Multiple Translocation of the Effector Gene among Chromosomes of the Rice Blast Fungus and Related Species
Magnaporthe oryzae is the causal agent of rice blast disease, a devastating problem worldwide. This fungus has caused breakdown of resistance conferred by newly developed commercial cultivars. To address how the rice blast fungus adapts itself to new resistance genes so quickly, we examined chromosomal locations of AVR-Pita, a subtelomeric gene family corresponding to the Pita resistance gene, in various isolates of M. oryzae (including wheat and millet pathogens) and its related species. We found that AVR-Pita (AVR-Pita1 and AVR-Pita2) is highly variable in its genome location, occurring in chromosomes 1, 3, 4, 5, 6, 7, and supernumerary chromosomes, particularly in rice-infecting isolates. When expressed in M. oryzae, most of the AVR-Pita homologs could elicit Pita-mediated resistance, even those from non-rice isolates. AVR-Pita was flanked by a retrotransposon, which presumably contributed to its multiple translocation across the genome. On the other hand, family member AVR-Pita3, which lacks avirulence activity, was stably located on chromosome 7 in a vast majority of isolates. These results suggest that the diversification in genome location of AVR-Pita in the rice isolates is a consequence of recognition by Pita in rice. We propose a model that the multiple translocation of AVR-Pita may be associated with its frequent loss and recovery mediated by its transfer among individuals in asexual populations. This model implies that the high mobility of AVR-Pita is a key mechanism accounting for the rapid adaptation toward Pita. Dynamic adaptation of some fungal plant pathogens may be achieved by deletion and recovery of avirulence genes using a population as a unit of adaptation.
Vyšlo v časopise:
Multiple Translocation of the Effector Gene among Chromosomes of the Rice Blast Fungus and Related Species. PLoS Pathog 7(7): e32767. doi:10.1371/journal.ppat.1002147
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002147
Souhrn
Magnaporthe oryzae is the causal agent of rice blast disease, a devastating problem worldwide. This fungus has caused breakdown of resistance conferred by newly developed commercial cultivars. To address how the rice blast fungus adapts itself to new resistance genes so quickly, we examined chromosomal locations of AVR-Pita, a subtelomeric gene family corresponding to the Pita resistance gene, in various isolates of M. oryzae (including wheat and millet pathogens) and its related species. We found that AVR-Pita (AVR-Pita1 and AVR-Pita2) is highly variable in its genome location, occurring in chromosomes 1, 3, 4, 5, 6, 7, and supernumerary chromosomes, particularly in rice-infecting isolates. When expressed in M. oryzae, most of the AVR-Pita homologs could elicit Pita-mediated resistance, even those from non-rice isolates. AVR-Pita was flanked by a retrotransposon, which presumably contributed to its multiple translocation across the genome. On the other hand, family member AVR-Pita3, which lacks avirulence activity, was stably located on chromosome 7 in a vast majority of isolates. These results suggest that the diversification in genome location of AVR-Pita in the rice isolates is a consequence of recognition by Pita in rice. We propose a model that the multiple translocation of AVR-Pita may be associated with its frequent loss and recovery mediated by its transfer among individuals in asexual populations. This model implies that the high mobility of AVR-Pita is a key mechanism accounting for the rapid adaptation toward Pita. Dynamic adaptation of some fungal plant pathogens may be achieved by deletion and recovery of avirulence genes using a population as a unit of adaptation.
Zdroje
1. HeathMC 1981 A generalized concept of host-parasite specificity. Phytopathology 71 1121 1123
2. KiyosawaS 1982 Genetics and epidemiological modeling of breakdown of plant disease resistance. Ann Rev Phytopathol 20 93 117
3. LeachJECruzCMVBaiJLeungH 2001 Pathogen fitness penalty as a predictor of durability of disease resistance genes. Ann Rev Phytopathol 39 187 224
4. McDonaldBALindeC 2002 Pathogen population genetics, evolutionary potential, and durable resistance. Ann Rev Phytopathol 40 349 379
5. FlorHH 1956 The complementary genic systems in flax and flax rust. Adv Genet 8 29 54
6. FudalIRossSBrunHBesnardA-LErmelM 2009 Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Mol Plant-Microbe Interact 22 932 941
7. Van de WouwAPCozijnsenAJHaneJKBrunnerPCMcDonaldBA 2010 Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog 6 e1001180
8. De WitPJGMMehrabiRvan den BurgHAStergiopoulosI 2009 Fungal effector proteins: past, present and future. Mol Plant Pathol 10 735 747
9. GoutLKuhnMLVincenotLBernard-SamainSCattolicoL 2007 Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Envion Microbiol 9 2978 2992
10. SchürchSLindeCCKnoggeWJacksonLFMcDonaldBA 2004 Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Mol Plant-Microbe Interact 17 1114 1125
11. KiyosawaSAndoIIshiguroKNemotoFHashimotoA 1991 Three examples of yearly change of frequencies of unnecessary virulence genes under field conditions where resistance genes for rice blast are not present. Bull Fukushima Pref Agri Exp Stn 30 23 36
12. HirataKKusabaMChumaIOsueJNakayashikiH 2007 Speciation in Pyricularia inferred from multilocus phylogenetic analysis. Mycol Res 111 799 808
13. KatoHYamamotoMYamaguchi-OzakiTKadouchiHIwamotoY 2000 Pathogenicity, mating ability and DNA restriction fragment length polymorphisms of Pyricularia populations isolated from Gramineae, Bambusideae and Zingiberaceae plants. J Gen Plant Pathol 66 30 47
14. CouchBCKohnLM 2002 A multilocus gene genealogy concordant with host preference indicates segregation of a new species, Magnaporthe oryzae, from M. grisea. Mycologia 94 683 693
15. TosaYHirataKTambaHNakagawaSChumaI 2004 Genetic constitution and pathogenicity of Lolium isolates of Magnaporthe oryzae in comparison with host species-specific pathotypes of the blast fungus. Phytopathology 94 454 462
16. KatoH 1983 Responses of Italian millet, oat, timothy, Italian ryegrass and perennial ryegrass to Pyricularia species isolated from cereals and grasses. Proc Kanto-Tosan Plant Prot Soc 30 22 23 (In Japanese)
17. ZeiglerRSScottRPLeungHBordeosAAKumarJ 1997 Evidence of parasexual exchange of DNA in the rice blast fungus challenges its exclusive clonality. Phytopathology 87 284 294
18. KatoHYamaguchiTNishiharaN 1976 The perfect state of Pyricularia oryzae Cav. in culture. Ann Phytopathol Soc Jpn 42 507 510
19. YaegashiHNishiharaN 1976 Production of the perfect stage in Pyricularia from cereals and grasses. Ann Phytopathol Soc Jpn 42 511 515
20. UeyamaATsudaM 1975 Formation of the perfect state in culture of Pyricularia sp. from some graminaceous plants (preliminary report). Trans Mycol Soc Jpn 16 420 422
21. TakabayashiNTosaYOhHSMayamaS 2002 A gene-for-gene relationship underlying the species-specific parasitism of Avena/Triticum isolates of Magnaporthe grisea on wheat cultivars. Phytopathology 92 1182 1188
22. TosaYTambaHTanakaKMayamaS 2006 Genetic analysis of host species specificity of Magnaporthe oryzae isolates from rice and wheat. Phytopathology 96 480 484
23. ValentBKhangCH 2010 Recent advances in rice blast effector research. Curr Opin Plant Biol 13 434 441
24. SilueDNotteghemJLTharreauD 1992 Evidence of a gene-for-gene relationship in the Oryza sativa – Magnaporthe grisea pathosystem. Phytopathology 82 577 580
25. KangSSweigardJAValentB 1995 The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 8 939 948
26. SweigardJACarrollAMKangSFarrallLChumleyFG 1995 Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7 1221 1233
27. FarmanMLLeongSA 1998 Chromosome walking to the AVR1-CO39 avirulence gene of Magnaporthe grisea: Discrepancy between the physical and genetic maps. Genetics 150 1049 1058
28. OrbachMJFarrallLSweigardJAChumleyFGValentB 2000 A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12 2019 2032
29. BöhnertHUFudalIDiohWTharreauDNotteghemJ-L 2004 A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistance rice. Plant Cell 16 2499 2513
30. LiWWangBWuJLuGHuY 2009 The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol Plant-Microbe Interact 22 411 420
31. MikiSMatsuiKKitoHOtsukaKAshizawaT 2009 Molecular cloning and characterization of the AVR-Pia locus from a Japanese field isolate of Magnaporthe oryzae. Mol Plant Pathol 10 361 374
32. YoshidaKSaitohHFujisawaSKanzakiHMatsumuraH 2009 Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21 1573 1591
33. DaiYJiaYCorrellJWangXWangY 2010 Diversification and evolution of the avirulence gene AVR-Pita1 in field isolates of Magnaporthe oryzae. Fun Genet Biol 37 973 980
34. KangSLebrunMHFarrallLValentB 2001 Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Mol Plant-Microbe Interact 14 671 674
35. TakahashiMAshizawaTHirayaeKMoriwakiJSoneT 2010 One of two major paralogs of AVR-Pita1 is functional in Japanese rice blast isolates. Phytopathology 100 612 618
36. ZhouEJiaYSinghPCorrellJCLeeFN 2007 Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genet Biol 44 1024 1034
37. BryanGTWuKSFarrallLJiaYHersheyHP 2000 A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12 2033 2045
38. JiaYMcAdamsSABryanGTHersheyHPValentB 2000 Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19 4004 4014
39. KhangCHParkS-YLeeY-HValentBKangS 2008 Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. Mol Plant-Microbe Interact 21 658 670
40. BerrimanMGhedinEHertz-FowlerCBlandinGRenauldH 2005 The genome of the African trypanosome Trypanosoma brucei. Science 309 416 422
41. DreesenOLiBCrossGAM 2007 Telomere structure and function in trypanosomes: a proposal. Nat Rev Microbiol 5 70 75
42. TaylorJERudenkoG 2006 Switching trypanosome coats: what's in the wardrobe? Trends in Genet 22 614 620
43. GardnerMJHallNFungEWhiteOBerrimanM 2002 Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419 498 511
44. Freitas-JuniorLHBottiusEPirritLADeitschKWScheidigC 2000 Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407 1018 1022
45. LuoCXHanamuraHSezakiHKusabaMYaegashiH 2002 Relationship between avirulence genes of the same family in rice blast fungus Magnaporthe grisea. J Gen Plant Pathol 68 300 306
46. LuoCXYinLFKoyanagiSFarmanMLKusabaM 2005 Genetic mapping and chromosomal assignment of Magnaporthe oryzae avirulence genes AvrPik, AvrPiz, and AvrPiz-t controlling cultivar specificity on rice. Phytopathology 95 640 647
47. NittaNFarmanMLLeongSA 1997 Genome organization of Magnaporthe grisea: integration of genetic maps, clustering of transposable elements and identification of genome duplications and rearrangements. Theor Appl Genet 95 20 32
48. ChumaITosaYTagaMNakayashikiHMayamaS 2003 Meiotic behavior of a supernumerary chromosome in Magnaporthe oryzae. Curr Genet 43 191 198
49. OrbachMJChumleyFGValentB 1996 Electrophoretic karyotypes of Magnaporthe grisea pathogens of diverse grasses. Mol Plant-Microbe Interact 9 261 271
50. TalbotNJSalchYPMaMHamerJE 1993 Karyotypic variation within clonal lineages of the rice blast fungus, Magnaporthe grisea. Appl Environ Microbiol 59 585 593
51. ChumaIZhanS-WAsanoSNgaNTTVyTTP 2010 PWT1, an avirulence gene of Magnaporthe oryzae tightly linked to the rDNA locus, is recognized by two staple crops, common wheat and barley. Phytopathology 100 436 443
52. ZhengYZhangGLinFWangZJinG 2008 Development of microsatellite markers and construction of genetic map in rice blast pathogen Magnaporthe grisea. Fungal Genet Biol 45 1340 1347
53. NakayashikiHMatsuoHChumaIIkedaKBetsuyakuS 2001 Pyret, a Ty3/gypsy retrotransposon in Magnaporthe grisea contains an extra domain between the nucleocapsid and protease domains. Nucleic Acids Res 29 4106 4113
54. KangS 2001 Organization and distribution pattern of MGLR-3, a novel retrotransposon in the rice blast fungus Magnaporthe grisea. Fungal Genet Biol 32 11 19
55. HamerJEFarrallLOrbachMJValentBChumleyFG 1989 Host species-specific conservation of a family of repeated DNA sequences in the genome of a fungal plant pathogen. Proc Natl Acad Sci USA 86 9981 9985
56. KachrooPAhujaMLeongSAChattooBB 1997 Organization and molecular analysis of repeated DNA sequences in the rice blast fungus Magnaporthe grisea. Curr Genet 31 361 369
57. KachrooPLeongSAChattooBB 1994 Pot2, an inverted repeat transposon from the rice blast fungus Magnaporthe grisea. Mol Gen Genet 245 339 348
58. FarmanMLTauraSLeongSA 1996 The Maganaporthe grisea DNA fingerprinting probe MGR586 contains the 3' end of an inverted repeat transposon. Mol Gen Genet 251 675 681
59. KitoHTakahashiYSatoJFukiyaSSoneT 2003 Occan, a novel transposon in the Fot1 family, is ubiquitously found in several Magnaporthe grisea isolates. Curr Genet 42 322 331
60. FarmanMLTosaYNittaNLeongSA 1996 MAGGY, a retrotransposon in the genome of the rice blast fungus Magnaporthe grisea. Mol Gen Genet 251 665 674
61. AboukhaddourRCloutierSBallanceGMLamariL 2009 Genome characterization of Pyrenophora tritici-repentis isolates reveals high plasticity and independent chromosomal location of ToxA and ToxB. Mol Plant Pathol 10 201 212
62. MieczkowskiPALemoineFJPetesTD 2006 Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA repair 5 1010 1020
63. Van der PlankJE 1984 Disease Resistance in Plants. Academic Press, Inc 194
64. MurataSTakasakiNSaitohMOkadaN 1993 Determination of the phylogenetic relationships among Pacific salmonids by using short interspersed elements (SINEs) as temporal landmarks of evolution. Proc Natl Acad Sci USA 90 6995 6999
65. CovertSF 1998 Supernumerary chromosomes in filamentous fungi. Curr Genet 33 311 319
66. MiaoVPCovertSFVanEttenHD 1991 A fungal gene for antibiotic resistance on a dispensable (“B”) chromosome. Science 254 1773 1776
67. HanYLiuXBennyUKistlerCVanEttenHD 2001 Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J 25 305 314
68. AkagiYAkamatsuHOtaniHKodamaM 2009 Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8 1732 1738
69. HattaRItoKHosakiYTanakaTTanakaA 2002 A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161 59 70
70. JohnsonLJJohnsonRDAkamatsuHSalamiahAOtaniH 2001 Spontaneous loss of a conditionally dispensable chromosome from the Alternaria alternata apple pathotype leads to loss of toxin production and pathogenicity. Curr Genet 40 65 72
71. MasunakaAOhtaniKPeeverTLTimmerLWTsugeT 2005 An isolate of Alternaria alternata that is pathogenic to both tangerines and rough lemon and produces two host-selective toxins, ACT- and ACR-toxins. Phytopathology 95 241 247
72. ColemanJJRounsleySDRodriguez-CarresMKuoAWasmannCC 2009 The genome of Nectria haematococca: Contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5 e1000618
73. HeCRusuAGPoplawskiAMIrwinJAGMannersJM 1998 Transfer of a supernumerary chromosome between vegetatively incompatible biotypes of the fungus Colletotrichum gloeosporioides. Genetics 150 1459 1466
74. MaLJvan der DoesHCBorkovichKAColemanJJDaboussiMJ 2010 Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464 367 373
75. NoguchiMTYasudaNFujitaY 2006 Evidence of genetic exchange by parasexual recombination and genetic analysis of pathogenicity and mating type of parasexual recombinants in rice blast fungus, Magnaporthe oryzae. Phytopathology 96 746 750
76. YasudaNTsujimoto-NoguchiMFujitaY 2006 Partial mapping of avirulence genes AVR-Pii and AVR-Pia in the rice blast fungus Magnaporthe oryzae. Can J Plant Pathol 28 494 498
77. ChenQHWangYCLiANZhangZGZhengXB 2007 Molecular mapping of two cultivar-specific avirulence genes in the rice blast fungus Magnaporthe grisea. Mol Genet Genomics 277 139 148
78. FengSMaJLinFWangLPanQ 2007 Construction of an electronic physical map of Magnaporthe oryzae using genomic position-ready SSR markers. Chin Sci Bull 52 3346 3354
79. LuoCXYinLFOhtakaKKusabaM 2007 The 1.6 Mb chromosome carrying the avirulence gene AvrPik in Magnaporthe oryzae isolate 84R-62B is a chimera containing chromosome 1 sequences. Mycol Res 111 232 239
80. JonesJDGDanglJL 2006 The plant immune system. Nature 444 323 329
81. CarlsonMCelenzaJLEngFJ 1985 Evolution of the dispersed SUC gene family of Saccharomyces by rearrangements of chromosome telomeres. Mol Cell Biol 5 2894 2902
82. CharronMJReadEHautSRMichelsCA 1989 Molecular evolution of the telomere-associated MAL loci of Saccharomyces. Genetics 122 307 316
83. BrownCAMurrayAWVerstrepenKJ 2010 Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 20 895 903
84. DiohWTharreauDNotteghemJLOrbachMJLebrunM-H 2000 Mapping of avirulence genes in the rice blast fungus, Magnaporthe grisea, with RFLP and RAPD markers. Mol Plant-Microbe Interact 13 217 227
85. FarmanML 2007 Telomeres in the rice blast fungus Magnaporthe oryzae: the world of the end as we know it. FEMS Microbiol Lett 273 125 132
86. ValentBChumleyFG 1994 Avirulence genes and mechanisms of genetic instability in the rice blast fungus. ZeiglerRSLeongSATengPS The Rice Blast Disease Cambridge International Rice Research Institute, Los Banos and Commonwealth Agricultural Bureaux 111 134 Chapter 7
87. RehmeyerCLiWKusabaMKimY-SBrownD 2006 Organization of chromosome ends in the rice blast fungus, Magnaporthe oryzae. Nucl Acid Res 34 4685 4701
88. VerstrepenKKFinkGR 2009 Genetic and epigenetic mechanisms underlying cell-surface variability in protozoa and fungi. Annu Rev Genet 43 1 24
89. MurakamiJTosaYKataokaTTomitaRKawasakiJ 2000 Analysis of host species specificity of Magnaporthe grisea toward wheat using a genetic cross between isolates from wheat and foxtail millet. Phytopathology 90 1060 1067
90. NakayashikiHKiyotomiKTosaYMayamaS 1999 Transposition of the retrotransposon MAGGY in heterologous species of filamentous fungi. Genetics 153 693 703
91. RömlingUTümmlerB 2000 Achieving 100% type ability of Pseudomonas aeruginosa by pulsed-field gel electrophoresis. J Clin Microbiol 38 464 465
92. TamuraKDudleyJNeiMKumarS 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24 1596 1599
93. KimuraNTsugeT 1993 Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J Bacteriol 175 4427 4435
94. TosaYOsueJEtoYOhHNakayashikiH 2005 Evolution of an avirulence gene, AVR1-CO39, concomitant with the evolution and differentiation of Magnaporthe oryzae. Mol Plant-Microbe Interact 18 1148 1160
95. RonquistFHülsenbeckJP 2003 MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 1572 1574
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 7
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Requires Glycerol for Maximum Fitness During The Tick Phase of the Enzootic Cycle
- Comparative Genomics Yields Insights into Niche Adaptation of Plant Vascular Wilt Pathogens
- The Role of IL-15 Deficiency in the Pathogenesis of Virus-Induced Asthma Exacerbations
- “Persisters”: Survival at the Cellular Level