Evolution of Linked Avirulence Effectors in Is Affected by Genomic Environment and Exposure to Resistance Genes in Host Plants

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Brassica napus (canola) cultivars and isolates of the blackleg fungus, Leptosphaeria maculans interact in a ‘gene for gene’ manner whereby plant resistance (R) genes are complementary to pathogen avirulence (Avr) genes. Avirulence genes encode proteins that belong to a class of pathogen molecules known as effectors, which includes small secreted proteins that play a role in disease. In Australia in 2003 canola cultivars with the Rlm1 resistance gene suffered a breakdown of disease resistance, resulting in severe yield losses. This was associated with a large increase in the frequency of virulence alleles of the complementary avirulence gene, AvrLm1, in fungal populations. Surprisingly, the frequency of virulence alleles of AvrLm6 (complementary to Rlm6) also increased dramatically, even though the cultivars did not contain Rlm6. In the L. maculans genome, AvrLm1 and AvrLm6 are linked along with five other genes in a region interspersed with transposable elements that have been degenerated by Repeat-Induced Point (RIP) mutations. Analyses of 295 Australian isolates showed deletions, RIP mutations and/or non-RIP derived amino acid substitutions in the predicted proteins encoded by these seven genes. The degree of RIP mutations within single copy sequences in this region was proportional to their proximity to the degenerated transposable elements. The RIP alleles were monophyletic and were present only in isolates collected after resistance conferred by Rlm1 broke down, whereas deletion alleles belonged to several polyphyletic lineages and were present before and after the resistance breakdown. Thus, genomic environment and exposure to resistance genes in B. napus has affected the evolution of these linked avirulence genes in L. maculans.

Vyšlo v časopise: Evolution of Linked Avirulence Effectors in Is Affected by Genomic Environment and Exposure to Resistance Genes in Host Plants. PLoS Pathog 6(11): e32767. doi:10.1371/journal.ppat.1001180
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001180

Souhrn

Zdroje

1. FittBDL

BrunH

BarbettiMJ

RimmerSR

2006 World-wide importance of phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus). Eur J Plant Pathol 114 3 15

2. FlorHH

1955 Host-parasite interactions in flax rust - its genetic and other implications. Phytopathology 45 680 685

3. BalesdentMH

AttardA

KuhnML

RouxelT

2002 New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology 92 1122 1133

4. YuF

LydiateDJ

RimmerSR

2005 Identification of two novel genes for blackleg resistance in Brassica napus. Theor Appl Genet 110 969 979

5. DelourmeR

ChevreAM

BrunH

RouxelT

BalesdentMH

2006 Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). Eur J Plant Pathol 114 41 52

6. YuF

LydiateDJ

RimmerSR

2008 Identification and mapping of a third blackleg resistance locus in Brassica napus derived from B. rapa subsp. sylvestris. Genome 51 64 72

7. RouxelT

BalesdentMH

2005 The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol Plant Pathol 6 225 241

8. FudalI

RossS

GoutL

BlaiseF

KuhnML

2007 Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Mol Plant Microbe Interact 20 459 470

9. GoutL

FudalI

KuhnML

BlaiseF

EckertM

2006 Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol Microbiol 60 67 80

10. ParlangeF

DaverdinG

FudalI

KuhnML

BalesdentMH

2009 Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol Microbiol 71 851 863

11. HogenhoutSA

Van der HoornRA

TerauchiR

KamounS

2009 Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact 22 115 122

12. StukenbrockEH

McDonaldBA

2009 Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Mol Plant Microbe Interact 22 371 380

13. SpragueSJ

BalesdentMH

BrunH

HaydenHL

MarcroftSJ

2006 Major gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence of populations of Leptosphaeria maculans in France and Australia. Eur J Plant Pathol 114 33 44

14. CrouchJH

LewisBG

MithenRF

1994 The effect of A genome substitution on the resistance of Brassica napus to infection by Leptosphaeria maculans. Plant Breeding 112 265 278

15. SpragueSJ

MarcroftSJ

HaydenHL

HowlettBJ

2006 Major gene resistance to blackleg in Brassica napus overcome within three years of commercial production in southeastern Australia. Plant Disease 90 190 198

16. Van de WouwAP

StonardJF

HowlettBJ

WestJS

FittBD

2010 Determining frequencies of avirulent alleles in airborne Leptosphaeria maculans inoculum using quantitative PCR. Plant Pathology 59 809 818

17. Van de WouwAP

MarcroftSJ

BarbettiMJ

HuaL

SalisburyPA

2009 Dual control of avirulence in Leptosphaeria maculans towards a Brassica napus cultivar with ‘sylvestris-derived’ resistance suggests involvement of two resistance genes. Plant Pathology 58 305 313

18. RouxelT

PenaudA

PinochetX

BrunH

GoutL

2003 A 10-year survey of populations of Leptosphaeria maculans in France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape. Eur J Plant Pathol 109 871 881

19. BrunH

ChevreAM

FittBD

PowersS

BesnardAL

2010 Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol 185 285 299

20. GoutL

KuhnML

VincenotL

Bernard-SamainS

CattolicoL

2007 Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environ Microbiol 9 2978 2992

21. SelkerEU

GarrettPW

1988 DNA sequence duplications trigger gene inactivation in Neurospora crassa. Proc Natl Acad Sci U S A 85 6870 6874

22. FudalI

RossS

BrunH

BesnardAL

ErmelM

2009 Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Mol Plant Microbe Interact 22 932 941

23. BrunH

LevivierS

SomdaI

RuerD

RenardM

2000 A field method for evaluating the potential durability of new resistance sources: application to the Leptosphaeria maculans-Brassica napus pathosystem. Phytopathology 90 961 966

24. CozijnsenAJ

HowlettBJ

2003 Characterisation of the mating-type locus of the plant pathogenic ascomycete Leptosphaeria maculans. Curr Genet 43 351 357

25. HaneJK

OliverRP

2008 RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinformatics 9 478

26. RepM

van der DoesHC

MeijerM

van WijkR

HoutermanPM

2004 A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol Microbiol 53 1373 1383

27. PondSL

FrostSD

MuseSV

2005 HyPhy: hypothesis testing using phylogenies. Bioinformatics 21 676 679

28. TamuraK

DudleyJ

NeiM

KumarS

2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599

29. KishinoH

HasegawaM

1989 Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol 29 170 179

30. McDonaldBA

LindeC

2002 Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40 349 379

31. RouxelT

WillnerE

CoudardL

BalesdentMH

2003 Screening and identification of resistance to Leptosphaeria maculans (stem canker) in Brassica napus accessions. Euphytica 133 219 231

32. CouchBC

FudalI

LebrunMH

TharreauD

ValentB

2005 Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice. Genetics 170 613 630

33. FarmanML

EtoY

NakaoT

TosaY

NakayashikiH

2002 Analysis of the structure of the AVR1-CO39 avirulence locus in virulent rice-infecting isolates of Magnaporthe grisea. Mol Plant Microbe Interact 15 6 16

34. RepM

2005 Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol Lett 253 19 27

35. MaLJ

van der DoesHC

BorkovichKA

ColemanJJ

DaboussiMJ

2010 Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464 367 373

36. FriesenTL

StukenbrockEH

LiuZ

MeinhardtS

LingH

2006 Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38 953 956

37. LiuZ

FarisJD

OliverRP

TanKC

SolomonPS

2009 SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLoS Pathog 5 e1000581

38. HaneJK

LoweRG

SolomonPS

TanKC

SchochCL

2007 Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19 3347 3368

39. HaasBJ

KamounS

ZodyMC

JiangRH

HandsakerRE

2009 Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461 393 398

40. 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

41. RepM

KistlerHC

2010 The genomic organization of plant pathogenicity in Fusarium species. Curr Opin Plant Biol 13 1 7

42. IrelanJT

HagemannAT

SelkerEU

1994 High frequency repeat-induced point mutation (RIP) is not associated with efficient recombination in Neurospora. Genetics 138 1093 1103

43. IdnurmA

HowlettBJ

2003 Analysis of loss of pathogenicity mutants reveals that repeat-induced point mutations can occur in the Dothideomycete Leptosphaeria maculans. Fungal Genet Biol 39 31 37

44. BrunnerPC

StefanatoFL

McDonaldBA

2008 Evolution of the CYP51 gene in Mycosphaerella graminicola: evidence for intragenic recombination and selective replacement. Mol Plant Pathol 9 305 316

45. van den BurgHA

WesterinkN

FrancoijsKJ

RothR

WoestenenkE

2003 Natural disulfide bond-disrupted mutants of AVR4 of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, circumvent Cf-4-mediated resistance, but retain their chitin binding ability. J Biol Chem 278 27340 27346

46. ChengJ

RandallAZ

SweredoskiMJ

BaldiP

2005 SCRATCH: a protein structure and structural feature prediction server. Nucleic Acids Res 33 W72 76

47. SchurchS

LindeCC

KnoggeW

JacksonLF

McDonaldBA

2004 Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Mol Plant Microbe Interact 17 1114 1125

48. StukenbrockEH

McDonaldBA

2007 Geographical variation and positive diversifying selection in the host-specific toxin SnToxA. Mol Plant Pathol 8 321 332

49. RozenS

SkaletskyH

2000 Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132 365 386

50. GardinerDM

CozijnsenAJ

WilsonLM

PedrasMS

HowlettBJ

2004 The sirodesmin biosynthetic gene cluster of the plant pathogenic fungus Leptosphaeria maculans. Mol Microbiol 53 1307 1318