A Genetic Screen Reveals Arabidopsis Stomatal and/or Apoplastic Defenses against pv. DC3000
Bacterial infection of plants often begins with colonization of the plant surface, followed by entry into the plant through wounds and natural openings (such as stomata), multiplication in the intercellular space (apoplast) of the infected tissues, and dissemination of bacteria to other plants. Historically, most studies assess bacterial infection based on final outcomes of disease and/or pathogen growth using whole infected tissues; few studies have genetically distinguished the contribution of different host cell types in response to an infection. The phytotoxin coronatine (COR) is produced by several pathovars of Pseudomonas syringae. COR-deficient mutants of P. s. tomato (Pst) DC3000 are severely compromised in virulence, especially when inoculated onto the plant surface. We report here a genetic screen to identify Arabidopsis mutants that could rescue the virulence of COR-deficient mutant bacteria. Among the susceptible to coronatine-deficient Pst DC3000 (scord) mutants were two that were defective in stomatal closure response, two that were defective in apoplast defense, and four that were defective in both stomatal and apoplast defense. Isolation of these three classes of mutants suggests that stomatal and apoplastic defenses are integrated in plants, but are genetically separable, and that COR is important for Pst DC3000 to overcome both stomatal guard cell- and apoplastic mesophyll cell-based defenses. Of the six mutants defective in bacterium-triggered stomatal closure, three are defective in salicylic acid (SA)-induced stomatal closure, but exhibit normal stomatal closure in response to abscisic acid (ABA), and scord7 is compromised in both SA- and ABA-induced stomatal closure. We have cloned SCORD3, which is required for salicylic acid (SA) biosynthesis, and SCORD5, which encodes an ATP-binding cassette (ABC) protein, AtGCN20/AtABCF3, predicted to be involved in stress-associated protein translation control. Identification of SCORD5 begins to implicate an important role of stress-associated protein translation in stomatal guard cell signaling in response to microbe-associated molecular patterns and bacterial infection.
Vyšlo v časopise:
A Genetic Screen Reveals Arabidopsis Stomatal and/or Apoplastic Defenses against pv. DC3000. PLoS Pathog 7(10): e32767. doi:10.1371/journal.ppat.1002291
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002291
Souhrn
Bacterial infection of plants often begins with colonization of the plant surface, followed by entry into the plant through wounds and natural openings (such as stomata), multiplication in the intercellular space (apoplast) of the infected tissues, and dissemination of bacteria to other plants. Historically, most studies assess bacterial infection based on final outcomes of disease and/or pathogen growth using whole infected tissues; few studies have genetically distinguished the contribution of different host cell types in response to an infection. The phytotoxin coronatine (COR) is produced by several pathovars of Pseudomonas syringae. COR-deficient mutants of P. s. tomato (Pst) DC3000 are severely compromised in virulence, especially when inoculated onto the plant surface. We report here a genetic screen to identify Arabidopsis mutants that could rescue the virulence of COR-deficient mutant bacteria. Among the susceptible to coronatine-deficient Pst DC3000 (scord) mutants were two that were defective in stomatal closure response, two that were defective in apoplast defense, and four that were defective in both stomatal and apoplast defense. Isolation of these three classes of mutants suggests that stomatal and apoplastic defenses are integrated in plants, but are genetically separable, and that COR is important for Pst DC3000 to overcome both stomatal guard cell- and apoplastic mesophyll cell-based defenses. Of the six mutants defective in bacterium-triggered stomatal closure, three are defective in salicylic acid (SA)-induced stomatal closure, but exhibit normal stomatal closure in response to abscisic acid (ABA), and scord7 is compromised in both SA- and ABA-induced stomatal closure. We have cloned SCORD3, which is required for salicylic acid (SA) biosynthesis, and SCORD5, which encodes an ATP-binding cassette (ABC) protein, AtGCN20/AtABCF3, predicted to be involved in stress-associated protein translation control. Identification of SCORD5 begins to implicate an important role of stress-associated protein translation in stomatal guard cell signaling in response to microbe-associated molecular patterns and bacterial infection.
Zdroje
1. WhalenMInnesRBentAStaskawiczB 1991 Identification of Pseudomonas syringae pathogens of Arabidopsis thaliana and a bacterial gene determining avirulence on both Arabidopsis and soybean. Plant Cell 3 49 59
2. PrestonGM 2000 Pseudomonas syringae pv. tomato: the right pathogen, of the right plant, at the right time. Mol Plant Pathol 1 263 275
3. KatagiriFThilmonyRHeSY 2002 The Arabidopsis thaliana-Pseudomonas syringae interaction. SomervilleCRMeyerowitzEM The Arabidopsis Book Rockville American Society of Plant Biologists 1 35
4. MitchellRE 1982 Coronatine production by some phytopathogenic Pseudomonads. Physiol Plant Pathol 20 83 89
5. MaSWMorrisVLCuppelsDA 1991 Characterization of a DNA region required for production of the phytotoxin coronatine by Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 4 69 77
6. MittalSDavisKR 1995 Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 8 165 171
7. BenderCLAlarcón-ChaidezFGrossDC 1999 Pseudomonas syringae phytotoxins: mode of action, regulation and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63 266 292
8. CintasNAKoikeSTBullCT 2002 A new pathovar, Pseudomonas syringae pv. alisalensis, proposed for the causal agent of bacterial blight of broccoli and broccoli raab. Plant Dis 86 992 998
9. BenderCLStoneHESimsJJCookseyDA 1987 Reduced pathogen fitness of Pseudomonas syringae pv. tomato Tn5 mutants defective in coronatine production. Physiol Mol Plant Pathol 30 273 283
10. Peñaloza-VázquezAPrestonGMCollmerABenderCL 2000 Regulatory interactions between the hrp Type III protein secretion system and coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000. Microbiology 146 2447 2456
11. BrooksDMHernández-GuzmánGKloekAPAlarcón-ChaidezFSreedharanA 2004 Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 17 162 174
12. BrooksDMBenderCLKunkelBN 2005 The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defenses in Arabidopsis thaliana. Mol Plant Pathol 6 629 639
13. CuiJBahramiAKPringleEGHernandez-GuzmanGBenderCL 2005 Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc Natl Acad Sci U S A 102 1791 1796
14. MelottoMUnderwoodWKoczanJNomuraKHeSY 2006 Plant stomata function in innate immunity against bacterial invasion. Cell 126 969 980
15. UppalapatiSRIshigaYWangdiTKunkelBNAnandA 2007 The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 20 955 965
16. UppalapatiSRIshigaYWangdiTUrbanczyk-WochniakEIshigaT 2008 Pathogenicity of Pseudomonas syringae pv. tomato on tomato seedlings: phenotypic and gene expression analyses of the virulence function of coronatine. Mol Plant Microbe Interact 21 383 395
17. IshigaYUppalapatiSRIshigaTElavarthiSMartinB 2009 The phytotoxin coronatine induces light-dependent reactive oxygen species in tomato seedlings. New Phytol 181 147 160
18. FreemanBCBeattleGA 2009 Bacterial growth restriction during host resistance to Pseudomonas syringae is associated with leaf water loss and localized cessation of vascular activity in Arabidopsis thaliana. Mol Plant Microbe Interact 22 857 867
19. ZengWHeSY 2010 A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol 153 1188 1198
20. KatsirLSchilmillerALStaswickPEHeSYHoweGA 2008 COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci U S A 105 7100 7105
21. FonsecaSChiniAHambergMAdieBPorzelA 2009 (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5 344 350
22. SheardLBTanXMaoHWithersJNissanGB 2010 Mechanism of jasmonate recognition by an inositol phosphate-potentiated COI1-JAZ co-receptor. Nature 468 400 405
23. UppalapatiSRAyoubiPWengHPalmerDAMitchellRE 2005 The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J 42 201 217
24. 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
25. ZhaoYThilmonyRBenderCLSchallerAHeSY 2003 Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36 485 499
26. ClayNKAdioAMDenouxCJanderGAusubelFM 2009 Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323 95 101
27. MilletYADannaCHClayNKSongnuanWSimonMD 2010 Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22 973 990
28. MustilliA-CMerlotSVavasseurAFenziFGiraudatJ 2002 Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14 3089 3099
29. XieXWangYWilliamsonLHolroydGHTagliaviaC 2006 The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Curr Biol 16 882 887
30. DesikanRCheungM-KClarkeAGoldingSSagiM 2004 Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum. Funct Plant Biol 31 913 920
31. NawrathCHeckSParinthawongNMétrauxJP 2002 EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14 275 286
32. RossoMGLiYStrizhovNRiessBDekkerK 2003 An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53 247 259
33. Sánchez-FernándezRDaviesTGEColemanJODReaPA 2001 The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276 30231 30244
34. GarciaOBouigePForestierCDassaE 2004 Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J Mol Biol 343 249 265
35. VerrierPJBirdDBurlaBDassaEForestierC 2008 Plant ABC proteins - a unified nomenclature and updated inventory. Trends Plant Sci 13 151 159
36. ZengWMelottoMHeSY 2010 Plant stomata: a checkpoint of host immunity and pathogen virulence. Curr Opin Biotechnol 21 599 603
37. de AldanaCRVMartonMJHinnebuschAG 1995 GCN20, a novel ATP binding cassette protein, and GCN1 reside in a complex that mediates activation of the eIF-2 alpha kinase GCN2 in amino acid-starved cells. EMBO J 14 3184 3199
38. MartonMJde AldanaCRVQiuHChakraburttyKHinnebuschAG 1997 Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2α kinase GCN2. Mol Cell Biol 17 4474 4489
39. HinnebuschAG 2005 Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59 407 450
40. MonaghanJLiX 2010 The HEAT repeat protein ILITYHIA is required for plant immunity. Plant Cell Physiol 51 742 753
41. de Torres-ZabalaMTrumanWBennettMHLafforgueGMansfieldJW 2007 Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signaling pathway to cause disease. EMBO J 26 1434 1443
42. WeigelDAhnJHBlazquezMABorevitzJOChristensenSK 2000 Activation tagging in Arabidopsis. Plant Physiol 122 1003 1013
43. HuangGZhangLBirchRG 2000 Rapid amplification and cloning of Tn5 flanking fragments by inverse PCR. Lett Appl Microbiol 31 149 153
44. SambrookJMacCallumPRussellDW 2001 Molecular Cloning: A Laboratory Manual, 3rd edition New York Cold Spring Harbor Laboratory Press
45. KepplerLDBakerCJAtkinsonMM 1989 Active oxygen production during a bacteria-induced hypersensitive reaction in tobacco suspension cells. Phytopathology 79 974 978
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 10
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Severe Acute Respiratory Syndrome Coronavirus Envelope Protein Regulates Cell Stress Response and Apoptosis
- The SARS-Coronavirus-Host Interactome: Identification of Cyclophilins as Target for Pan-Coronavirus Inhibitors
- Biochemical and Structural Insights into the Mechanisms of SARS Coronavirus RNA Ribose 2′-O-Methylation by nsp16/nsp10 Protein Complex
- Evolutionarily Divergent, Unstable Filamentous Actin Is Essential for Gliding Motility in Apicomplexan Parasites