A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene

New Phytologist

Volumn 214, Issue 2, 2017, Pages 619-631

  Zhong, Ziming ^a   Marcel, Thierry C ^b   Hartmann, Fanny E ^a   Ma, Xin ^a   Plissonneau, Clémence ^a,b   Zala, Marcello ^a   Ducasse, Aurélie ^b   Confais, Johann ^b   Compain, Jérôme ^b   Lapalu, Nicolas ^b   Amselem, Joëlle ^b   McDonald, Bruce A ^a   Croll, Daniel ^a,c   Palma Guerrero, Javier ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

avirulence; AvrStb6; gene for gene interaction; genome wide association study (GWAS); quantitative trait locus (QTL) mapping; Stb6; Zymoseptoria tritici

Indexed keywords

CULTIVAR; FUNGUS; GENE; GENETIC ANALYSIS; PATHOGEN; PHENOTYPE; PROTEIN; VIRULENCE; WHEAT;

FRANCE; SWITZERLAND;

MYCOSPHAERELLA GRAMINICOLA; TRITICUM AESTIVUM;

FUNGAL PROTEIN; PLANT PROTEIN;

AMINO ACID SEQUENCE; ASCOMYCETES; CHEMISTRY; CHROMOSOMAL MAPPING; DISEASE RESISTANCE; GENE LINKAGE DISEQUILIBRIUM; GENETIC POLYMORPHISM; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHENOTYPE; PLANT DISEASE; PLANT GENE; QUANTITATIVE TRAIT LOCUS; SECRETION (PROCESS); VIRULENCE; WHEAT;

AMINO ACID SEQUENCE; ASCOMYCOTA; BASE SEQUENCE; CHROMOSOME MAPPING; DISEASE RESISTANCE; FUNGAL PROTEINS; GENES, PLANT; GENOME-WIDE ASSOCIATION STUDY; LINKAGE DISEQUILIBRIUM; PHENOTYPE; PLANT DISEASES; PLANT PROTEINS; POLYMORPHISM, GENETIC; QUANTITATIVE TRAIT LOCI; TRITICUM; VIRULENCE;

EID: 85013059427     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14434     Document Type: Article

References (89)

1. Anders S, Pyl PT, Huber W. 2015. HTSeq – a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166–169.
2. Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT et al. 2010. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627–631.
3. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120.
4. Bourras S, McNally KE, Muller MC, Wicker T, Keller B. 2016. Avirulence genes in cereal powdery mildews: the Gene-for-Gene Hypothesis 2.0. Frontiers in Plant Science 7: 241.
5. Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F. 2010. Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genetics 6: e1000940.
6. Brading PA, Verstappen ECP, Kema GHJ, Brown JKM. 2002. A gene-for-gene relationship between wheat and Mycosphaerella graminicola, the Septoria tritici blotch pathogen. Phytopathology 92: 439–445.
7. Broman KW, Wu H, Sen S, Churchill GA. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889–890.
8. Brown JK, Chartrain L, Lasserre-Zuber P, Saintenac C. 2015. Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genetics and Biology 79: 33–41.
9. Chartrain L, Brading PA, Brown JKM. 2005. Presence of the Stb6 gene for resistance to Septoria tritici blotch (Mycosphaerella graminicola) in cultivars used in wheat-breeding programmes worldwide. Plant Pathology 54: 134–143.
10. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE et al. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nature Methods 10: 563–569.
11. Croll D, Lendenmann MH, Stewart E, McDonald BA. 2015. The impact of recombination hotspots on genome evolution of a fungal plant pathogen. Genetics 201: 1213–1228.
12. Dalman K, Himmelstrand K, Olson A, Lind M, Brandstrom-Durling M, Stenlid J. 2013. A genome-wide association study identifies genomic regions for virulence in the non-model organism Heterobasidion annosum s.s. PLoS ONE 8: e53525.
13. Dodds P, Thrall P. 2009. Recognition events and host-pathogen co-evolution in gene-for-gene resistance to flax rust. Functional Plant Biology 36: 395–408.
14. Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL et al. 2011. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proceedings of the National Academy of Sciences, USA 108: 9166–9171.
15. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2: 953–971.
16. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A et al. 2016. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research 44: D279–D285.
17. Flor HH. 1956. The complementary genic systems in flax and flax rust. Advances in Genetics Incorporating Molecular Genetic Medicine 8: 29–54.
18. Flutre T, Duprat E, Feuillet C, Quesneville H. 2011. Considering transposable element diversification in de novo annotation approaches. PLoS ONE 6: e16526.
19. Friesen TL, Faris JD, Solomon PS, Oliver RP. 2008. Host-specific toxins: effectors of necrotrophic pathogenicity. Cellular Microbiology 10: 1421–1428.
20. Garrison E, Marth G. 2012. Haplotype-based variant detection from short-read sequencing. arXiv preprint arxive:1207.3907 [q-bio.GN].
21. Ghaffary SMT, Robert O, Laurent V, Lonnet P, Margale E, van der Lee TAJ, Visser RGF, Kema GHJ. 2011. Genetic analysis of resistance to septoria tritici blotch in the French winter wheat cultivars Balance and Apache. Theoretical and Applied Genetics 123: 741–754.
22. Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES. 2014. TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE 9: e90346.
23. Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205–227.
24. Goodwin SB, Ben M'Barek S, Dhillon B, Wittenberg AHJ, Crane CF, Hane JK, Foster AJ, Van der Lee TAJ, Grimwood J, Aerts A et al. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genetics 7: e1002070.
25. Govrin EM, Levine A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology 10: 751–757.
26. Grandaubert J, Bhattacharyya A, Stukenbrock EH. 2015. RNA-seq-based gene annotation and comparative genomics of four fungal grass pathogens in the genus Zymoseptoria identify novel orphan genes and species-specific invasions of transposable elements. G3 – Genes Genomes Genetics 5: 1323–1333.
27. Guy L, Kultima JR, Andersson SG. 2010. genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26: 2334–2335.
28. Hammond-Kosack KE, Rudd JJ. 2008. Plant resistance signalling hijacked by a necrotrophic fungal pathogen. Plant Signaling & Behavior 3: 993–995.
29. Hartmann FE, Sanchez-Vallet A, McDonald BA, Croll D. 2016. A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements. ISME Journal 54: 323–346.
30. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, Manolio TA. 2009. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proceedings of the National Academy of Sciences, USA 106: 9362–9367.
31. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444: 323–329.
32. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JD. 1994. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266: 789–793.
33. Kellner R, Bhattacharyya A, Poppe S, Hsu TY, Brem RB, Stukenbrock EH. 2014. Expression profiling of the wheat pathogen Zymoseptoria tritici reveals genomic patterns of transcription and host-specific regulatory programs. Genome Biology and Evolution 6: 1353–1365.
34. Kema GH, Verstappen EC, Waalwijk C. 2000. Avirulence in the wheat septoria tritici leaf blotch fungus Mycosphaerella graminicola is controlled by a single locus. Molecular Plant-Microbe Interactions 13: 1375–1379.
35. Kema GHJ, Yu DZ, Rijkenberg FHJ, Shaw MW, Baayen RP. 1996. Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86: 777–786.
36. Keon J, Antoniw J, Carzaniga R, Deller S, Ward JL, Baker JM, Beale MH, Hammond-Kosack K, Rudd JJ. 2007. Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Molecular Plant-Microbe Interactions 20: 178–193.
37. Koeck M, Hardham AR, Dodds PN. 2011. The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cellular Microbiology 13: 1849–1857.
38. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 305: 567–580.
39. Laluk K, Mengiste T. 2010. Necrotroph attacks on plants: wanton destruction or covert extortion? Arabidopsis Book 8: e0136.
40. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9: 357–359.
41. Lee WS, Rudd JJ, Hammond-Kosack KE, Kanyuka K. 2014. Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Molecular Plant-Microbe Interactions 27: 236–243.
42. Lendenmann MH, Croll D, Stewart EL, McDonald BA. 2014. Quantitative trait locus mapping of melanization in the plant pathogenic fungus Zymoseptoria tritici. G3 – Genes Genomes Genetics 4: 2519–2533.
43. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.
44. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Proc GPD. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.
45. Liu ZH, Zhang ZC, Faris JD, Oliver RP, Syme R, McDonald MC, McDonald BA, Solomon PS, Lu SW, Shelver WL et al. 2012. The cysteine rich necrotrophic effector Sntox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS Pathogens 8: e1002467.
46. Mammadov J, Sun X, Gao Y, Ochsenfeld C, Bakker E, Ren R, Flora J, Wang X, Kumpatla S, Meyer D et al. 2015. Combining powers of linkage and association mapping for precise dissection of QTL controlling resistance to gray leaf spot disease in maize (Zea mays L.). BMC Genomics 16: 916.
47. Manenti G, Galvan A, Pettinicchio A, Trincucci G, Spada E, Zolin A, Milani S, Gonzalez-Neira A, Dragani TA. 2009. Mouse genome-wide association mapping needs linkage analysis to avoid false-positive loci. PLoS Genetics 5: e1000331.
48. Marone D, Russo MA, Laido G, De Leonardis AM, Mastrangelo AM. 2013. Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: active guardians in host defense responses. International Journal of Molecular Sciences 14: 7302–7326.
49. Marshall R, Kombrink A, Motteram J, Loza-Reyes E, Lucas J, Hammond-Kosack KE, Thomma BPHJ, Rudd JJ. 2011. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiology 156: 756–769.
50. McWilliam H, Li WZ, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R. 2013. Analysis tool web services from the EMBL-EBI. Nucleic Acids Research 41: W597–W600.
51. Mirzadi Gohari A. 2015. Identification and functional characterization of putative (a)virulence factors in the fungal wheat pathogen Zymoseptoria tritici. PhD thesis, Wageningen University, Wageningen, the Netherlands.
52. Muller LA, Lucas JE, Georgianna DR, McCusker JH. 2011. Genome-wide association analysis of clinical vs. nonclinical origin provides insights into Saccharomyces cerevisiae pathogenesis. Molecular Ecology 20: 4085–4097.
53. O'Driscoll A, Kildea S, Doohan F, Spink J, Mullins E. 2014. The wheat–Septoria conflict: a new front opening up? Trends in Plant Science 19: 602–610.
54. Oliver RP, Friesen TL, Faris JD, Solomon PS. 2012. Stagonospora nodorum: from pathology to genomics and host resistance. Annual Review of Phytopathology 50: 23–43.
55. Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B. 2000. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12: 2019–2032.
56. Palma-Guerrero J, Hall CR, Kowbel D, Welch J, Taylor JW, Brem RB, Glass NL. 2013. Genome wide association identifies novel loci involved in fungal communication. PLoS Genetics 9: e1003669.
57. Palma-Guerrero J, Ma X, Torriani SF, Zala M, Francisco CS, Hartmann FE, Croll D, McDonald BA. 2016a. Comparative transcriptome analyses in Zymoseptoria tritici reveal significant differences in gene expression among strains during plant infection. Molecular Plant Microbe Interactions. (in press).
58. Palma-Guerrero J, Torriani SFF, Zala M, Carter D, Courbot M, Rudd JJ, McDonald BA, Croll D. 2016b. Comparative transcriptomic analyses of Zymoseptoria tritici strains show complex lifestyle transitions and intraspecific variability in transcription profiles. Molecular Plant Pathology 17: 845–859.
59. Plissonneau C, Stürchler A, Croll D. 2016. The evolution of orphan regions in genemes of a fungal pathogen of wheat. mBio. doi: 10.1128/mBio.01231-16.
60. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ et al. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics 81: 559–575.
61. Raffaele S, Kamoun S. 2012. Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Reviews Microbiology 10: 417–430.
62. R-Core-Team. 2013. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
63. Rep M. 2005. Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiology Letters 253: 19–27.
64. Rietveld CA, Medland SE, Derringer J, Yang J, Esko T, Martin NW, Westra HJ, Shakhbazov K, Abdellaoui A, Agrawal A et al. 2013. GWAS of 126,559 individuals identifies genetic variants associated with educational attainment. Science 340: 1467–1471.
65. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.
66. Robinson MD, Oshlack A. 2010. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology 11: R25.
67. Robinson MD, Smyth GK. 2008. Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics 9: 321–332.
68. Rouxel T, Balesdent M-H 2010. Avirulence genes. Encyclopedia of life sciences (ELS). Chichester, UK: John Wiley & Sons.
69. Rudd JJ, Kanyuka K, Hassani-Pak K, Derbyshire M, Andongabo A, Devonshire J, Lysenko A, Saqi M, Desai NM, Powers SJ et al. 2015. Transcriptome and metabolite profiling of the Infection cycle of Zymoseptoria tritici on wheat reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions and a variation on the hemibiotrophic lifestyle definition. Plant Physiology 167: 1158–1185.
70. Rudd JJ, Keon J, Hammond-Kosack KE. 2008. The wheat mitogen-activated protein kinases TaMPK3 and TaMPK6 are differentially regulated at multiple levels during compatible disease interactions with Mycosphaerella graminicola. Plant Physiology 147: 802–815.
71. Sanchez-Vallet A, McDonald MC, Solomon PS, McDonald BA. 2015. Is Zymoseptoria tritici a hemibiotroph? Fungal Genetics and Biology 79: 29–32.
72. Shetty NP, Kristensen BK, Newman MA, Moller K, Gregersen PL, Jorgensen HJL. 2003. Association of hydrogen peroxide with restriction of Septoria tritici in resistant wheat. Physiological and Molecular Plant Pathology 62: 333–346.
73. Sonah H, O'Donoughue L, Cober E, Rajcan I, Belzile F. 2015. Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean. Plant Biotechnology Journal 13: 211–221.
74. Sperschneider J, Gardiner DM, Dodds PN, Tini F, Covarelli L, Singh KB, Manners JM, Taylor JM. 2016. EffectorP: predicting fungal effector proteins from secretomes using machine learning. New Phytologist 210: 743–761.
75. Stergiopoulos I, de Wit PJGM. 2009. Fungal effector proteins. Annual Review of Phytopathology 47: 233–263.
76. Stewart EL, Croll D, Lendenmann MH, Sanchez-Vallet A, Hartmann FE, Palma-Guerrero J, Ma X, McDonald BA. 2016. QTL mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici. Molecular Plant Pathology. doi: 10.1111/mpp.12515.
77. Stewart EL, McDonald BA. 2014. Measuring quantitative virulence in the wheat pathogen Zymoseptoria tritici using high-throughput automated image analysis. Phytopathology 104: 985–992.
78. Stotz HU, Mitrousia GK, de Wit PJGM, Fitt BDL. 2014. Effector-triggered defence against apoplastic fungal pathogens. Trends in Plant Science 19: 491–500.
79. Tabib Ghaffary SM, Faris JD, Friesen TL, Visser RG, van der Lee TA, Robert O, Kema GH. 2012. New broad-spectrum resistance to Septoria tritici blotch derived from synthetic hexaploid wheat. Theoretical and Applied Genetics 124: 125–142.
80. Talas F, Kalih R, Miedaner T, McDonald BA. 2016. Genome-wide association study identifies novel candidate genes for aggressiveness, deoxynivalenol production, and azole sensitivity in natural field populations of Fusarium graminearum. Molecular Plant-Microbe Interactions 29: 417–430.
81. Tarailo-Graovac M, Chen N. 2009. Using RepeatMasker to identify repetitive elements in genomic sequences. Current Protocols in Bioinformatics 25: 4.10.1–4.10.14.
82. Thomma BPHJ, Nurnberger T, Joosten MHAJ. 2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23: 4–15.
83. Utermark J, Karlovsky P. 2008. Genetic transformation of filamentous fungi by Agrobacterium tumefaciens. Protocol Exchange. doi:10.1038/nprot.2008.83.
84. de Wit PJ. 2007. How plants recognize pathogens and defend themselves. Cellular and Molecular Life Sciences 64: 2726–2732.
85. de Wit PJGM, Mehrabi R, van den Burg HA, Stergiopoulos I. 2009. Fungal effector proteins: past, present and future. Molecular Plant Pathology 10: 735–747.
86. Zhan J, Linde CC, Jurgens T, Merz U, Steinebrunner F, McDonald BA. 2005. Variation for neutral markers is correlated with variation for quantitative traits in the plant pathogenic fungus Mycosphaerella graminicola. Molecular Ecology 14: 2683–2693.
87. Zhan J, Mundt CC, Hoffer ME, McDonald BA. 2002. Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem. Journal of Evolutionary Biology 15: 634–647.
88. Zhan J, Torriani SF, McDonald BA. 2007. Significant difference in pathogenicity between MAT1-1 and MAT1-2 isolates in the wheat pathogen Mycosphaerella graminicola. Fungal Genetics and Biology 44: 339–346.
89. Zheng X, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS. 2012. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28: 3326–3328.