#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Finished Genome of the Fungal Wheat Pathogen Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis


The plant-pathogenic fungus Mycosphaerella graminicola (asexual stage:
Septoria tritici) causes septoria tritici blotch, a disease that greatly reduces the yield and quality of wheat. This disease is economically important in most wheat-growing areas worldwide and threatens global food production. Control of the disease has been hampered by a limited understanding of the genetic and biochemical bases of pathogenicity, including mechanisms of infection and of resistance in the host. Unlike most other plant pathogens, M. graminicola has a long latent period during which it evades host defenses. Although this type of stealth pathogenicity occurs commonly in Mycosphaerella and other Dothideomycetes, the largest class of plant-pathogenic fungi, its genetic basis is not known. To address this problem, the genome of M. graminicola was sequenced completely. The finished genome contains 21 chromosomes, eight of which could be lost with no visible effect on the fungus and thus are dispensable. This eight-chromosome dispensome is dynamic in field and progeny isolates, is different from the core genome in gene and repeat content, and appears to have originated by ancient horizontal transfer from an unknown donor. Synteny plots of the M. graminicola chromosomes versus those of the only other sequenced Dothideomycete, Stagonospora nodorum, revealed conservation of gene content but not order or orientation, suggesting a high rate of intra-chromosomal rearrangement in one or both species. This observed “mesosynteny” is very different from synteny seen between other organisms. A surprising feature of the M. graminicola genome compared to other sequenced plant pathogens was that it contained very few genes for enzymes that break down plant cell walls, which was more similar to endophytes than to pathogens. The stealth pathogenesis of M. graminicola probably involves degradation of proteins rather than carbohydrates to evade host defenses during the biotrophic stage of infection and may have evolved from endophytic ancestors.


Vyšlo v časopise: Finished Genome of the Fungal Wheat Pathogen Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis. PLoS Genet 7(6): e32767. doi:10.1371/journal.pgen.1002070
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002070

Souhrn

The plant-pathogenic fungus Mycosphaerella graminicola (asexual stage:
Septoria tritici) causes septoria tritici blotch, a disease that greatly reduces the yield and quality of wheat. This disease is economically important in most wheat-growing areas worldwide and threatens global food production. Control of the disease has been hampered by a limited understanding of the genetic and biochemical bases of pathogenicity, including mechanisms of infection and of resistance in the host. Unlike most other plant pathogens, M. graminicola has a long latent period during which it evades host defenses. Although this type of stealth pathogenicity occurs commonly in Mycosphaerella and other Dothideomycetes, the largest class of plant-pathogenic fungi, its genetic basis is not known. To address this problem, the genome of M. graminicola was sequenced completely. The finished genome contains 21 chromosomes, eight of which could be lost with no visible effect on the fungus and thus are dispensable. This eight-chromosome dispensome is dynamic in field and progeny isolates, is different from the core genome in gene and repeat content, and appears to have originated by ancient horizontal transfer from an unknown donor. Synteny plots of the M. graminicola chromosomes versus those of the only other sequenced Dothideomycete, Stagonospora nodorum, revealed conservation of gene content but not order or orientation, suggesting a high rate of intra-chromosomal rearrangement in one or both species. This observed “mesosynteny” is very different from synteny seen between other organisms. A surprising feature of the M. graminicola genome compared to other sequenced plant pathogens was that it contained very few genes for enzymes that break down plant cell walls, which was more similar to endophytes than to pathogens. The stealth pathogenesis of M. graminicola probably involves degradation of proteins rather than carbohydrates to evade host defenses during the biotrophic stage of infection and may have evolved from endophytic ancestors.


Zdroje

1. EyalZSchareALPrescottJMvan GinkelM 1987 The Septoria Diseases of Wheat: Concepts and Methods of Disease Management Mexico, DF CIMMYT

2. HardwickNVJonesDRSloughJE 2001 Factors affecting diseases of winter wheat in England and Wales, 1989–98. Plant Pathol 50 453 462

3. McDougallP 2006 Phillips McDougall Agriservice Report Scotland, UK Pathhead, Midlothian

4. LindeCCZhanJMcDonaldBA 2002 Population structure of Mycosphaerella graminicola: From lesions to continents. Phytopathology 92 946 955

5. KemaGHJYuDRijkenbergFHJShawMWBaayenRP 1996 Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86 777 786

6. DuncanKEHowardRJ 2000 Cytological analysis of wheat infection by the leaf blotch pathogen Mycosphaerella graminicola. Mycol Res 104 1074 1082

7. JingH-CLovellDGutteridgeRJenkDKornyukhinD 2008 Phenotypic and genetic analysis of the Triticum monococcum–Mycosphaerella graminicola interaction. New Phytol 179 1121 1132

8. AdhikariTBBalajiBBreedenJGoodwinSB 2007 Resistance of wheat to Mycosphaerella graminicola involves early and late peaks of gene expression. Physiol Mol Plant Pathol 71 55 68

9. KemaGHJvan der LeeTAJMendesOVerstappenECPLankhorstRK 2008 Large-scale gene discovery in the septoria tritici blotch fungus Mycosphaerella graminicola with a focus on in planta expression. Mol Plant-Microbe Interact 21 1249 1260

10. KeonJAntoniwJCarzanigaRDellerSWardJL 2007 Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Mol Plant-Microbe Interact 20 178 193

11. WittenbergAHJvan der LeeTAJBen M'BarekSWareSBGoodwinSB 2009 Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS ONE 4 e5863 doi:10.1371/journal.pone.0005863

12. ChainPSGrafhamDVFultonRSFitzGeraldMGHostetlerJ 2009 Genome project standards in a new era of sequencing. Science 326 236 237

13. NiermanWCPainAAndersonMJWortmanJRKimHS 2005 Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438 1151 1156

14. TorrianiSFFGoodwinSBKemaGHJPangilinanJLMcDonaldBA 2008 Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 45 628 637

15. SelkerEU 2002 Repeat-induced gene silencing in fungi. Adv Genet 46 439 450

16. CambareriEBJensenBCSchabtachESelkerEU 1989 Repeat-induced G-C to A-T mutations in Neurospora. Science 244 1571 1575

17. DhillonBCavalettoJRWoodKVGoodwinSB 2010 Accidental amplification and inactivation of a methyltransferase gene eliminates cytosine methylation in Mycosphaerella graminicola. Genetics 186 67 77

18. GardnerPPDaubJTateJGNawrockiEPKolbeDL 2008 Rfam: updates to the RNA families database. Nucleic Acids Res 37 D136 D140

19. LeeH-CLiLGuWXueZCrosthwaiteSK 2010 Diverse pathways generate microRNA-like RNAs and dicer-independent small interfering RNAs in fungi. Molecular Cell 38 803 814

20. FedorovaNDKhaldiNJoardarVSMaitiRAmedeoP 2008 Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4 e1000046 doi:10.1371/journal.pgen.1000046

21. MaL-Jvan der DoesHCBorkovichKAColemanJJDaboussiM-J 2010 Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464 367 373

22. KaySHahnSMaroisEHauseGBonasU 2007 A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318 648 651

23. GilesNHGeeverRFAschDKAvalosJCaseME 1991 Organization and regulation of the qa (quinic acid) genes in Neurospora crassa and other fungi. J Hered 82 1 7

24. MartinFKohlerAMuratCBalestriniRCoutinhoPM 2010 Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464 1033 1038

25. YunSHArieTKanekoIYoderOCTurgeonBG 2000 Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet Biol 31 7 20

26. DeanRATalbotNJEbboleDJFarmanMLMitchellTK 2005 The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434 980 986

27. CuomoCAGüldenerUXuJ-RTrailFTurgeonBG 2007 The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317 1400 1402

28. CantarelBLCoutinhoPMRancurelCBernardTLombardV 2009 The Carbohydrate-Active enZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37 D233 D238

29. Caracuel-RiosZTalbotNJ 2007 Cellular differentiation and host invasion by the rice blast fungus Magnaporthe grisea. Curr Opin Microbiol 10 339 345

30. JonesRNViegasWHoubenA 2008 A century of B chromosomes in plants: so what?. Ann Bot 101 767 775

31. JonesNHoubenA 2003 B chromosomes in plants: escapees from the A chromosome genome? Trends Plant Sci 8 417 423

32. CovertSF 1998 Supernumerary chromosomes in filamentous fungi. Curr Genet 33 311 319

33. MiaoVPCovertSFVanEttenHD 1991 A fungal gene for antibiotic resistance on a dispensable (“B”) chromosome. Science 254 1773 1776

34. HattaRItoKHosakiYTanakaTTanakaA 2002 A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161 59 70

35. WangCSkrobekAButtTM 2003 Concurrence of losing a chromosome and the ability to produce destruxins in a mutant of Metarhizium anisopliae. FEMS Microbiol Lett 226 373 378

36. MaselAMHeCZPoplawskiAMIrwinJAGMannersJM 1996 Molecular evidence for chromosome transfer between biotypes of Colletotrichum gloeosporioides. Mol Plant-Microbe Interact 9 339 348

37. ColemanJJRounsleySDRodriguez-CarresMKuoAWasmannCC 2009 The genome of Nectria haematococca: Contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5 e1000618 doi:10.1371/journal.pgen.1000618

38. WareSB 2006 Aspects of sexual reproduction in Mycosphaerella species on wheat and barley: genetic studies on specificity, mapping, and fungicide resistance. Wageningen University, The Netherlands: Ph.D. thesis

39. StukenbrockEHJørgensenFGZalaMHansenTTMcDonaldBA 2010 Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola. PLoS Genet 6 e1001189 doi:10.1371/journal.pgen.1001189

40. StukenbrockEHBankeSJavan-NikkhahMMcDonaldBA 2007 Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol Biol Evol 24 398 411

41. JamesTKauffFSchochCLMathenyPBHofstetterV 2006 Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443 818 822

42. HousworthEAPostlethwaitJ 2002 Measures of synteny conservation between species pairs. Genetics 162 441 448

43. MartinFAertsAAhrénDBrunADanchinEGJ 2008 The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452 88 92

44. AparicioSChapmanJStupkaEPutnamNChiaJ-M 2002 Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297 1301 1310

45. SalamovASolovyevVV 2000 Ab initio gene finding in Drosophila genomic DNA. Genome Res 10 516 522

46. BirneyEDurbinR 2000 Using GeneWise in the Drosophila annotation experiment. Genome Res 10 547 548

47. ZdobnovEMApweilerR 2001 InterProScan – an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17 847 848

48. KanehisaMGotoSKawashimaSOkunoYHattoriM 2004 The KEGG resource for deciphering the genome. Nucleic Acids Res 32 D277 D280

49. AshburnerMBallCABlakeJABotsteinDButlerH 2000 Gene Ontology: tool for the unification of biology. Nat Genet 25 25 29

50. TatusovRLFedorovaNDJacksonJDJacobsARKiryutinB 2003 The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4 41

51. KooninEVFedorovaNDJacksonJDJacobsARKrylovDM 2004 A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome Biol 5 R7

52. Griffiths-JonesSMoxonSMarshallMKhannaAEddySR 2005 Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 33 D121 D124

53. KurtzSPhillippyADelcherALSmootMShumwayM 2004 Versatile and open software for comparing large genomes. Genome Biology 5 R12

54. HaneJKLoweRGTSolomonPSTanK-CSchochCL 2007 Dothideomycete–plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. The Plant Cell 19 3347 3368

55. CooleyRNCatenCE 1991 Variation in electrophoretic karyotype between strains of Septoria nodorum. Mol Gen Genet 228 17 23

56. de VriesRPFrisvadJCvan de VondervoortPJIBurgersKKuijpersAFA 2005 Aspergillus vadensis, a new species of the group of black Aspergilli. Antonie Van Leeuwenhoek 87 195 203

57. KrzywinskiMScheinJBirolIConnorsJGascoyneR 2009 Circos: An information aesthetic for comparative genomics. Genome Res 19 1639 1645

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 6
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

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#