Unusual evolutionary mechanisms to escape effector-triggered immunity in the fungal phytopathogen Leptosphaeria maculans

Molecular Ecology

Volumn 26, Issue 7, 2017, Pages 2183-2198

  Plissonneau, C ^a,b   Blaise, F ^a   Ollivier, B ^a   Leflon, M ^c   Carpezat, J ^c   Rouxel, T ^a   Balesdent, M H ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b ETH ZURICH   (Switzerland)

^c Terres Inovia   (France)

Author keywords

effector; evolution; fitness; gene for gene interaction; oilseed rape; stem canker

Indexed keywords

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ASCOMYCETES; DISEASE RESISTANCE; EVOLUTION; FUNGAL GENE; GENE FREQUENCY; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHENOTYPE; PLANT DISEASE; PLANT IMMUNITY; POPULATION GENETICS; PROTEIN SECONDARY STRUCTURE; RAPESEED; VIRULENCE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ASCOMYCOTA; BIOLOGICAL EVOLUTION; BRASSICA NAPUS; DISEASE RESISTANCE; GENE FREQUENCY; GENES, FUNGAL; GENETICS, POPULATION; MUTATION; PHENOTYPE; PLANT DISEASES; PLANT IMMUNITY; POLYMORPHISM, GENETIC; PROTEIN STRUCTURE, SECONDARY; SELECTION, GENETIC; VIRULENCE;

EID: 85015230819     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.14046     Document Type: Article

References (63)

1. Aguileta G, Refrégier G, Yockteng R, Fournier E, Giraud T (2009) Rapidly evolving genes in pathogens: methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infection, Genetics and Evolution, 9, 656–670.
2. Ansan-Melayah D, Balesdent M-H, Buée M, Rouxel T (1995) Genetic characterization of AvrLm1, the first avirulence gene of Leptosphaeria maculans. Phytopathology, 85, 1525–1529.
3. Balesdent M-H, Attard A, Kühn ML, Rouxel T (2002) New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology, 92, 1122–1133.
4. Balesdent M-H, Barbetti M, Li H, Sivasithamparam K, Gout L, Rouxel T (2005) Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology, 95, 1061–1071.
5. Balesdent M-H, Louvard K, Pinochet X, Rouxel T (2006) A large-scale survey of races of Leptosphaeria maculans occurring on oilseed rape in France. European Journal of Plant Pathology, 114, 53–65.
6. Balesdent M-H, Fudal I, Ollivier B et al. (2013) The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytologist, 198, 887–898.
7. Balesdent M-H, Plissonneau C, Coudard L et al. (2015) Résistance du colza au phoma : où en est l'efficacité de Rlm7 ? Phytoma, 684, 20–24.
8. Blondeau K, Blaise F, Graille M et al. (2015) Crystal structure of the effector AvrLm4-7 of Leptosphaeria maculans reveals insights into its translocation into plant cell and recognition by resistance proteins. The Plant Journal, 83, 610–624.
9. Bourras S, McNally KE, Ben-David R et al. (2016) Multiple avirulence loci and allele-specific effector recognition control the Pm3 race-specific resistance of wheat to powdery mildew. The Plant Cell, 27, 2991–3012.
10. Brown JKM (2015) Durable resistance of crops to disease: a Darwinian perspective. Annual Review of Phytopathology, 53, 513–539.
11. Brun H, Chèvre A-M, Fitt BDL et al. (2010) Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytologist, 185, 285–299.
12. Chen Y, Liu Z, Halterman DA (2012) Molecular determinants of resistance activation and suppression by Phytophthora infestans effector IPI-O. PLoS Pathogen, 8, e1002595.
13. Chen C, Lian B, Hu J et al. (2013) Genome comparison of two Magnaporthe oryzae field isolates reveals genome variations and potential virulence effectors. BMC Genomics, 14, 887.
14. Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research, 16, 10881–10890.
15. Daverdin G, Rouxel T, Gout L et al. (2012) Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PloS Pathogens, 8, e1003020.
16. Delourme R, Chèvre A-M, Brun H et al. (2006) Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). European Journal of Plant Pathology, 114, 41–52.
17. Dilmaghani A, Balesdent MH, Didier JP et al. (2009) The Leptosphaeria maculans – Leptosphaeria biglobosa species complex in the American continent. Plant Pathology, 58, 1044–1058.
18. Dodds PN, Lawrence GJ, Catanzariti A-M et al. (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proceedings of the National Academy of Sciences of the United States of America, 103, 8888–8893.
19. Fitt BDL, Brun H, Barbetti MJ, Rimmer SR (2006) World-Wide importance of phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus). European Journal of Plant Pathology, 114, 3–15.
20. Flor HH (1955) Host-parasite interaction in flax rust – its genetics and other implications. Phytopathology, 45, 680–685.
21. Fudal I, Ross S, Gout L et al. (2007) Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Molecular Plant-Microbe Interaction, 20, 459–470.
22. Fudal I, Ross S, Brun H et al. (2009) Repeat-Induced Point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Molecular Plant-Microbe Interaction, 22, 932–941.
23. Galagan JE, Selker EU (2004) RIP: the evolutionary cost of genome defense. Trends in Genetics, 20, 417–423.
24. Ghanbarnia K, Fudal I, Larkan NJ et al. (2014) Rapid identification of the Leptosphaeria maculans avirulence gene AvrLm2, using an intraspecific comparative genomics approach. Molecular Plant Pathology, 16, 699–709.
25. Gout L, Fudal I, Kuhn M-L et al. (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Molecular Microbiology, 60, 67–80.
26. Gout L, Kuhn ML, Vincenot L et al. (2007) Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environmental Microbiology, 9, 2978–2992.
27. Hane JK, Oliver RP (2008) RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinformatics, 9, 478.
28. Houterman PM, Cornelissen BJC, Rep M (2008) Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathogens, 4, e1000061.
29. Houterman PM, Ma L, Van Ooijen G et al. (2009) The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly. The Plant Journal, 58, 970–978.
30. Huang Y-J, Balesdent M-H, Li Z-Q, Evans N, Rouxel T, Fitt BDL (2010) Fitness cost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeria maculans (phoma stem canker of oilseed rape). European Journal of Plant Pathology, 126, 279–291.
31. Huang J, Si W, Deng Q, Liand P, Yang S (2014a) Rapid evolution of avirulence genes in rice blast fungus Magnaporthe oryzae. BMC Genetics, 15, 45.
32. Huang YJ, Qi A, King GJ, Fitt BDL (2014b) Assessing quantitative resistance against Leptosphaeria maculans (Phoma Stem Canker) in Brassica napus (Oilseed Rape) in young plants. PLoS ONE, 9, e84924.
33. Iida Y, van ‘t Hof P, Beenen H et al. (2015) Novel mutations detected in avirulence genes overcoming tomato Cf resistance genes in isolates of a Japanese population of Cladosporium fulvum. PLoS ONE, 10, e0123271.
34. Irelan JT, Hagemann AT, Selker EU (1994) High frequency repeat-induced point mutation (RIP) is not associated with efficient recombination in Neurospora. Genetics, 138, 1093–1103.
35. Larkan NJ, Lydiate DJ, Yu F, Rimmer SR, Borhan MH (2014) Co-localisation of the blackleg resistance genes Rlm2 and LepR3 on Brassica napus chromosome A10. BMC Plant Biology, 14, 387.
36. Larkan NJ, Ma L, Borhan MH (2015) The Brassica napus receptor-like protein RLM2 is encoded by a second allele of the LepR3/Rlm2 blackleg resistance locus. Plant Biotechnology Journal, 13, 983–992.
37. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402–408.
38. Lo Presti L, Lanver D, Schweizer G et al. (2015) Fungal effectors and plant susceptibility. Annual Review of Plant Biology, 66, 513–545.
39. Manning VA, Ciuffetti LM (2015) Necrotrophic effector epistasis in the Pyrenophora tritici-repentis-wheat interaction. PLoS ONE, 10, e0123548.
40. Massingham T, Goldman N (2005) Detecting amino acid sites under positive selection and purifying selection. Genetics, 169, 1753–1762.
41. Mundt CC (2014) Durable resistance: a key to sustainable management of pathogens and pests. Infection, Genetics and Evolution, 27, 446–455.
42. Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics, 148, 929–936.
43. 2 accumulation in Brassica napus. Molecular Plant Pathology, 17, 818–831.
44. Parlange F, Daverdin G, Fudal I et al. (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. Molecular Microbiology, 71, 851–863.
45. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods, 8, 785–786.
46. Plissonneau C, Daverdin G, Ollivier B et al. (2016) A game of hide and seek between avirulence genes AvrLm4-7 and AvrLm3 in Leptosphaeria maculans. New Phytologist, 209, 1613–1624.
47. Pond SLK, Posada D, Gravenor MB, Woelk CH, Frost SDW (2006) GARD: a genetic algorithm for recombination detection. Bioinformatics, 22, 3096–3098.
48. Rep M, Meijer M, Houterman PM, van der Does HC, Cornelissen BJC (2005) Fusarium oxysporum evades I-3-mediated resistance without altering the matching avirulence gene. Molecular Plant-Microbe Interaction, 18, 15–23.
49. Rouxel T, Balesdent M-H (2016) Life, death and rebirth of avirulence effectors in a fungal pathogen of Brassica crops, Leptosphaeria maculans. New Phytologist. doi: 10.1111/nph.14411.
50. Rouxel T, Penaud A, Pinochet X et al. (2003) A 10-year survey of populations of Leptosphaeria maculans in France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape. European Journal of Plant Pathology, 109, 871–881.
51. Rouxel T, Grandaubert J, Hane JK et al. (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nature Communications, 2, 202.
52. Sievers F, Wilm A, Dineen D et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7, 539.
53. Sperschneider J, Ying H, Dodds PN et al. (2014) Diversifying selection in the wheat stem rust fungus acts predominantly on pathogen-associated gene families and reveals candidate effectors. Frontiers in Plant Sciences, 5, 372.
54. Sprague SJ, Balesdent M-H, Brun H et al. (2006) Major gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence of populations of Leptosphaeria maculans in France and Australia. European Journal of Plant Pathology, 114, 33–40.
55. Stachowiak A, Olechnowicz J, Jedryczka M et al. (2006) Frequency of avirulence alleles in field populations of Leptosphaeria maculans in Europe. European Journal of Plant Pathology, 114, 67–75.
56. Stergiopoulos I, Cordovez V, Ökmen B, Beenen HG, Kema GHJ, de Wit PJGM (2014) Positive selection and intragenic recombination contribute to high allelic diversity in effector genes of Mycosphaerella fijiensis, causal agent of the black leaf streak disease of banana. Molecular Plant Pathology, 15, 447–460.
57. Stukenbrock EH, McDonald BA (2009) Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Molecular Plant-Microbe Interaction, 22, 371–380.
58. Van de Wouw AP, Cozijnsen AJ, Hane JK et al. (2010) Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathogens, 6, e1001180.
59. Van de Wouw AP, Lowe RGT, Elliott CE, Dubois DJ, Howlett BJ (2014) An avirulence gene, AvrLmJ1, from the blackleg fungus, Leptosphaeria maculans, confers avirulence to Brassica juncea cultivars. Molecular Plant Pathology, 15, 523–530.
60. Van den Burg HA, Westerink N, Francoijs K-J et al. (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. Journal of Biological Chemistry, 278, 27340–27346.
61. West JS, Fitt BDL (2005) Population dynamics and dispersal of Leptosphaeria maculans (blackleg of canola). Australasian Plant Pathology, 34, 457–461.
62. Yang Z (2007) PAML 4: Phylogenetic Analysis by Maximum Likelihood. Molecular Biology and Evolution, 24, 1586–1591.
63. Zhang X, Peng P, Kutcher R, Balesdent MH, Delourme R, Fernando DWG (2015) Breakdown of Rlm3 resistance in the Brassica napus–Leptosphaeria maculans pathosystem in western Canada. European Journal of Plant Pathology, 14, 659–674.