Quantitative and Qualitative Stem Rust Resistance Factors in Barley Are Associated with Transcriptional Suppression of Defense Regulons

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Stem rust (Puccinia graminis f. sp. tritici; Pgt) is a devastating fungal disease of wheat and barley. Pgt race TTKSK (isolate Ug99) is a serious threat to these Triticeae grain crops because resistance is rare. In barley, the complex Rpg-TTKSK locus on chromosome 5H is presently the only known source of qualitative resistance to this aggressive Pgt race. Segregation for resistance observed on seedlings of the Q21861 × SM89010 (QSM) doubled-haploid (DH) population was found to be predominantly qualitative, with little of the remaining variance explained by loci other than Rpg-TTKSK. In contrast, analysis of adult QSM DH plants infected by field inoculum of Pgt race TTKSK in Njoro, Kenya, revealed several additional quantitative trait loci that contribute to resistance. To molecularly characterize these loci, Barley1 GeneChips were used to measure the expression of 22,792 genes in the QSM population after inoculation with Pgt race TTKSK or mock-inoculation. Comparison of expression Quantitative Trait Loci (eQTL) between treatments revealed an inoculation-dependent expression polymorphism implicating Actin depolymerizing factor3 (within the Rpg-TTKSK locus) as a candidate susceptibility gene. In parallel, we identified a chromosome 2H trans-eQTL hotspot that co-segregates with an enhancer of Rpg-TTKSK-mediated, adult plant resistance discovered through the Njoro field trials. Our genome-wide eQTL studies demonstrate that transcript accumulation of 25% of barley genes is altered following challenge by Pgt race TTKSK, but that few of these genes are regulated by the qualitative Rpg-TTKSK on chromosome 5H. It is instead the chromosome 2H trans-eQTL hotspot that orchestrates the largest inoculation-specific responses, where enhanced resistance is associated with transcriptional suppression of hundreds of genes scattered throughout the genome. Hence, the present study associates the early suppression of genes expressed in this host–pathogen interaction with enhancement of R-gene mediated resistance.

Vyšlo v časopise: Quantitative and Qualitative Stem Rust Resistance Factors in Barley Are Associated with Transcriptional Suppression of Defense Regulons. PLoS Genet 7(7): e32767. doi:10.1371/journal.pgen.1002208
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002208

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Zdroje

1. JonesJDDanglJL 2006 The plant immune system. Nature 444 323 329

2. BentAFMackeyD 2007 Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45 399 436

3. FlorH 1955 Host-parasite interaction in flax rust-its genetics and other implications. Phytopathology 45 680 685

4. GarcíaAVParkerJE 2009 Heaven's Gate: nuclear accessibility and activities of plant immune regulators. Trends Plant Sci 14 479 487

5. StewartRRobertsonW 1968 Fungus spores from prehistoric potsherds. Mycologia 60 701 704

6. KislevME 1982 Stem rust of wheat 3300 years old found in Israel. Science 216 993 994

7. PetersonP 2001 Stem rust of wheat: Exploring the concepts. PetersonP Stem rust of wheat: From ancient enemy to modern foe St. Paul, Minnesota The American Phytopathological Society 1 15

8. LeonardK 2001 Stem rust - Future enemy? PetersonP Stem rust of wheat: From ancient enemy to modern foe St. Paul, Minnesota The American Phytopathological Society 119 146

9. LeonardKSzaboL 2005 Stem rust of small grains and grasses caused by Puccinia graminis. Mol Plant Pathol 6 99 111

10. LinKBushnellWSmithASzaboL 1998 Temporal accumulation patterns of defence response gene transcripts in relation to resistant reactions in oat inoculated with Puccinia graminis. Physiol Mol Plant Pathol 52 95 114

11. SellamMWilcoxsonR 1976 Development of Puccinia graminis f. sp. tritici on resistant and susceptible barley cultivars. Phytopathology 66 667 668

12. SteffensonBJJinYBrueggemanRSKleinhofsASunY 2009 Resistance to stem rust race TTKSK maps to the rpg4/Rpg5 complex of chromosome 5H of barley. Phytopathology 99 1135 1141

13. PretoriusZASinghRPWagoireWWPayneTS 2000 Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis 84 203 203

14. SinghRHodsonDJinYHuerta-EspinoJKinyuaM 2006 Current status, likely migration and strategies to mitigate the threat to wheat production from race Ug99 (TTKS) of stem rust pathogen. CAB Reviews 1 1 13

15. SinghRHodsonDHuerta-EspinoJJinYNjauP 2008 Will stem rust destroy the world's wheat crop? Advances in Agronomy 98 271 309

16. BrueggemanRDrukaANirmalaJCavileerTDraderT 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

17. BrueggemanRSteffensonBJKleinhofsA 2009 The rpg4/Rpg5 stem rust resistance locus in barley: resistance genes and cytoskeleton dynamics. Cell Cycle 8 977 981

18. KliebensteinD 2009 Quantitative genomics: analyzing intraspecific variation using global gene expression polymorphisms or eQTLs. Annu Rev Plant Biol 60 93 114

19. DamervalCMauriceAJosseJMde VienneD 1994 Quantitative trait loci underlying gene product variation: a novel perspective for analyzing regulation of genome expression. Genetics 137 289 301

20. JansenRCNapJP 2001 Genetical genomics: the added value from segregation. Trends Genet 17 388 391

21. BremRBYvertGClintonRKruglyakL 2002 Genetic dissection of transcriptional regulation in budding yeast. Science 296 752 755

22. SchadtEEMonksSADrakeTALusisAJCheN 2003 Genetics of gene expression surveyed in maize, mouse and man. Nature 422 297 302

23. MorleyMMolonyCMWeberTMDevlinJLEwensKG 2004 Genetic analysis of genome-wide variation in human gene expression. Nature 430 743 747

24. HansenBGHalkierBAKliebensteinDJ 2008 Identifying the molecular basis of QTLs: eQTLs add a new dimension. Trends Plant Sci 13 72 77

25. WentzellAMRoweHCHansenBGTicconiCHalkierBA 2007 Linking metabolic QTLs with network and cis-eQTLs controlling biosynthetic pathways. PLoS Genet 3 e162. doi:10.1371/journal.pgen.0030162

26. SteffensonBJJinYRossnagelBGRasmussenJBKaoK 1995 Genetics of multiple disease resistance in a doubled-haploid population of barley. Plant Breeding 114 50 54

27. MillerJLambertJ 1955 Variability and inheritance of reaction of barley to race 15B of stem rust. Agron J 47 373 377

28. StakmanEStewartDLoegeringW 1962 Identification of physiological races of Puccinia graminis f.sp. tritici. US Dept Agric Agric Res Serv: Publ. no. E617

29. SunYSteffensonB 2005 Reaction of barley seedlings with different stem rust resistance genes to Puccinia graminis f. sp. tritici and Puccinia graminis f. sp. secalis. Can J Plant Pathol 27 80 89

30. DrukaAPotokinaELuoZBonarNDrukaI 2008 Exploiting regulatory variation to identify genes underlying quantitative resistance to the wheat stem rust pathogen Puccinia graminis f. sp. tritici in barley. Theor Appl Genet 117 261 272

31. ZhangLCastell-MillerCDahlSSteffensonBKleinhofsA 2008 Parallel expression profiling of barley-stem rust interactions. Funct Integr Genomics 8 187 198

32. CloseTJWanamakerSICaldoRATurnerSMAshlockDA 2004 A new resource for cereal genomics: 22K barley GeneChip comes of age. Plant Physiol 134 960 968

33. NettletonDHwangJCaldoRWiseR 2006 Estimating the number of true null hypotheses from a histogram of p-values. J Agricult Biol Env Stat 11 337 356

34. TaoYXieZChenWGlazebrookJChangHS 2003 Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15 317 330

35. CaldoRANettletonDWiseRP 2004 Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. Plant Cell 16 2514 2528

36. MoscouMJLauterNCaldoRANettletonDWiseRP 2011 Quantitative and temporal definition of the Mla transcriptional regulon during barley-powdery mildew interactions. Mol Plant-Microbe Interact 24 694 705

37. WiseRPMoscouMJBogdanoveAJWhithamSA 2007 Transcript profiling in host-pathogen interactions. Annu Rev Phytopathol 45 329 369

38. ZhouLMiderosSXBaoLHanlonRArredondoFD 2009 Infection and genotype remodel the entire soybean transcriptome. BMC Genomics 10 49

39. BastenCWeirBZengZ 2004 QTL Cartographer, Version 1.17f. Department of Statistics, North Carolina State University, Raleigh, NC

40. ZengZB 1994 Precision mapping of quantitative trait loci. Genetics 136 1457 1468

41. ChurchillGADoergeRW 1994 Empirical threshold values for quantitative trait mapping. Genetics 138 963 971

42. LauterNMoscouMJHabigerJMooseSP 2008 Quantitative genetic dissection of shoot architecture traits in maize: Towards a functional genomics approach. Plant Genome 1 99 110

43. WestMAKimKKliebensteinDJvan LeeuwenHMichelmoreRW 2007 Global eQTL mapping reveals the complex genetic architecture of transcript-level variation in Arabidopsis. Genetics 175 1441 1450

44. CloseTJBhatPRLonardiSWuYRostoksN 2009 Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10 582

45. SchulteDCloseTJGranerALangridgePMatsumotoT 2009 The international barley sequencing consortium—at the threshold of efficient access to the barley genome. Plant Physiol 149 142 147

46. PotokinaEDrukaALuoZWiseRWaughR 2008 Gene expression quantitative trait locus analysis of 16 000 barley genes reveals a complex pattern of genome-wide transcriptional regulation. Plant J 53 90 101

47. SchwessingerBZipfelC 2008 News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11 389 395

48. SvenssonJTCrosattiCCampoliCBassiRStancaAM 2006 Transcriptome analysis of cold acclimation in barley albina and xantha mutants. Plant Physiol 141 257 270

49. WaliaHWilsonCWahidACondaminePCuiX 2006 Expression analysis of barley (Hordeum vulgare L.) during salinity stress. Funct Integr Genomics 6 143 156

50. AbebeTWiseRPSkadsenRW 2009 Comparative transcriptional profiling established the awn as the major photosynthetic organ of the barley spike while the lemma and the palea primarily protect the seed. Plant Genome 2 247 259

51. ChenXHackettCANiksREHedleyPEBoothC 2010 An eQTL analysis of partial resistance to Puccinia hordei in barley. PLoS ONE 5 e8598 doi:10.1371/journal.pone.0008598

52. ZhouXSuZ 2007 EasyGO: Gene Ontology-based annotation and functional enrichment analysis tool for agronomical species. BMC Genomics 8 246

53. MatsumuraHReichSItoASaitohHKamounS 2003 Gene expression analysis of plant host-pathogen interactions by SuperSAGE. Proc Natl Acad Sci USA 100 15718 15723

54. MysoreKSD'AscenzoMDHeXMartinGB 2003 Overexpression of the disease resistance gene Pto in tomato induces gene expression changes similar to immune responses in human and fruitfly. Plant Physiol 132 1901 1912

55. ZimmerliLSteinMLipkaVSchulze-LefertPSomervilleS 2004 Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J 40 633 646

56. de KoningDJHaleyCS 2005 Genetical genomics in humans and model organisms. Trends Genet 21 377 381

57. RockmanMVKruglyakL 2006 Genetics of global gene expression. Nat Rev Genet 7 862 872

58. KerwinREJimenez-GomezJMFulopDHarmerSLMaloofJN 2011 Network quantitative trait loci mapping of circadian clock outputs identifies metabolic pathway-to-clock linkages in Arabidopsis. Plant Cell 23 471 485

59. PotokinaEDrukaALuoZMoscouMWiseR 2008 Tissue-dependent limited pleiotropy affects gene expression in barley. Plant J 56 287 296

60. ChenXNiksREHedleyPEMorrisJDrukaA 2010 Differential gene expression in nearly isogenic lines with QTL for partial resistance to Puccinia hordei in barley. BMC Genomics 11 629

61. LiYÁlvarezOAGuttelingEWTijstermanMFuJ 2006 Mapping determinants of gene expression plasticity by genetical genomics in C. elegans. PLoS Genet 2 e222 doi:10.1371/journal.pgen.0020222

62. SmithENKruglyakL 2008 Gene-environment interaction in yeast gene expression. PLoS Biol 6 e83 doi:10.1371/journal.pbio.0060083

63. CarlierMFLaurentVSantoliniJMelkiRDidryD 1997 Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol 136 1307 1322

64. MiklisMConsonniCBhatRALipkaVSchulze-LefertP 2007 Barley MLO modulates actin-dependent and actin-independent antifungal defense pathways at the cell periphery. Plant Physiol 144 1132 1143

65. HückelhovenR 2007 Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45 101 127

66. MozhuiKCiobanuDCSchikorskiTWangXLuL 2008 Dissection of a QTL hotspot on mouse distal chromosome 1 that modulates neurobehavioral phenotypes and gene expression. PLoS Genet 4 e1000260 doi:10.1371/journal.pgen.1000260

67. DrukaAPotokinaELuoZJiangNChenX 2010 Expression quantitative trait loci analysis in plants. Plant Biotechnol J 8 10 27

68. BrueggemanRRostoksNKudrnaDKilianAHanF 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

69. ZhangLFetchTNirmalaJSchmiererDBrueggemanR 2006 Rpr1, a gene required for Rpg1-dependent resistance to stem rust in barley. Theor Appl Genet 113 847 855

70. SpoelSHKoornneefAClaessensSMKorzeliusJPVan PeltJA 2003 NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15 760 770

71. UppalapatiSRAyoubiPWengHPalmerDAMitchellRE 2005 The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J 42 201 217

72. ThilmonyRUnderwoodWHeSY 2006 Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 46 34 53

73. RömerPHahnSJordanTStraußTBonasU 2007 Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318 645 648

74. KaySHahnSMaroisEHauseGBonasU 2007 A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318 648 651

75. MoscouMJBogdanoveAJ 2009 A simple cipher governs DNA recognition by TAL effectors. Science 326 1501

76. BochJScholzeHSchornackSLandgrafAHahnS 2009 Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326 1509 1512

77. BorovkovaIGSteffensonBJJinYRasmussenJBKilianA 1995 Identification of molecular markers linked to the stem rust resistance gene rpg4 in barley. Phytopathology 85 181 185

78. LargeE 1954 Growth stages in cereals: Illustration of the Feeke's scale. Plant Pathol 3 128 129

79. ZadoksJChangTKonzakC 1974 A decimal code for the growth stages of cereals. Weed Res 14 415 421

80. WestMAvan LeeuwenHKozikAKliebensteinDJDoergeRW 2006 High-density haplotyping with microarray-based expression and single feature polymorphism markers in Arabidopsis. Genome Res 16 787 795

81. MosigMOLipkinEKhutoreskayaGTchourzynaESollerM 2001 A whole genome scan for quantitative trait loci affecting milk protein percentage in Israeli-Holstein cattle, by means of selective milk DNA pooling in a daughter design, using an adjusted false discovery rate criterion. Genetics 157 1683 1698

82. WangJWilliamsRWManlyKF 2003 WebQTL: web-based complex trait analysis. Neuroinformatics 1 299 308