L, McWeeney S, Miles MF, Tabakoff B, Williams RW (2005) Complex genetics of interactions of alcohol and CNS function and behaviour. Alcohol Clin Exp Res 29:1706-719 CrossRef
43. Miklis M, Consonni C, Bhat RA, Lipka V, Schulze-Lefert P, Panstruga R (2007) Barley MLO modulates actin-dependent and actin-independent antifungal defense pathways at the cell periphery. Plant Physiol 144:1132-143 CrossRef
44. Miller JD, Lambert JW (1965) Variability and inheritance of reaction of barley to race l5B of stem rust. Aqron J 47:373-77
45. Molina A, Volrath S, Guyer D, Maleck K, Ryals J, Ward E (1999) Inhibition of protoporphyrinogen oxidase expression in / Arabidopsis causes a lesion-mimic phenotype that induces systemic acquired resistance. Plant J 17:667-78 j.1365-313X.1999.00420.x">CrossRef
46. Mounier N, Arrigo AP (2002) Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones 7:167-76 CrossRef
47. Nakashima T, Sekiguchi T, Kuraoka A, Fukushima K, Shibata Y, Komiyama S, Nishimoto T (1993) Molecular cloning of a human cDNA encoding a novel protein, DAD1, whose defect causes apoptotic cell death in hamster BHK21 cells. Mol Cell Biol 13:6367-374
48. Nirmala J, Brueggeman R, Maier C, Clay C, Rostoks N, Kannangara CG, von Wettstein D, Steffenson BJ, Kleinhofs A (2006) Subcellular localization and functions of the barley stem rust resistance receptor-like serine/threonine-specific protein kinase Rpg1. Proc Natl Acad Sci USA 103:7518-523 CrossRef
49. Nishii K, Tsuzuki T, Kumai M, Takeda N, Koga H, Aizawa S, Nishimoto T, Shibata Y (1999) Abnormalities of developmental cell death in / Dad1-deficient mice. Genes Cells 4:243-52 j.1365-2443.1999.00256.x">CrossRef
50. Noutoshi Y, Kuromori T, Wada T, Hirayama T, Kamiya A, Imura Y, Yasuda M, Nakashita H, Shirasu K, Shinozaki K (2006) Loss of necrotic spotted lesions 1 associates with cell death and defense responses in / Arabidopsis thaliana. Plant Mol Biol 62:29-2 CrossRef
51. Orrenius S, Nicotera P (1994) The calcium ion and cell death. J Neural Transm Suppl 43:1-1
52. Orvar BL, Sangwan V, Omann F, Dhindsa RS (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23:785-94 j.1365-313x.2000.00845.x">CrossRef
53. Ouellet F, Carpentier E, Cope MJ, Monroy AF, Sarhan F (2001) Regulation of a wheat actin-depolymerizing factor during cold acclimation. Plant Physiol 125:360-68 CrossRef
54. Parkinson H, Sarkans U, Shojatalab M, Abeygunawardena N, Contrino S, Coulson R, Farne A, Lara GG, Holloway E, Kapushesky M, Lilja P, Mukherjee G, Oezcimen A, Rayner T, Rocca-Serra P, Sharma A, Sansone S, Brazma A (2005) ArrayExpress—a public repository for microarray gene expression data at the EBI. Nucleic Acids Res 33:D553–D555 CrossRef
55. Potokina E, Druka A, Luo ZW, Wise R, Waugh R, Kearsey M (2007) eQTL analysis of 16,000 barley genes reveals a complex pattern of genome wide transcriptional regulation. Plant J (in press)
56. Rostoks N, Schmierer D, Kudrna D, Kleinhofs A (2003) Barley putative hypersensitive induced reaction genes: genetic mapping, sequence analyses and differential expression in disease lesion mimic mutants. Theor Appl Genet 107:1094-101 CrossRef
57. Rostoks N, Ramsay L, MacKenzie K, Cardle L, Bhat PR, Roose ML, Svensson JT, Stein N, Varshney RK, Marshall DF, Graner A, Close TJ, Waugh R (2006a) Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties. Proc Natl Acad Sci USA 103:18656-8661 CrossRef
58. Rostoks N, Schmierer D, Mudie S, Drader T, Brueggeman R, Caldwell DG, Waugh R, Kleinhofs A (2006b) Barley necrotic locus nec1 encodes the cyclic nucleotide-gated ion channel 4 homologous to the Arabidopsis HLM1. Mol Genet Genomics 275:159-68 CrossRef
59. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-86
60. Schadt EE, Lamb J, Yang X, Zhu J, Edwards S, Guhathakurta D, Sieberts SK, Monks S, Reitman M, Zhang C, Lum PY, Leonardson A, Thieringer R, Metzger JM, Yang L, Castle J, Zhu H, Kash SF, Drake TA, Sachs A, Lusis AJ (2005) An integrative genomics approach to infer causal associations between gene expression and disease. Nat Genet 37:710-17 CrossRef
61. Schulze-Lefert P, Panstruga R (2003) Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu Rev Phytopathol 41:641-67 CrossRef
62. Shi C, Uzarowska A, Ouzunova M, Landbeck M, Wenzel G, Lubberstedt T (2007) Identification of candidate genes associated with cell wall digestibility and eQTL (expression quantitative trait loci) analysis in a Flint?×?Flint maize recombinant inbred line population. BMC Genomics 8:22 CrossRef
63. Shirasu K, Lahaye T, Tan MW, Zhou F, Azevedo C, Schulze-Lefert P (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in / C. elegans. Cell 99:355-66 CrossRef
64. Stakman EC, Stewart DM, Loegering WQ (1962) Identification of physiologic races of / Puccinia graminis var. / tritici. USDA Agricultural Research Service Bulletin. Vol 617
65. Steffenson BJ, Miller JD, Jin Y (1993) Detection of stem rust resistance gene / Rpg1 in barley seedlings. Plant Dis 77:626-29
66. Street NR, Skogstrom O, Sjodin A, Tucker J, Rodriguez-Acosta M, Nilsson P, Jansson S, Taylor G (2006) The genetics and genomics of the drought response in Populus. Plant J 48:321-41 j.1365-313X.2006.02864.x">CrossRef
67. Wang S, Basten CJ, Zeng Z-B (2007) Windows QTL Cartographer 2.5. Dept of Statistics, North Carolina State University, Raleigh, NC. (http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)
68. Welsh MJ, Gaestel M (1998) Small heat-shock protein family: function in health and disease. Ann NY Acad Sci 851:28-5 j.1749-6632.1998.tb08973.x">CrossRef
69. West MA, Kim K, Kliebenstein DJ, van Leeuwen H, Michelmore RW, Doerge RW, St Clair DA (2007) Global eQTL mapping reveals the complex genetic architecture of transcript-level variation in / Arabidopsis. Genetics 175:1441-450 CrossRef
70. Whitham SA, Anderberg RJ, Chisholm ST, Carrington JC (2000) Arabidopsis RTM2 gene is necessary for specific restriction of tobacco etch virus and encodes an unusual small heat shock-like protein. Plant Cell 12:569-82 CrossRef
71. Wray GA (2007) The evolutionary significance of / cis-regulatory mutations. Nat Rev Genet 8:206-16 CrossRef
72. Xu W, Stamnes M (2006) The actin-depolymerizing factor homology and charged/helical domains of drebrin and / mAbp1 direct membrane binding and localization via distinct interactions with actin. J Biol Chem 281:11826-1833 jbc.M510141200">CrossRef
73. Yaguchi H, Togawa K, Moritani M, Itakura M (2005) Identification of candidate genes in the type 2 diabetes modifier locus using expression QTL. Genomics 85:591-99 j.ygeno.2005.01.006">CrossRef
74. Yamada T, Takatsu Y, Kasumi M, Marubashi W, Ichimura K (2004) A homolog of the defender against apoptotic death gene (DAD1) in senescing gladiolus petals is down-regulated prior to the onset of programmed cell death. J Plant Physiol 161:1281-283 j.jplph.2004.06.005">CrossRef
75. Yulug IG, See CG, Fisher EM, Ylug IG (1995) The DAD1 protein, whose defect causes apoptotic cell death, maps to human chromosome 14. Genomics 26:433-35 CrossRef
76. Zhang L, Fetch T, Nirmala J, Schmierer D, Brueggeman R, Steffenson B, Kleinhofs A (2006) / Rpr1, a gene required for / Rpg1-dependent resistance to stem rust in barley. Theor Appl Genet 113:847-55 CrossRef
77. Zhou F, Kurth J, Wei F, Elliott C, Vale G, Yahiaoui N, Keller B, Somerville S, Wise R, Schulze-Lefert P (2001) Cell-autonomous expression of barley / Mla1 confers race-specific resistance to the powdery mildew fungus via a / Rar1-independent signaling pathway. Plant Cell 13:337-50 CrossRef - 作者单位：Arnis Druka (1)
Elena Potokina (2)
Zewei Luo (2)
Nicola Bonar (1)
Ilze Druka (1) (3)
Ling Zhang (4)
David F. Marshall (1)
Brian J. Steffenson (5)
Timothy J. Close (6)
Roger P. Wise (7)
Andris Kleinhofs (4)
Robert W. Williams (8)
Michael J. Kearsey (2)
Robbie Waugh (1)
1. Genetics Programme, Scottish Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK
2. School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK
3. School of Computing and Creative Technologies, University of Abertay, Dundee, DD1 1HG, UK
4. Department of Crop and Soil Sciences, Washington State University, Pullman, WA, 99164, USA
5. Department of Plant Pathology, University of Minnesota, St Paul, MN, 55108, USA
6. Department of Botany and Plant Sciences, University of California, Riverside, CA, 92521, USA
7. Corn Insects and Crop Genetics Research, USDA-ARS and Department of Plant Pathology, Iowa State University, Ames, IA, 50011, USA
8. Department of Anatomy and Neurobiology, University of Tennessee, Memphis, TN, 38163, USA - ISSN：1432-2242
文摘
We previously mapped mRNA transcript abundance traits (expression-QTL or eQTL) using the Barley1 Affymetrix array and ‘whole plant-tissue from 139 progeny of the Steptoe?×?Morex (St/Mx) reference barley mapping population. Of the 22,840 probesets (genes) on the array, 15,987 reported transcript abundance signals that were suitable for eQTL analysis, and this revealed a genome-wide distribution of 23,738 significant eQTLs. Here we have explored the potential of using these mRNA abundance eQTL traits as surrogates for the identification of candidate genes underlying the interaction between barley and the wheat stem rust fungus Puccinia graminis f. sp. tritici. We re-analysed quantitative ‘resistance phenotype-data collected on this population in 1990/1991 and identified six loci associated with barley’s reaction to stem rust. One of these coincided with the major stem rust resistance locus Rpg1, that we had previously positionally cloned using this population. Correlation analysis between phenotype values for rust infection and mRNA abundance values reported by the 22,840 GeneChip probe sets placed Rpg1, which is on the Barley1 GeneChip, in the top five candidate genes for the major QTL on chromosome 7H corresponding to the location of Rpg1. A second co-located with the rpg4/Rpg5 stem rust resistance locus that has been mapped in a different population and the remaining four were novel. Correlation analyses identified candidate genes for the rpg4/Rpg5 locus on chromosome 5H. By combining our data with additional published mRNA profiling data sets, we identify a putative sensory transduction histidine kinase as a strong candidate for a novel resistance locus on chromosome 2H and compile candidate gene lists for the other three loci.