#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The OXI1 Kinase Pathway Mediates -Induced Growth Promotion in Arabidopsis


Piriformospora indica is an endophytic fungus that colonizes roots of many plant species and promotes growth and resistance to certain plant pathogens. Despite its potential use in agriculture, little is known on the molecular basis of this beneficial plant-fungal interaction. In a genetic screen for plants, which do not show a P. indica- induced growth response, we isolated an Arabidopsis mutant in the OXI1 (Oxidative Signal Inducible1) gene. OXI1 has been characterized as a protein kinase which plays a role in pathogen response and is regulated by H2O2 and PDK1 (3-PHOSPHOINOSITIDE-DEPENDENT PROTEIN KINASE1). A genetic analysis showed that double mutants of the two closely related PDK1.1 and PDK1.2 genes are defective in the growth response to P. indica. While OXI1 and PDK1 gene expression is upregulated in P. indica-colonized roots, defense genes are downregulated, indicating that the fungus suppresses plant defense reactions. PDK1 is activated by phosphatidic acid (PA) and P. indica triggers PA synthesis in Arabidopsis plants. Under beneficial co-cultivation conditions, H2O2 formation is even reduced by the fungus. Importantly, phospholipase D (PLD)α1 or PLDδ mutants, which are impaired in PA synthesis do not show growth promotion in response to fungal infection. These data establish that the P. indica-stimulated growth response is mediated by a pathway consisting of the PLD-PDK1-OXI1 cascade.


Vyšlo v časopise: The OXI1 Kinase Pathway Mediates -Induced Growth Promotion in Arabidopsis. PLoS Pathog 7(5): e32767. doi:10.1371/journal.ppat.1002051
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002051

Souhrn

Piriformospora indica is an endophytic fungus that colonizes roots of many plant species and promotes growth and resistance to certain plant pathogens. Despite its potential use in agriculture, little is known on the molecular basis of this beneficial plant-fungal interaction. In a genetic screen for plants, which do not show a P. indica- induced growth response, we isolated an Arabidopsis mutant in the OXI1 (Oxidative Signal Inducible1) gene. OXI1 has been characterized as a protein kinase which plays a role in pathogen response and is regulated by H2O2 and PDK1 (3-PHOSPHOINOSITIDE-DEPENDENT PROTEIN KINASE1). A genetic analysis showed that double mutants of the two closely related PDK1.1 and PDK1.2 genes are defective in the growth response to P. indica. While OXI1 and PDK1 gene expression is upregulated in P. indica-colonized roots, defense genes are downregulated, indicating that the fungus suppresses plant defense reactions. PDK1 is activated by phosphatidic acid (PA) and P. indica triggers PA synthesis in Arabidopsis plants. Under beneficial co-cultivation conditions, H2O2 formation is even reduced by the fungus. Importantly, phospholipase D (PLD)α1 or PLDδ mutants, which are impaired in PA synthesis do not show growth promotion in response to fungal infection. These data establish that the P. indica-stimulated growth response is mediated by a pathway consisting of the PLD-PDK1-OXI1 cascade.


Zdroje

1. Peškan-BerghöferTShahollariBGiongPHHehlSMarkertC 2004 Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol Plant 122 465 477

2. OelmüllerRSherametiITripathiSVarmaA 2009 Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49 1 17

3. SelosseMADuboisMPAlvarezN 2009 Do Sebacinales commonly associate with plant roots as endophytes? Mycol Res 113 1062 1069

4. VermaSVarmaA 1998 Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90 896 903

5. ShahollariBVadasseryJVarmaAOelmüllerR 2007 A leucine-rich repeat protein is required for growth promotion and enhanced seed production mediated by the endophytic fungus Piriformospora indica in Arabidopsis thaliana. Plant J 50 1 13

6. SherametiIShahollariBVenusYAltschmiedLVarmaA 2005 The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J Biol Chem 280 26241 26247

7. SherametiIVenusYDrzewieckiCTripathiSDanVM 2008 PYK10, a beta-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J 54 428 439

8. SherametiITripathiSVarmaAOelmüllerR 2008 The root-colonizing endophyte Piriformospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol Plant Microbe Interact 21 799 807

9. VadasseryJRanfSDrzewieckiCMithöferAMazarsC 2009 A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59 193 206

10. VadasseryJTripathiSPrasadRVarmaAOelmüllerR 2009 Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J Plant Physiol 166 1263 1274

11. WallerFAchatzBBaltruschatHFodorJBeckerK 2005 The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102 13386 13391

12. ShahollariBPeškan-BerghöferTOelmüllerR 2004 Receptor kinases with leucine-rich repeats are enriched in Triton X-100 insoluble plasma membrane microdomains from plants. Physiol Plant 122 397 403

13. YadavVKumarMDeepDKKumarHSharmaR 2010 A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285 26532 26544

14. BaltruschatHFodorJHarrachBDNiemczykEBarnaB 2008 Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180 501 510

15. SunCJohnsonJMCaiDSherametiIOelmüllerR 2010 Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167 1009 1017

16. SteinEMolitorAKogelKHWallerF 2008 Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49 1747 1751

17. AlessiDR 2001 Discovery of PDK1, one of the missing links in insulin signal transduction. Colworth Medal Lecture. Biochem Soc Trans 29 1 14

18. StorzPTokerA 2002 3'-phosphoinositide-dependent kinase-1 (PDK-1) in PI 3-kinase signaling. Front Biosci 7 d886 902

19. MoraAKomanderDvan AaltenDMAlessiDR 2004 PDK1, the master regulator of AGC kinase signal transduction. Semin Cell Dev Biol 15 161 170

20. AnthonyRGHenriquesRHelferAMeszarosTRiosG 2004 A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23 572 581

21. AnthonyRGKhanSCostaJPaisMSBögreL 2006 The Arabidopsis protein kinase PTI1-2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J Biol Chem 281 37536 37546

22. DevaiahSPRothMRBaughmanELiMTamuraP 2006 Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dα1 knockout mutant. Phytochemistry 67 1907 1924

23. MunnikTMeijerHJTer RietBHirtHFrankW 2000 Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J 22 147 154

24. LaxaltAMMunnikT 2002 Phospholipid signalling in plant defence. Curr Opin Plant Biol 5 332 338

25. ZhangYZhuHZhangQLiMYanM 2009 Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21 2357 2377

26. TesterinkCMunnikT 2005 Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10 368 375

27. WangXDevaiahSPZhangWWeltiR 2006 Signaling functions of phosphatidic acid. Prog Lipid Res 45 250 278

28. LiMHongYWangX 2009 Phospholipase D- and phosphatidic acid-mediated signaling in plants. BBA - Mol Cell Biol L 1791 927 935

29. DeakMCasamayorACurrieRADownesCPAlessiDR 1999 Characterisation of a plant 3-phosphoinositide-dependent protein kinase-1 homologue which contains a pleckstrin homology domain. FEBS Lett 451 220 226

30. BögreLOkrészLHenriquesRAnthonyRG 2003 Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci 8 424 431

31. RentelMCLecourieuxDOuakedFUsherSLPetersenL 2004 OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427 858 861

32. van der LuitAHPiattiTvan DoornAMusgraveAFelixG 2000 Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 123 1507 1516

33. YamaguchiTMinamiEUekiJShibuyaN 2005 Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46 579 587

34. OyamaTShimuraYOkadaK 2002 The IRE gene encodes a protein kinase homologue and modulates root hair growth in Arabidopsis. Plant J 30 289 299

35. ForemanJDemidchikVBothwellJHMylonaPMiedemaH 2003 Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422 442 446

36. AriszSATesterinkCMunnikT 2009 Plant PA signaling via diacylglycerol kinase. Biochim Biophys Acta 1791 869 875

37. QinCWangX 2002 The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLDζ1 with distinct regulatory domains. Plant Physiol 128 1057 1068

38. ZhangWWanXHongYLiWWangX 2010 Plant phospholipase D. Berlin Heidelberg, Germany Springer-Verlag 39 62 In Lipid Signaling in Plants (ed T Munnik)

39. BargmannBOLaxaltAMter RietBTesterinkCMerquiolE 2009 Reassessing the role of phospholipase D in the Arabidopsis wounding response. Plant Cell Environ 32 837 850

40. VadasseryJRitterCVenusYCamehlIVarmaA 2008 The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microbe Interact 21 1371 1383

41. CamehlISherametiIVenusYBethkeGVarmaA 2010 Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol 185 1062 1073

42. PetersenLNIngleRAKnightMRDenbyKJ 2009 OXI1 protein kinase is required for plant immunity against Pseudomonas syringae in Arabidopsis. J Exp Bot 60 3727 3735

43. WangHNgwenyamaNLiuYWalkerJCZhangS 2007 Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19 63 73

44. WangX 2005 Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol 139 566 573

45. BargmannBOMunnikT 2006 The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9 515 522

46. XueHChenXLiG 2007 Involvement of phospholipid signaling in plant growth and hormone effects. Curr Opin Plant Biol 10 483 489

47. HongYPanXWeltiRWangX 2008 Phospholipase Dα3 is involved in the hyperosmotic response in Arabidopsis. Plant Cell 20 803 816

48. HongYDevaiahSPBahnSCThamasandraBNLiM 2009 Phospholipase Dε and phosphatidic acid enhance Arabidopsis nitrogen signaling and growth. Plant J 58 376 387

49. FangYVilella-BachMBachmannRFlaniganAChenJ 2001 Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294 1942 1945

50. HuangPFrohmanMA 2007 The potential for phospholipase D as a new therapeutic target. Expert Opin Ther Tar 11 707 716

51. FosterDAXuL 2003 Phospholipase D in cell proliferation and cancer. Mol Cancer Res 1 789 800

52. CrawfordNM 1995 Nitrate: nutrient and signal for plant growth. Plant Cell 7 859 868

53. Walch-LiuPIvanovIIFilleurSGanYRemansT 2006 Nitrogen regulation of root branching. Ann Bot 97 875 881

54. HirelBLe GouisJNeyBGallaisA 2007 The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58 2369 2387

55. LiMWeltiRWangX 2006 Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Dζ1 and Dζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142 750 761

56. Cruz-RamirezAOropeza-AburtoARazo-HernandezFRamirez-ChavezEHerrera-EstrellaL 2006 Phospholipase Dζ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103 6765 6770

57. BayascasJR 2010 PDK1: the major transducer of PI 3-kinase actions. Curr Top Microbiol Immunol 346 9 29

58. LawlorMAMoraAAshbyPRWilliamsMRMurray-TaitV 2002 Essential role of PDK1 in regulating cell size and development in mice. EMBO J 21 3728 3738

59. ZhangWWangCQinCWoodTOlafsdottirG 2003 The oleate-stimulated phospholipase D, PLDδ, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15 2285 2295

60. MurashigeTSkoogF 1962 A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15 473 497

61. BargmannBOLaxaltAMter RietBvan SchootenBMerquiolE 2009 Multiple PLDs required for high salinity and water deficit tolerance in plants. Plant Cell Physiol 50 78 89

62. BütehornBRhodyDFrankenP 2000 Isolation and characterisation of Pitef1 encoding the translation elongation factor EF-1a of the root endophyte Piriformospora indica. Plant Biol 2 687 692

63. PfafflMW 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 e45

64. Veljovic-JovanovicSNoctorGFoyerCH 2002 Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. Plant Physiol Bioch 40 501 507

65. MunnikTMusgraveAde VrijeT 1994 Rapid turnover of polyphosphoinositides in carnation flower petals. Planta 193 89 98

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 5
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#