Anti-Apoptotic Machinery Protects the Necrotrophic Fungus from Host-Induced Apoptotic-Like Cell Death during Plant Infection

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Necrotrophic fungi are unable to occupy living plant cells. How such pathogens survive first contact with living host tissue and initiate infection is therefore unclear. Here, we show that the necrotrophic grey mold fungus Botrytis cinerea undergoes massive apoptotic-like programmed cell death (PCD) following germination on the host plant. Manipulation of an anti-apoptotic gene BcBIR1 modified fungal response to PCD-inducing conditions. As a consequence, strains with reduced sensitivity to PCD were hyper virulent, while strains in which PCD was over-stimulated showed reduced pathogenicity. Similarly, reduced levels of PCD in the fungus were recorded following infection of Arabidopsis mutants that show enhanced susceptibility to B. cinerea. When considered together, these results suggest that Botrytis PCD machinery is targeted by plant defense molecules, and that the fungal anti-apoptotic machinery is essential for overcoming this host-induced PCD and hence, for establishment of infection. As such, fungal PCD machinery represents a novel target for fungicides and antifungal drugs.

Vyšlo v časopise: Anti-Apoptotic Machinery Protects the Necrotrophic Fungus from Host-Induced Apoptotic-Like Cell Death during Plant Infection. PLoS Pathog 7(8): e32767. doi:10.1371/journal.ppat.1002185
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002185

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Zdroje

1. GlazebrookJ 2005 Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43 205 227

2. ButtnerDBonasU 2003 Common infection strategies of plant and animal pathogenic bacteria. Cur Opin Plant Biol 6 312 319

3. SextonACHowlettBJ 2006 Parallels in fungal pathogenesis on plant and animal hosts. Eukar Cell 5 1941 1949

4. van KanJAL 2006 Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11 247 253

5. El OirdiMBouarabK 2007 Plant signalling components EDS1 and SGT1 enhance disease caused by the necrotrophic pathogen Botrytis cinerea. New Phytol 175 131 139

6. GovrinEMLevineA 2000 The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10 751 757

7. FerrariSGallettiRDenouxCDe LorenzoGAusubelFM 2007 Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol 144 367 379

8. RoweHCKliebensteinDJ 2008 Complex genetics control natural variation in Arabidopsis thaliana resistance to Botrytis cinerea. Genetics 180 2237 2250

9. ZhengZQamarSAChenZMengisteT 2006 Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48 592 605

10. FerrariSPlotnikovaJMDe LorenzoGAusubelFM 2003 Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35 193 205

11. RoweHCWalleyJWCorwinJChanEKFDeheshK 2010 Deficiencies in jasmonate-mediated plant defense reveal quantitative variation in Botrytis cinerea pathogenesis. PLoS Pathog 6 e1000861

12. VeronesePNakagamiHBluhmBAbuQamarSChenX 2006 The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18 257 273

13. BednarekPPislewska-BednarekMSvatosASchneiderBDoubskyJ 2009 A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323 101 106

14. ClayNKAdioAMDenouxCJanderGAusubelFM 2009 Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323 95 101

15. KliebensteinDJRoweHCDenbyKJ 2005 Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. Plant J 44 25 36

16. ŁaźniewskaJMacioszekVLawrenceCKononowiczA 2010 Fight to the death: Arabidopsis thaliana defense response to fungal necrotrophic pathogens. Acta Physiol Plant 32 1 10

17. GlazebrookJAusubelFM 1994 Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci U S A 91 8955 8959

18. ZhouNTootleTLGlazebrookJ 1999 Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11 2419 2428

19. FinkelshteinAShlezingerNBunisOSharonA 2011 Botrytis cinerea BcNma is involved in apoptotic cell death but not in stress adaptation. Fung Genet Biol 48 621 630

20. ItoS-iIharaTTamuraHTanakaSIkedaT 2007 [alpha]-Tomatine, the major saponin in tomato, induces programmed cell death mediated by reactive oxygen species in the fungal pathogen Fusarium oxysporum. FEBS Lett 581 3217 3222

21. SharonAFinkelshteinA 2009 Programmed cell death in fungus–plant interactions. EsserKDeisingH The Mycota 2 ed Heidelberg Springer 221 236

22. UrenAGBeilharzTO'ConnellMJBuggSJvan DrielR 1999 Role for yeast inhibitor of apoptosis (IAP)-like proteins in cell division. Proc Natl Acad Sci U S A 96 10170 10175

23. WalterDWissingSMadeoFFahrenkrogB 2006 The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in Saccaromyces cerevisiae and is a substrate for the yeast homologue of Omi/HtrA2. J Cell Sci 119 1843 1851

24. SharonAFinkelsteinAShlezingerNHatamI 2009 Fungal apoptosis: function, genes and gene function. FEMS Microbiol Rev 33 833 854

25. EscaffitFVauteOChevillard-BrietMSeguiBTakamiY 2007 Cleavage and cytoplasmic relocalization of histone deacetylase 3 are important for apoptosis progression. Mol Cell Biol 27 554 567

26. KonishiAShimizuSHirotaJTakaoTFanY 2003 Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 114 673 688

27. Veneault-FourreyCBarooahMEganMWakleyGTalbotNJ 2006 Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312 580 583

28. NesherIBarhoomSSharonA 2008 Cell cycle and cell death are not necessary for appressorium formation and plant infection in the fungal plant pathogen Colletotrichum gloeosporioides. BMC Biol 6 9

29. GlawischnigE 2007 Camalexin. Phytochemistry 68 401 406

30. DickmanMBParkYKOltersdorfTLiWClementeT 2001 Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci U S A 98 6957 6962

31. NurnbergerTBrunnerF 2002 Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr Opin Plant Biol 5 318 324

32. Van GijsegemFGeninSBoucherC 1993 Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Tren Microbiol 1 175 180

33. BakerBZambryskiPStaskawiczBDinesh-KumarSP 1997 Signaling in plant-microbe interactions. Science 276 726 733

34. BergeyDRHoweGARyanCA 1996 Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci U S A 93 12053 12058

35. Al-OlayanEMWilliamsGTHurdH 2002 Apoptosis in the malaria protozoan, Plasmodium berghei: a possible mechanism for limiting intensity of infection in the mosquito. Int J Parasitol 32 1133 1143

36. Fernandez-ArenasECabezonVBermejoCArroyoJNombelaC 2007 Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol Cel Prot 6 460 478

37. Jaso-FriedmannLLearyJHEvansDL 2000 Role of nonspecific cytotoxic cells in the induction of programmed cell death of pathogenic protozoans: participation of the fas ligand-fas receptor system. Exper Parasitol 96 75 88

38. SambrookJFritschEFManiatisT 1989 Molecular cloning: a laboratory manual. Cold spring harbor, NY Laboratory Press

39. SiewersVSmedsgaardJTudzynskiP 2004 The P450 monooxygenase BcABA1 is essential for abscisic acid biosynthesis in Botrytis cinerea. Appl Environ Microbiol 70 3868 3876

40. TurgeonBGGarberRCYoderOC 1985 Transformation of the fungal maize pathogen Cochliobolus heterostrophus using the Aspergillus nidulans amd gene. Mol Gen Genet 201 450 453

41. ChagueVDanitL-VSiewersVGronoverCSTudzynskiP 2006 Ethylene sensing and gene activation in Botrytis cinerea: a missing link in ethylene regulation of fungus-plant interactions? Mol Plant-Microbe Interact 19 33 42

42. GuzmanPEckerJR 1990 Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2 513 523

43. BarhoomSSharonA 2007 Bcl-2 proteins link programmed cell death with growth and morphogenetic adaptations in the fungal plant pathogen Colletotrichum gloeosporioides. Fungal Genet Biol 44 32 43

44. LevSSharonAHadarRMaHHorwitzBA 1999 A mitogen-activated protein kinase of the corn leaf pathogen Cochliobolus heterostrophus is involved in conidiation, appressorium formation, and pathogenicity: diverse roles for mitogen-activated protein kinase homologs in foliar pathogens. Proc Natl Acad Sci U S A 96 13542 13547

45. KeoghRCDeverallBJMcLeodS 1980 Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean. Trans British Mycol Soc 74 329 333

46. SemighiniCPHarrisSD 2009 Methods to detect apoptotic-like cell death in filamentous fungi. SharonA Molecular and Cell Biology Methods for Fungi Humana Press USA