-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
GATA-Dependent Glutaminolysis Drives Appressorium Formation in by Suppressing TOR Inhibition of cAMP/PKA Signaling
Many fungal pathogens destroy important crops by first gaining entrance to the host using specialized appressorial cells. Understanding the molecular mechanisms that control appressorium formation could provide new routes for managing severe plant diseases. Here, we describe a previously unknown regulatory pathway that suppresses appressorium formation by the rice pathogen Magnaporthe oryzae. We provide evidence that a mutant M. oryzae strain, unable to form appressoria, accumulates intracellular glutamine that, in turn, inappropriately activates a conserved signaling pathway called TOR. Reducing intracellular glutamine levels, or inactivating TOR, restored appressorium formation to the mutant strain. TOR activation is thus a powerful inhibitor of appressorium formation and could be leveraged to develop sustainable mitigation practices against recalcitrant fungal pathogens.
Vyšlo v časopise: GATA-Dependent Glutaminolysis Drives Appressorium Formation in by Suppressing TOR Inhibition of cAMP/PKA Signaling. PLoS Pathog 11(4): e32767. doi:10.1371/journal.ppat.1004851
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004851Souhrn
Many fungal pathogens destroy important crops by first gaining entrance to the host using specialized appressorial cells. Understanding the molecular mechanisms that control appressorium formation could provide new routes for managing severe plant diseases. Here, we describe a previously unknown regulatory pathway that suppresses appressorium formation by the rice pathogen Magnaporthe oryzae. We provide evidence that a mutant M. oryzae strain, unable to form appressoria, accumulates intracellular glutamine that, in turn, inappropriately activates a conserved signaling pathway called TOR. Reducing intracellular glutamine levels, or inactivating TOR, restored appressorium formation to the mutant strain. TOR activation is thus a powerful inhibitor of appressorium formation and could be leveraged to develop sustainable mitigation practices against recalcitrant fungal pathogens.
Zdroje
1. Emmett RW, Parbery DG. Appressoria. Annu Rev Phytopathol. 1975; 13 : 147–65.
2. Dean RA. Signal pathways and appressorium morphogenesis. Annu Rev Phytopathol. 1997; 35 : 211–34. 15012522
3. Dagdas YF, Yoshino K, Dagdas G, Ryder LS, Bielska E, Steinberg G, et al. Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. Science. 2012; 336 : 1590–5. doi: 10.1126/science.1222934 22723425
4. Mendgen K, Hahn M, Deising H. Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol. 1996; 34 : 367–86. 15012548
5. Wilson RA, Talbot NJ. Under pressure: Investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol. 2009; 7 : 185–95. doi: 10.1038/nrmicro2032 19219052
6. Yi M, Valent B. Communication between filamentous pathogens and plants at the biotrophic interface. Annu Rev Phytopathol. 2013; 51 : 587–611. doi: 10.1146/annurev-phyto-081211-172916 23750888
7. O'Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, et al. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet. 2012; 44 : 1060–5. doi: 10.1038/ng.2372 22885923
8. Talbot NJ. On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annu Rev Microbiol. 2003; 57 : 177–202. 14527276
9. Li G, Zhou X, Xu JR. Genetic control of infection-related development in Magnaporthe oryzae. Curr Opin Microbiol. 2012; 15 : 678–84. doi: 10.1016/j.mib.2012.09.004 23085322
10. Fernandez J, Wilson RA. Cells in cells: morphogenetic and metabolic strategies conditioning rice infection by the blast fungus Magnaporthe oryzae. Protoplasma. 2014; 251 : 37–47. doi: 10.1007/s00709-013-0541-8 23990109
11. Fernandez J, Marroquin-Guzman M, Wilson RA. Mechanisms of Nutrient Acquisition and Utilization During Fungal Infections of Leaves. Ann Rev Phytopathol. 2014; 52 : 155–74. doi: 10.1146/annurev-phyto-102313-050135 24848414
12. Lee YH, Dean RA. cAMP regulates infection structure formation in the plant pathogenic fungus Magnaporthe grisea. Plant Cell. 1993; 5 : 693–700. 12271080
13. Jelitto TC, Page HA, Read ND. Role of external signals in regulating the pre-penetration phase of infection by the rice blast fungus Magnaporthe grisea. Planta. 1994; 194 : 471–7.
14. Adachi K, Hamer JE. Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grisea. Plant Cell. 1998; 10 : 1361–1373. 9707535
15. Xu JR, Urban M, Sweigard JA, Hamer JE. The CPKA gene of Magnaporthe grisea is essential for appressorial penetration. Mol Plant Microbe Interact. 1997; 10 : 187–94.
16. Xu JR, Hamer JE. MAP-kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 1996; 10, 2696–2706. 8946911
17. Saunders DG, Dagdas YF, Talbot NJ. Spatial un-coupling of mitosis and cytokinesis during appressorium - mediated plant infection by the rice blast fungus Magnaporthe oryzae. Plant Cell. 2010; 22 : 2417–28. doi: 10.1105/tpc.110.074492 20639448
18. Wilson RA, Gibson RP, Quispe CF, Littlechild JA, Talbot NJ. An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus. Proc Natl Acad Sci USA. 2010; 107 : 21902–7. doi: 10.1073/pnas.1006839107 21115813
19. Wilson RA, Arst HN Jr. Mutational analysis of AREA, a transcriptional activator mediating nitrogen metabolite repression in Aspergillus nidulans and a member of the "streetwise" GATA family of transcription factors. Microbiol Mol Biol Rev. 1998; 62 : 586–96. 9729601
20. Loewith R, Hall MN. Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics. 2011; 189 : 1177–1201. doi: 10.1534/genetics.111.133363 22174183
21. Fernandez J, Wright JD, Hartline D, Quispe CF, Madayiputhiya N, Wilson RA. Principles of carbon catabolite repression in the rice blast fungus: Tps1, Nmr1-3, and a MATE–Family Pump regulate glucose metabolism during Infection. PLoS Genet. 2012; 8: e1002673. doi: 10.1371/journal.pgen.1002673 22570632
22. Fernandez J, Wilson RA. Why no feeding frenzy? Mechanisms of nutrient acquisition and utilization during Infection by the rice blast fungus Magnaporthe oryzae. Mol Plant Microbe Interact. 2012; 25 : 1286–93. doi: 10.1094/MPMI-12-11-0326 22947213
23. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature. 2005; 434 : 980–6. 15846337
24. Mora J. Glutamine metabolism and cycling in Neurospora crassa. Microbiol Rev. 1990; 54 : 293–304. 2145504
25. Yan D. Protection of the glutamate pool concentration in enteric bacteria. Proc Natl Acad Sci USA. 2007; 104 : 9475–80. 17517610
26. Le A, Lane AN, Hamaker M, Bose S, Gouw A, Barbi J, et al. Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab. 2012; 15 : 110–121. doi: 10.1016/j.cmet.2011.12.009 22225880
27. Soanes DM, Chakrabarti A, Paszkiewicz KH, Dawe AL, Talbot NJ. Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae. PLoS Pathog. 2012; 8:e1002514. doi: 10.1371/journal.ppat.1002514 22346750
28. Crespo JL, Powers T, Fowler B, Hall MN. The TOR-controlled transcription activators GLN3, RTG1, and RTG3 are regulated in response to intracellular levels of glutamine. Proc Natl Acad Sci USA. 2002; 99 : 6784–9. 11997479
29. Crespo JL, Hall MN. Elucidating TOR signaling and rapamycin action: lessons from Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 2002; 66 : 579–591. 12456783
30. Gallinetti J, Harputlugil E, Mitchell JR. Amino acid sensing in dietary-restriction-mediated longevity: roles of signal-transducing kinases GCN2 and TOR. Biochem J. 2013; 449 : 1–10. doi: 10.1042/BJ20121098 23216249
31. Peng T, Golub TR, Sabatini DM. The immunosuppressant rapamycin mimics a starvation-like signal distinct from amino acid and glucose deprivation. Mol Cell Biol. 2002; 22 : 5575–84. 12101249
32. Barbet NC, Schneider U, Helliwell SB, Stansfield I, Tuite MF, Hall MN. TOR controls translation initiation and early G1 progression in yeast. Mol Biol Cell. 1996; 7 : 25–42. 8741837
33. Heitman J, Movva NR, Hall M. Targets for cell cycle arrest by the immunosuppresant rapamycin in yeast. Science. 1991; 253 : 905–9. 1715094
34. Gamboa - Melendez H, Billon-Grand G, Fevre M, Mey G. Role of the Botrytis cinerea FKBP12 ortholog in pathogenic development and in sulfur regulation. Fung Genet Biol. 2009; 46 : 308–20. doi: 10.1016/j.fgb.2008.11.011 19116175
35. Yu F, Gu Q, Yun Y, Yin Y, Xu JR, Shim WB, et al. The TOR signaling pathway regulates vegetative development and virulence in Fusarium graminearum. New Phytol. 2014; 203 : 219–32. doi: 10.1111/nph.12776 24684168
36. Franceschetti M, Bueno E, Wilson RA, Tucker SL, Gomez-Mena C, Calder G, et al. Fungal virulence and development is regulated by alternative pre-mRNA 3′ end processing in Magnaporthe oryzae. PLoS Pathog. 2011; 7:e1002441. doi: 10.1371/journal.ppat.1002441 22194688
37. Rodriguez-Romero J, Franceschetti M, Bueno E, Sesma A. Multilayer Regulatory Mechanisms Control Cleavage Factor I Proteins in Filamentous Fungi. Nucleic Acids Res. 2015; (43): 179–95. doi: 10.1093/nar/gku1297 25514925
38. Fernandez J, Marroquin-Guzman M, Wilson RA. Evidence for a transketolase-mediated metabolic checkpoint governing biotrophic growth in rice cells by the blast fungus Magnaporthe oryzae. PLOS Pathogens 2014; 10 (9): e10004354.
39. Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science. 2006; 312 : 580–3. 16645096
40. Diaz-Troya S, Perez-Perez ME, Florencio FJ, Crespo JL. The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy. 2008; 4 : 851–865. 18670193
41. Beck T, Hall MN. The TOR signaling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature. 1999; 402 : 689–692. 10604478
42. Georis I, Feller A, Tate JJ, Cooper TG, Dubois E. Nitrogen catabolite repression-sensitive transcription as a readout of Tor pathway regulation: the genetic background, reporter gene and GATA factor assayed determine the outcomes. Genetics. 2009; 181 : 861–74. doi: 10.1534/genetics.108.099051 19104072
43. Powers RW III, Kaeberlein M, Caldwell SD, Kennedy BK, Fields S. Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 2006; 20 : 174–84. 16418483
44. Neklesa TK, Davis RW. A Genome-Wide Screen for Regulators of TORC1 in Response to Amino Acid Starvation Reveals a Conserved Npr2/3 Complex. PLoS Genet. 2009; 5: e1000515. doi: 10.1371/journal.pgen.1000515 19521502
45. Kershaw MJ, Talbot NJ. Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc Natl Acad Sci USA. 2009; 106 : 15967–72 doi: 10.1073/pnas.0901477106 19717456
46. Chen D, Wang Y, Zhou X, Wang Y, Xu J-R. The Sch9 Kinase Regulates Conidium Size, Stress Responses, and Pathogenesis in Fusarium graminearum. PLoS ONE. 2014; 9(8): e105811. doi: 10.1371/journal.pone.0105811 25144230
47. Oh Y, Franck WL, Han S, Shows A, Gokce E, Meng S, et al. Polyubiquitin is required for growth, development and pathogenicity in the Rice Blast Fungus Magnaporthe oryzae. PLoS One. 2012; 7: e42868. doi: 10.1371/journal.pone.0042868 22900059
48. Soulard A, Cremonesi A, Moes S, Schütz F, Jenö P, Hall MN. The rapamycin-sensitive phosphoproteome reveals that TOR controls protein kinase A toward some but not all substrates. Mol Biol Cell. 2010; 21 : 3475–86. doi: 10.1091/mbc.E10-03-0182 20702584
49. Stephan JS, Yeh YY, Ramachandran V, Deminoff SJ, Herman PK. The Tor and PKA signaling pathways independently target the Atg1/Atg13 protein kinase complex to control autophagy. Proc Natl Acad Sci USA. 2009; 106 : 17049–54. doi: 10.1073/pnas.0903316106 19805182
50. Park G, Xue C, Zheng L, Lam S, Xu JR. MST12 regulates infectious growth but not appressorium formation in the rice blast fungus Magnaporthe grisea. Mol Plant Microbe Interact. 2002; 15 : 183–92. 11952120
51. Ryder LS, Dagdas YF, Mentlak TA, Kershaw MJ, Thornton CR, Schuster M, et al. NADPH oxidases regulate septin-mediated cytoskeletal remodeling during plant infection by the rice blast fungus. Proc Natl Acad Sci USA. 2013; 110 : 3179–84. doi: 10.1073/pnas.1217470110 23382235
52. Xu JR, Staiger CJ, Hamer JE. Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc Natl Acad Sci USA. 1998; 95 : 12713–8. 9770551
53. Fernandez J, Yang KT, Cornwell KM, Wright JD, Wilson RA. Growth in rice cells requires de novo purine biosynthesis by the blast fungus Magnaporthe oryzae. Sci Rep. 2013; 3 : 2398. doi: 10.1038/srep02398 23928947
54. Zhou X, Li G, Xu JR. Efficient approaches for generating GFP fusion and epitope-tagging constructs in filamentous fungi. Methods Mol Biol. 2011; 722 : 199–212. doi: 10.1007/978-1-61779-040-9_15 21590423
55. Fernandez J, Marroquin-Guzman M, Nandakumar R, Shijo S, Cornwell K, Li G, et al. Plant defense suppression is mediated by a fungal sirtuin during rice infection by Magnaporthe oryzae. Mol Micro. 2014; 94 : 70–88.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium
Článek Relay of Herpes Simplex Virus between Langerhans Cells and Dermal Dendritic Cells in Human SkinČlánek Does the Arthropod Microbiota Impact the Establishment of Vector-Borne Diseases in Mammalian Hosts?Článek The Ebola Epidemic Crystallizes the Potential of Passive Antibody Therapy for Infectious DiseasesČlánek Hepatitis D Virus Infection of Mice Expressing Human Sodium Taurocholate Co-transporting PolypeptideČlánek A Redox Regulatory System Critical for Mycobacterial Survival in Macrophages and Biofilm Development
Článok vyšiel v časopisePLOS Pathogens
Najčítanejšie tento týždeň
2015 Číslo 4- 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?
-
Všetky články tohto čísla
- Pathogens as Biological Weapons of Invasive Species
- Selection and Spread of Artemisinin-Resistant Alleles in Thailand Prior to the Global Artemisinin Resistance Containment Campaign
- Endopeptidase-Mediated Beta Lactam Tolerance
- Prospective Large-Scale Field Study Generates Predictive Model Identifying Major Contributors to Colony Losses
- Relay of Herpes Simplex Virus between Langerhans Cells and Dermal Dendritic Cells in Human Skin
- Structural Determinants of Phenotypic Diversity and Replication Rate of Human Prions
- Sigma Factor SigB Is Crucial to Mediate Adaptation during Chronic Infections
- EphrinA2 Receptor (EphA2) Is an Invasion and Intracellular Signaling Receptor for
- Toxin-Induced Necroptosis Is a Major Mechanism of Lung Damage
- Heterologous Expression in Remodeled . : A Platform for Monoaminergic Agonist Identification and Anthelmintic Screening
- Novel Disease Susceptibility Factors for Fungal Necrotrophic Pathogens in Arabidopsis
- Interleukin 21 Signaling in B Cells Is Required for Efficient Establishment of Murine Gammaherpesvirus Latency
- Phosphorylation at the Homotypic Interface Regulates Nucleoprotein Oligomerization and Assembly of the Influenza Virus Replication Machinery
- Human Papillomaviruses Activate and Recruit SMC1 Cohesin Proteins for the Differentiation-Dependent Life Cycle through Association with CTCF Insulators
- Ubiquitous Promoter-Localization of Essential Virulence Regulators in
- TGF-β Suppression of HBV RNA through AID-Dependent Recruitment of an RNA Exosome Complex
- The Immune Adaptor ADAP Regulates Reciprocal TGF-β1-Integrin Crosstalk to Protect from Influenza Virus Infection
- Antagonism of miR-328 Increases the Antimicrobial Function of Macrophages and Neutrophils and Rapid Clearance of Non-typeable (NTHi) from Infected Lung
- The Epigenetic Regulator G9a Mediates Tolerance to RNA Virus Infection in
- Does the Arthropod Microbiota Impact the Establishment of Vector-Borne Diseases in Mammalian Hosts?
- Hantaan Virus Infection Induces Both Th1 and ThGranzyme B+ Cell Immune Responses That Associated with Viral Control and Clinical Outcome in Humans
- Viral Inhibition of the Transporter Associated with Antigen Processing (TAP): A Striking Example of Functional Convergent Evolution
- Plasma Membrane Profiling Defines an Expanded Class of Cell Surface Proteins Selectively Targeted for Degradation by HCMV US2 in Cooperation with UL141
- Optineurin Regulates the Interferon Response in a Cell Cycle-Dependent Manner
- IFIT1 Differentially Interferes with Translation and Replication of Alphavirus Genomes and Promotes Induction of Type I Interferon
- The EBNA3 Family of Epstein-Barr Virus Nuclear Proteins Associates with the USP46/USP12 Deubiquitination Complexes to Regulate Lymphoblastoid Cell Line Growth
- Hepatitis C Virus RNA Replication Depends on Specific and -Acting Activities of Viral Nonstructural Proteins
- A Neuron-Specific Antiviral Mechanism Prevents Lethal Flaviviral Infection of Mosquitoes
- The Aspartate-Less Receiver (ALR) Domains: Distribution, Structure and Function
- Global Genome and Transcriptome Analyses of Epidemic Isolate 98-06 Uncover Novel Effectors and Pathogenicity-Related Genes, Revealing Gene Gain and Lose Dynamics in Genome Evolution
- The Ebola Epidemic Crystallizes the Potential of Passive Antibody Therapy for Infectious Diseases
- Ebola Virus Entry: A Curious and Complex Series of Events
- Conserved Spirosomes Suggest a Single Type of Transformation Pilus in Competence
- Spatial Structure, Transmission Modes and the Evolution of Viral Exploitation Strategies
- Bacterial Cooperation Causes Systematic Errors in Pathogen Risk Assessment due to the Failure of the Independent Action Hypothesis
- Transgenic Fatal Familial Insomnia Mice Indicate Prion Infectivity-Independent Mechanisms of Pathogenesis and Phenotypic Expression of Disease
- Cerebrospinal Fluid Cytokine Profiles Predict Risk of Early Mortality and Immune Reconstitution Inflammatory Syndrome in HIV-Associated Cryptococcal Meningitis
- Utilize Host Actin for Efficient Maternal Transmission in
- Borna Disease Virus Phosphoprotein Impairs the Developmental Program Controlling Neurogenesis and Reduces Human GABAergic Neurogenesis
- An Effector Peptide Family Required for Toll-Mediated Immunity
- Hepatitis D Virus Infection of Mice Expressing Human Sodium Taurocholate Co-transporting Polypeptide
- A Redox Regulatory System Critical for Mycobacterial Survival in Macrophages and Biofilm Development
- Quadruple Quorum-Sensing Inputs Control Virulence and Maintain System Robustness
- Leukocyte-Derived IFN-α/β and Epithelial IFN-λ Constitute a Compartmentalized Mucosal Defense System that Restricts Enteric Virus Infections
- A Strategy for O-Glycoproteomics of Enveloped Viruses—the O-Glycoproteome of Herpes Simplex Virus Type 1
- Macrocyclic Lactones Differ in Interaction with Recombinant P-Glycoprotein 9 of the Parasitic Nematode and Ketoconazole in a Yeast Growth Assay
- Neofunctionalization of the α1,2fucosyltransferase Paralogue in Leporids Contributes to Glycan Polymorphism and Resistance to Rabbit Hemorrhagic Disease Virus
- The Extracytoplasmic Linker Peptide of the Sensor Protein SaeS Tunes the Kinase Activity Required for Staphylococcal Virulence in Response to Host Signals
- Murine CMV-Induced Hearing Loss Is Associated with Inner Ear Inflammation and Loss of Spiral Ganglia Neurons
- Dual miRNA Targeting Restricts Host Range and Attenuates Neurovirulence of Flaviviruses
- GATA-Dependent Glutaminolysis Drives Appressorium Formation in by Suppressing TOR Inhibition of cAMP/PKA Signaling
- Role of Hypoxia Inducible Factor-1α (HIF-1α) in Innate Defense against Uropathogenic Infection
- Genetic Analysis Using an Isogenic Mating Pair of Identifies Azole Resistance Genes and Lack of Locus’s Role in Virulence
- A Temporal Gate for Viral Enhancers to Co-opt Toll-Like-Receptor Transcriptional Activation Pathways upon Acute Infection
- Neutrophil Recruitment to Lymph Nodes Limits Local Humoral Response to
- PLOS Pathogens
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Toxin-Induced Necroptosis Is a Major Mechanism of Lung Damage
- Transgenic Fatal Familial Insomnia Mice Indicate Prion Infectivity-Independent Mechanisms of Pathogenesis and Phenotypic Expression of Disease
- Role of Hypoxia Inducible Factor-1α (HIF-1α) in Innate Defense against Uropathogenic Infection
- EphrinA2 Receptor (EphA2) Is an Invasion and Intracellular Signaling Receptor for
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy