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How genomic variation accelerates pathogen evolution in Zymoseptoria tritici
- 1. How variation in the genome speeds up the evolution of Zymoseptoria tritici Daniel Croll University of Neuchâtel Zymoseptoria community meeting 2017
- 2. What facilitates pathogen evolution at the population level?
- 3. Evolved pathogen population Ancestral pathogen population Gain of virulence mutation
- 4. Evolved pathogen population Ancestral pathogen population Map adaptive mutations Gain of virulence mutation
- 5. The complexity of the wheat-Z. tritici interaction Bulgaria Israel Kavkaz M3 Shaphir TE9111 1A5 1E4 3A1 3A4 3A5 3B2 3B4 3B8 3C 7 3D 1 3D 3 3D 7 3F1 3F3 3F4 3F5IPO 323 Fungal isolate Wheatcultivar 0 25 50 75 100 Sporulation % Apache Courtot Estanzuela M6 Solamouni Synthetic Tadinia Taichung Veranopolis (Plissonneau, Marcel, Croll)Single Swiss population
- 6. Investigating the genetic basis of pathogen evolution Availabledatasets Genotype only Genotype + Phenotype Genotype + Ecology QTL mapping Pathogen reproductive mode Selection scans SexualAsexual Genome-wide association mapping (GWAS) Environmental association studies Genome comparisons & selection analyses among lineages Plissonneau et al. 2017
- 7. Investigating the genetic basis of pathogen evolution Availabledatasets Genotype only Genotype + Phenotype Genotype + Ecology QTL mapping Pathogen reproductive mode Selection scans SexualAsexual Genome-wide association mapping (GWAS) Environmental association studies Genome comparisons & selection analyses among lineages Plissonneau et al. 2017
- 8. Oregon, USA Switzerland Israel Australia Mapping loci underlying adaptation to cultivar Toronit 0 20 40 Population Pathogenreproduction [%leafareacoveredbyspores] Australia Israel Sw itzerland O regon RO regon S
- 9. Complex genetic basis for adaptation to Toronit 1 2 3 4 5 6 7 8 9 10 11 12 13 0 1 2 3 4 5 6 7 8 9 10 Chromosome -log10(pvalue) * ThiopurineS- methyltransferase Reticulon AMPbinding PeptidaseC19 Zn-finger,MYNDtype * * * * unknownprotein unknown protein Phosphatidylserine decarboxylase Significance threshold (Hartmann et al. The ISME Journal 2017) Genome-wide association study (n = 106 strains)
- 10. Chromosomal rearrangements facilitated gene loss 0 1 2 3 4 5 6 7 8 9 10 -log10(p-value) Bonferroni (α = 0.05) Chromosomal position (in kb) 1740 1760 1780 1800 1820 1840 1860 1880 1900 1920 1940 Genes Reference genome Transposable elements Transposable elements Genes Genomeof Swissisolate candidate effector gene (Hartmann et al. The ISME Journal 2017) Effector gene
- 11. Chromosomal rearrangements facilitated gene loss 0 1 2 3 4 5 6 7 8 9 10 -log10(p-value) Bonferroni (α = 0.05) Chromosomal position (in kb) 1740 1760 1780 1800 1820 1840 1860 1880 1900 1920 1940 Genes Reference genome Transposable elements Transposable elements Genes Genomeof Swissisolate candidate effector gene (Hartmann et al. The ISME Journal 2017) Effector gene
- 12. The avirulence factor for Stb6 resistance
- 13. The avirulence factor for Stb6 resistance Phenotypic variation on Stb6 Chinese Spring Ziming Zhong Thierry Marcel Javier Palma Guerrero
- 14. The avirulence factor for Stb6 resistance 0 10 20 30 40 LOD score Mapposition(cM) Chromosome 5 Pycnidia density 80 60 40 20 0 80 60 40 20 0 1E4 allele 1A5 allele Numberofprogeny 61326 bp 0 25 50 75 100 0 50 100 150 200 250 QTL mapping on Stb6 Chinese Spring (Zhong et al. New Phyt 2017)
- 15. The avirulence factor for Stb6 resistance 0 10 20 30 40 LOD score Mapposition(cM) Chromosome 5 Pycnidia density 80 60 40 20 0 80 60 40 20 0 1E4 allele 1A5 allele Numberofprogeny 61326 bp 0 25 50 75 100 0 50 100 150 200 250 1 2 3 4 5 6 7 8 9 10 11 12 13 16 19 0 5 10 15 20 25 0 1 2 3 4 5 6 0 1 2 3 4 0 1 2 3 0 1 2 3 0 1 2 0 1 2 0 1 2 0 1 2 0 1 2 0 1 0 1 0 1 0 1 0 Chromosomes (position in Mb) −log10(p) GWAS on Stb6 Shafir QTL mapping on Stb6 Chinese Spring (Zhong et al. New Phyt 2017)
- 16. Telomeric Avr-Stb6 encodes a small secreted protein M R SILQG LLA FA LAVGVQAR V SCGG IGD LC KAGD SCCN YP GTDC FQDGQ Y PRCHTACGH F Q FG FCHDGKQ CNCQV ILGCG CV * M R SILQG LLA FA LAVGVQAR V SCGG IGD LC KAGD SCCN YP GTDC FQDGQ Y PRCHTACGH F Q FG FCHDGKQ CNCQV ILGCG CV * M R SILQG LLA FA LAVGVQAR VVCGG IGD LC KAG PSCCN YP ITNC FQDGQ Y PRCHTACGNW N FG FCHDGKQ CNCQT IPGCG CV * R R R Signal peptide 1A5 1E4 80706050403020100 0 10 20 30 40 50 60 70 80 90 100 Chromosome 5 Chromosome position (kb) Chromosome position (kb) IPO323 1E4 1A5 08060402 83 83 83 Transposable elements Genes (Zhong et al. New Phyt 2017)
- 17. Evolved pathogen population Ancestral pathogen population Source of evolutionary novelty Map adaptive mutations
- 18. Major variability in chromosomal structure (Plissonneau et al, under review) Complete PacBio genome assemblies of sympatric strains IPO323 1A5 1E4 3D1 3D7 0 Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb 2.4 Mb 0 Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb 0 Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb 0 Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb 0 Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb 2.4 Mb complete chromosome 8
- 19. Constructing a pan-genome for Z. tritici (Plissonneau et al, under review) 1006 464 483 411 859 93 5575 118 83 114 93 127 128 163 102 5848 85 48 92 122 76 197 105 509 111 147 94 534 9149 IPO323 1A5 1E4 3D1 3D7 5 complete genomes (PacBio & RNA-seq based annotation)
- 20. Z. tritici core genome? Orphan genes underlie massive genomic plasticity ●●● ● ● ●●● ● ●● ● ● ● ● ●● ●● ● ● ● ●●● ● ●●● ● ● ●●● ● ● ●●● ● ●● ● ● ● ● ●● ●● ● ● ● ● ●● ● ● ●● ● ● 10’000 12’000 14’000 16’000 1 2 3 4 5 Number of genomes sampled Numberofgenes ● ● Core genome Pangenome Numberofgenes Number of genomes sampled (Plissonneau et al, under review)
- 21. Conservation of core genome in species-level analysis 127 Illumina sequenced genomes (Plissonneau et al, under review)
- 22. Conservation of core genome in species-level analysis 0 25 50 75 100 Deletionspergene(%) Singleton Accessory Core Pangenome category 127 Illumina sequenced genomes (Plissonneau et al, under review)
- 23. Number of genes C onserved Incom plete loss Incom plete gain Z. tritici Z. pseudotritici Z. brevis C onserved Incom plete loss Incom plete gain Z. ardabiliae Z. passerinii n.d. n.d. n.d. Gene presence-absence Gene presentOrtholog found Ortholog missing 0 2’000 4’000 6’000 8’000 10’000 n=8’866 n=1’024 n=5 Origin of gene presence-absence polymorphism last split ~11’000 ybp Number of genes C onserved Incom plete loss Incom plete gain. tritici . pseudotritici . brevis C onserved Incom plete loss Incom plete gain . ardabiliae . passerinii n.d. n.d. n.d. Gene presentOrtholog found 0 2’000 4’000 6’000 8’000 10’000 n=8’866 n=1’024 n=599 Species- specific genes Shared among species (Grandaubert et al. G3 2015) (Hartmann & Croll, MBE 2017)
- 24. Number of genes C onserved Incom plete loss Incom plete gain Z. tritici Z. pseudotritici Z. brevis C onserved Incom plete loss Incom plete gain Z. ardabiliae Z. passerinii n.d. n.d. n.d. Gene presence-absence Gene presentOrtholog found Ortholog missing 0 2’000 4’000 6’000 8’000 10’000 n=8’866 n=1’024 n=5 Origin of gene presence-absence polymorphism last split ~11’000 ybp Number of genes C onserved Incom plete loss Incom plete gain. tritici . pseudotritici . brevis C onserved Incom plete loss Incom plete gain . ardabiliae . passerinii n.d. n.d. n.d. Gene presentOrtholog found 0 2’000 4’000 6’000 8’000 10’000 n=8’866 n=1’024 n=599 Species- specific genes Shared among species (Grandaubert et al. G3 2015) (Hartmann & Croll, MBE 2017)
- 25. Conserved protein domain Secreted 0 10 20 30 40 50 60 All genes Yes No Cell wall degrading enzymes Secondary metabolite backbone Small secreted proteins Yes Protein functions Coregenesaffectedbyrecentlosses(%) Incomplete losses Recently lost core Zymoseptoria genes Z. tritici Z. pseudotritici Z. brevis Z. ardabiliae Z. passerinii n.d. n.d. n.d. (Hartmann & Croll, MBE 2017)
- 26. Conserved protein domain Secreted 0 10 20 30 40 50 60 All genes Yes No Cell wall degrading enzymes Secondary metabolite backbone Small secreted proteins Yes Protein functions Coregenesaffectedbyrecentlosses(%) Incomplete losses Recently lost core Zymoseptoria genes Z. tritici Z. pseudotritici Z. brevis Z. ardabiliae Z. passerinii n.d. n.d. n.d. (Hartmann & Croll, MBE 2017)
- 27. Z. tritici-specific genes not having reached fixation Conserved protein domain Secreted 0 10 20 30 40 50 60 All genes Yes No Cell wall degrading enzymes Secondary metabolite backbone Small secreted proteins Yes Protein functions Coregenesaffectedbyrecentlosses(%) Orphangenesnotfixedinspecies(%) Incomplete losses Incomplete gains (Hartmann & Croll, MBE 2017)
- 28. Evolved pathogen population Ancestral pathogen population Source of evolutionary novelty Signatures of recent selection Map adaptive mutations
- 29. Evidence for recent selection in populations Composite likelihood ratio (CLR) and integrated haplotype score (iHS) 0 1 2 3 4 5 6 0 1 2 3 0 1 2 3 0 1 2 0 1 2 0 1 2 0 1 2 0 1 2 0 1 2 0 1 0 1 0 1 1 0 100 200 300 400 500 −4 −2 0 0 50 100 150 200 250 −8 −6 −4 −2 0 0 50 100 150 200 −6 −4 −2 0 0 100 200 300 −4 −2 0 CLR - |iHS| Chromosome (position in Mb) 1 2 3 4 5 6 7 8 9 10 11 12 13 CLR CLR - |iHS| CLR - |iHS| Australia Switzerland Israel Oregon - |iHS| 0 9 9 Pe (Hartmann et al, under review) 99.9% outliers
- 30. 0 1 2 3 4 5 6 0 1 2 3 0 1 2 3 0 1 2 0 1 2 0 1 2 0 1 2 0 1 2 0 1 2 0 1 0 1 0 1 1 0 100 200 300 400 500 −4 −2 0 0 50 100 150 200 250 −8 −6 −4 −2 0 0 50 100 150 200 −6 −4 −2 0 0 100 200 300 −4 −2 0 CLR - |iHS| Chromosome (position in Mb) 1 2 3 4 5 6 7 8 9 10 11 12 13 CLR CLR - |iHS| CLR - |iHS| Australia Switzerland Israel Oregon - |iHS| 0 9 9 Pe (Hartmann et al, under review) Evidence for recent selection in populations Composite likelihood ratio (CLR) and integrated haplotype score (iHS) 36.4% of loci under selection were shared among populations Selection on host infection arsenal: effector proteins, peroxide tolerance, degradation of host tissues Enrichment in membrane transporters (abiotic / biotic stress tolerance?) 99.9% outliers
- 31. Rapid evolution of effector loci Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb 2.4 Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb Mb 0.2 Mb 0.4 Mb 0.6 Mb 0.8 Mb 1 Mb 1.2 Mb 1.4 Mb 1.6 Mb 1.8 Mb 2 Mb 2.2 Mb 2.4 Mb Massive standing variation Selection on complex traits
- 32. Acknowledgements @danielcroll web: www.pathogen-genomics.org Funding agencies Marcello Zala Gerrit Kuhn, Philip Lobb Andrea Patrignani Grant 12-03 Bruce McDonald Pathogen genomics group Fanny Hartmann Norfarhan Mohd Assa’ad Simone Fouché Clémence Plissonneau Andrea Sánchez-Vallet Alessandra Stürchler Juliana Benevenuto Javier Palma Guerrero Nikhil Kumar Singh, Leen Abraham, Ursula Oggenfuss
- 33. Are there genetic factors that constrain pathogen adaptation from cultivar to cultivar? What environmental factors constrain pathogen adaptation? (Host mixtures, fungicides, agricultural practices, etc.)