Towards Establishment of a Rice Stress Response Interactome

English version České info

Rice (Oryza sativa) is a staple food for more than half the world and a model for studies of monocotyledonous species, which include cereal crops and candidate bioenergy grasses. A major limitation of crop production is imposed by a suite of abiotic and biotic stresses resulting in 30%–60% yield losses globally each year. To elucidate stress response signaling networks, we constructed an interactome of 100 proteins by yeast two-hybrid (Y2H) assays around key regulators of the rice biotic and abiotic stress responses. We validated the interactome using protein–protein interaction (PPI) assays, co-expression of transcripts, and phenotypic analyses. Using this interactome-guided prediction and phenotype validation, we identified ten novel regulators of stress tolerance, including two from protein classes not previously known to function in stress responses. Several lines of evidence support cross-talk between biotic and abiotic stress responses. The combination of focused interactome and systems analyses described here represents significant progress toward elucidating the molecular basis of traits of agronomic importance.

Vyšlo v časopise: Towards Establishment of a Rice Stress Response Interactome. PLoS Genet 7(4): e32767. doi:10.1371/journal.pgen.1002020
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002020

Souhrn

Zdroje

1. DhlaminiZSpillaneCMossJPRuaneJUrquiaN 2005 Status of Research and Application of Crop Biotechnologies in Developing Countries. Rome, Italy Food and Agriculture Oganization of the United Nations Natural Resources Management and Environment Department

2. FujitaMFujitaYNoutoshiYTakahashiFNarusakaY 2006 Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9 436 442

3. RualJFVenkatesanKHaoTHirozane-KishikawaTDricotA 2005 Towards a proteome-scale map of the human protein-protein interaction network. Nature 437 1173 1178

4. SongWYWangGLChenLLKimHSPiLY 1995 A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270 1804 1806

5. ChernMFitzgeraldHACanlasPENavarreDARonaldPC 2005 Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant Microbe Interact 18 511 520

6. DurrantWEDongX 2004 Systemic acquired resistance. Annu Rev Phytopathol 42 185 209

7. XuKXuXFukaoTCanlasPMaghirang-RodriguezR 2006 Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442 705 708

8. LeeSWHanSWSririyanumMParkCJSeoYS 2009 A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 326 850 853

9. RonaldPCBeutlerB 2010 Plant and animal host sensors of conserved microbial signatures. Science In Press

10. ShimonoMSuganoSNakayamaAJiangCJOnoK 2007 Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19 2064 2076

11. Bracha-DroriKShichrurKKatzAOlivaMAngeloviciR 2004 Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J 40 419 427

12. GrefenCLalondeSObrdlikP 2007 Split-ubiquitin system for identifying protein-protein interactions in membrane and full-length proteins. Curr Protoc Neurosci Chapter 5 Unit 5 27

13. ParkCJPengYChenXDardickCRuanD 2008 Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biol 6 e231 doi:10.1371/journal.pbio.0060231

14. DingXRichterTChenMFujiiHSeoYS 2009 A rice kinase-protein interaction map. Plant Physiol 149 1478 1492

15. NakashimaAChenLThaoNPFujiwaraMWongHL 2008 RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex. Plant Cell 20 2265 2279

16. ThaoNPChenLNakashimaAHaraSUmemuraK 2007 RAR1 and HSP90 form a complex with Rac/Rop GTPase and function in innate-immune responses in rice. Plant Cell 19 4035 4045

17. WongHLPinontoanRHayashiKTabataRYaenoT 2007 Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19 4022 4034

18. CheongYHMoonBCKimJKKimCYKimMC 2003 BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol 132 1961 1972

19. ZhuSTytgatJ 2004 Evolutionary epitopes of Hsp90 and p23: implications for their interaction. FASEB J 18 940 947

20. ShirasuK 2009 The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60 139 164

21. ChernMCanlasPEFitzgeraldHARonaldPC 2005 Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1. Plant J 43 623 635

22. StoreyJDTibshiraniR 2003 Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100 9440 9445

23. JeongHMasonSPBarabasiALOltvaiZN 2001 Lethality and centrality in protein networks. Nature 411 41 42

24. GandhiTKZhongJMathivananSKarthickLChandrikaKN 2006 Analysis of the human protein interactome and comparison with yeast, worm and fly interaction datasets. Nat Genet 38 285 293

25. ParkCJHanSWChenXRonaldPC 2010 Elucidation of XA21-mediated innate immunity. Cell Microbiol 12 1017 1025

26. de FolterSImminkRGKiefferMParenicovaLHenzSR 2005 Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17 1424 1433

27. WangYSPiLYChenXChakrabartyPKJiangJ 2006 Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18 3635 3646

28. PengYBartleyLEChenXDardickCChernM 2008 OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant 1 446 458

29. ChenXChernMCanlasPERuanDJiangC 2010 An ATPase promotes autophosphorylation of the pattern recognition receptor XA21 and inhibits XA21-mediated immunity. Proc Natl Acad Sci U S A 107 8029 8034

30. HeXZhangJ 2006 Why do hubs tend to be essential in protein networks? PLoS Genet 2 e88 doi:10.1371/journal.pgen.0020088

31. LuscombeNMBabuMMYuHSnyderMTeichmannSA 2004 Genomic analysis of regulatory network dynamics reveals large topological changes. Nature 431 308 312

32. JungKHSeoYSWaliaHCaoPFukaoT 2010 The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors. Plant Physiol 152 1674 1692

33. SanaTRFischerSWohlgemuthGKatrekarAJungKH 2010 Metabolomic and transcriptomic analysis of the rice response to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae. Metabolomics 6 451 465

34. KadotaYShirasuKGueroisR 2010 NLR sensors meet at the SGT1-HSP90 crossroad. Trends Biochem Sci 35 199 207

35. ShangYLiXCuiHHePThilmonyR 2006 RAR1, a central player in plant immunity, is targeted by Pseudomonas syringae effector AvrB. Proc Natl Acad Sci U S A 103 19200 19205

36. ChenLHamadaSFujiwaraMZhuTThaoNP 2010 The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host Microbe 7 185 196

37. BrutusASiciliaFMaconeACervoneFDe LorenzoG 2010 A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci U S A 107 9452 9457

38. ChinchillaDZipfelCRobatzekSKemmerlingBNurnbergerT 2007 A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448 497 500

39. XiongLYangY 2003 Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15 745 759

40. AsaiTTenaGPlotnikovaJWillmannMRChiuWL 2002 MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415 977 983

41. RenDLiuYYangKYHanLMaoG 2008 A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci U S A 105 5638 5643

42. ShenQHSaijoYMauchSBiskupCBieriS 2007 Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315 1098 1103

43. PengYBartleyLECanlasPERonaldPC 2010 OsWRKY IIa Transcription Factors Modulate Rice Innate Immunity. Rice 3 36 42

44. SaigaSFurumizuCYokoyamaRKurataTSatoS 2008 The Arabidopsis OBERON1 and OBERON2 genes encode plant homeodomain finger proteins and are required for apical meristem maintenance. Development 135 1751 1759

45. KorfhageUTrezziniGFMeierIHahlbrockKSomssichIE 1994 Plant homeodomain protein involved in transcriptional regulation of a pathogen defense-related gene. Plant Cell 6 695 708

46. CenturyKSLagmanRAAdkissonMMorlanJTobiasR 1999 Short communication: developmental control of Xa21-mediated disease resistance in rice. Plant J 20 231 236

47. ParkCJLeeSWChernMSharmaRCanlasPE 2010 Ectopic expression of rice Xa21 overcomes developmentally controlled resistance to Xanthomonas oryzae pv. oryzae. Plant Sci 179 466 471

48. HalfordNGHeySJ 2009 Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem J 419 247 259

49. JossierMBoulyJPMeimounPArjmandALessardP 2009 SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J 59 316 328

50. AsselberghBDe VleesschauwerDHofteM 2008 Global switches and fine-tuning-ABA modulates plant pathogen defense. Mol Plant Microbe Interact 21 709 719

51. LeeILehnerBCrombieCWongWFraserAG 2008 A single gene network accurately predicts phenotypic effects of gene perturbation in Caenorhabditis elegans. Nat Genet 40 181 188

52. CollavinLLunardiADel SalG 2010 p53-family proteins and their regulators: hubs and spokes in tumor suppression. Cell Death Differ 17 901 911

53. HazbunTRFieldsS 2001 Networking proteins in yeast. Proc Natl Acad Sci U S A 98 4277 4278

54. WangPIMarcotteEM 2010 It's the machine that matters: predicting gene function and phenotype from protein networks. J Proteomics 73 2277 2289

55. OrchardSArandaBHermjakobH 2010 The publication and database deposition of molecular interaction data. Curr Protoc Protein Sci Chapter 25

56. BarrettTTroupDBWilhiteSELedouxPRudnevD 2009 NCBI GEO: archive for high-throughput functional genomic data. Nucleic Acids Res 37 D885 890

57. ParkinsonHKapusheskyMKolesnikovNRusticiGShojatalabM 2009 ArrayExpress update—from an archive of functional genomics experiments to the atlas of gene expression. Nucleic Acids Res 37 D868 872

58. JungKHDardickCBartleyLECaoPPhetsomJ 2008 Refinement of light-responsive transcript lists using rice oligonucleotide arrays: evaluation of gene-redundancy. PLoS ONE 3 e3337 doi:10.1371/journal.pone.0003337