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Réarrangements chromosomiques Evolution des génomes de levures

Réarrangements chromosomiques Evolution des génomes de levures. 2ème réunion GTGC Nantes 12 et 13 octobre 2006 Gilles Fischer. Comparative genomics in yeasts:. significant results: - Gene identification and annotation - Sequence comparison and protein evolution. 100 85 65 61 51 48.

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Réarrangements chromosomiques Evolution des génomes de levures

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  1. Réarrangements chromosomiques Evolution des génomes de levures 2ème réunion GTGC Nantes 12 et 13 octobre 2006 Gilles Fischer

  2. Comparative genomics in yeasts: significant results: - Gene identification and annotation - Sequence comparison and protein evolution

  3. 100 85 65 61 51 48 100 * 90 70 50 Homo sapiens Mus musculus Takifugu rubripes Tetraodon negroviridis * Data from O. Jaillon et al., Nature, 2004 Ciona intestinalis Saccharomyces cerevisiae Saccharomyces paradoxus Saccharomyces mikatae Saccharomyces kudriavzevii Saccharomyces bayanus Saccharomyces exiguus Saccharomyces servazzii Saccharomyces castellii Candida glabrata Zygosaccharomyces rouxii Kluyveromyces thermotolerans Kluyveromyces waltii Saccharomyces kluyveri Kluyveromyces lactis Kluyveromyces marxianus Ashbya gossypii Pichia angusta Debaryomyces hansenii Pichia sorbitophila Candida guilliermondii Candida lusitaniae Candida tropicalis Candida parapsilosis Candida albicans Candida dubliniensis Yarrowia lipolytica Schizosaccharomyces pombe Cryptococcus neoformans 7 6 Hemiascomycetes 5 4 2 3 1 Neurospora, Magnaporthe, Aspergillus, etc… Euascomycetes Archiascomycetes Basidiomycetes

  4. Comparative genomics in yeasts: significant results: - Gene identification and annotation - Sequence comparison and protein evolution - Chromosome rearrangements 1> speciation process 2> level of chromosome reorganisation 3> rates of chromosomal rearrangements

  5. 1> speciation process: mechanisms for hybrid sterility - Chromosomal rearrangements chromosome imbalance at meiosis -Genetic incompatibilities Dominant and/or recessive incompatibilities Chambers et al., 1996 ; Greig et al., 2002 - DNA sequence divergence and Mismatch repair prevention of recombination between homologs Chambers et al., 1996 ; Hunter et al, 1996 ; Greig et al., 2003

  6. Chromosomal evolution in the Saccharomyces sensu stricto complex: Saccharomyces cerevisiae Saccharomyces paradoxus Saccharomyces mikatae Saccharomyces kudriavzevii Saccharomyces bayanus Saccharomyces exiguus Saccharomyces servazzii Saccharomyces castellii Candida glabrata Zygosaccharomyces rouxii Kluyveromyces thermotolerans Kluyveromyces waltii Saccharomyces kluyveri Kluyveromyces lactis Kluyveromyces marxianus Ashbya gossypii Pichia angusta Debaryomyces hansenii Pichia sorbitophila Candida guilliermondii Candida lusitaniae Candida tropicalis Candida parapsilosis Candida albicans Candida dubliniensis Yarrowia lipolytica Schizosaccharomyces pombe Cryptococcus neoformans 7 S. cerevisiae S. cariocanus 6 S. paradoxus S. mikatae S. kudriavzevii 5 4 S. bayanus var. uvarum 2 • monophyletic group of species • closely related to S. cerevisiae • viable hybrids 3 1 Neurospora, Magnaporthe, Aspergillus, etc… Euascomycetes Archiascomycetes Basidiomycetes

  7. Electrophoretic Karyotypes: Chromosomal Translocations: mechanism of post-zygotic isolation? S1 S2 S3 S1 S2 S6 S4 S6 S4 S3 S5 S5 sensu stricto species S. cerevisiae

  8. 4 translocations 2 translocations 4 translocations Chromosomal evolution in Saccharomyces sensu stricto: S. cariocanus 94 (0 translocation) S. paradoxus 81 S. cerevisiae (as reference) 94 99 S. mikatae S. kudriavzevii (0 translocation) S. bayanus ITS1 Fischer et al., Nature 2000

  9. Left sequence tag Right sequence tag 3 - 5 kb random genomic fragments cloned in sequencing plasmid Gene 1 Gene 2 In 2000: Genolevures I, Genomic exploration of 13 yeast species 0.2 to 0.5 X of genome coverage Souciet et al., FEBS Letters (special issue), 2000

  10. 0.4X about 2000 neighboring gene couples : gene 2 gene 1 S.bayanus gene 2’ gene 1’ S.cerevisiae Synteny conservation gene 1’ S.cerevisiae gene 2’ Synteny breakpoint Saccharomyces cerevisiae Saccharomyces paradoxus Saccharomyces mikatae Saccharomyces kudriavzevii Saccharomyces bayanus Saccharomyces exiguus Saccharomyces servazzii Saccharomyces castellii Candida glabrata Zygosaccharomyces rouxii Kluyveromyces thermotolerans Kluyveromyces waltii Saccharomyces kluyveri Kluyveromyces lactis Kluyveromyces marxianus Ashbya gossypii Pichia angusta Debaryomyces hansenii Pichia sorbitophila Candida guilliermondii Candida lusitaniae Candida tropicalis Candida parapsilosis Candida albicans Candida dubliniensis Yarrowia lipolytica Schizosaccharomyces pombe Cryptococcus neoformans 7 6 Hemiascomycetes 5 4 2 => 35 synteny breakpoints (80 predicted in total) 3 corresponded to translocations = > 32 breakpoints left ??? 3 1 Neurospora, Magnaporthe, Aspergillus, etc… Euascomycetes Archiascomycetes Basidiomycetes

  11. YML051w YML051w YML049w YML051w YJR055w YML046w YJR052w K. thermotolerans : YML046w YJR052w YJR053w YML048w K. lactis : YJR053w YJR052w YJR054w YJR055w YJR057w YML049w YJR056c YJR058c YML046w YML048w (i) Gene transposition: YJR052w YJR053w YJR054w YJR055w YJR057w X YJR056c YJR058c

  12. YML051w YML051w DUPLICATION YJR053w YJR053w YJR052w YJR052w YJR054w YJR054w YJR055w YJR055w YJR057w YJR057w YML049w YML049w YJR056c YJR056c YJR058c YJR058c YML046w YML046w YML048w YML048w (i) Gene transposition:

  13. YML051w YML051w YJR053w YJR053w YJR052w YJR052w YJR054w YJR054w YJR055w YJR055w YJR057w YJR057w YML049w YML049w YJR056c YJR056c YJR058c YJR058c YML046w YML046w YML048w YML048w (i) Gene transposition: RECIPROCAL GENE LOSS

  14. YML051w (i) Gene transposition: S. cerevisiae YJR053w YJR052w YJR054w YJR055w YJR057w X YJR056c YJR058c YML047c XIII YML049w YML046w YML048w

  15. YML051w (i) Gene transposition: S. bayanus YJR053w YJR052w YJR054w YJR055w YJR057w X YJR056c YJR058c YML047c XIII YML049w YML046w YML048w Fischer et al., Genome Research 2001

  16. (ii) Species specific gene duplication: YDR037w SuYDR037w (KRS1) IV IItIV SuYDR038c YDR036c YDR038c Relic of YDR037w paralog S. uvarum S. cerevisiae SuYDR037w II IVtII SuYBR60c SuYBR061c YBR60c YBR061c YBR060c YBR061c YDR037w (KRS1) 1000 2000 3000 4000 5000 Stringency 15/23 Fischer et al., Genome Research 2001

  17. Reciprocal gene loss => SPECIATION by a version of the Bateson-Dobzhansky-Muller mechanism: duplication Duplicate gene loss Reciprocal gene loss meiosis Hybrid 2n 1/4 of dead spores

  18. Reciprocal gene loss => SPECIATION by a version of the Bateson-Dobzhansky-Muller mechanism: Scannell et al., Nature 2006

  19. Sequence divergence and meiotic sterility: sequencing of 6 genes in 41 strains 0,3% S. cariocanus 5% 0,15% 1% 0,1% 15% 0,6% Liti et al., Genetics in press

  20. Sequence divergence and meiotic sterility: sequencing of 6 genes in 41 strains spore viability: - 1 reciprocal translocation=> 50% - 1 non reciprocal translocation => 75% - 4 reciprocal translocations => 6% Liti et al., Genetics in press

  21. Sequence divergence and meiotic sterility: sequencing of 6 genes in 41 strains Liti et al., Genetics in press

  22. Increasing DNA divergence Chromosomal translocations Reciprocal gene loss Whole Genome Duplication Conclusions:speciation results from several mechanisms superimposed? S. cerevisiae S. paradoxus S. cariocanus S. bayanus C. glabrata S. castellii K. waltii K. lactis A. gossypii

  23. Genome 1 Genome 2 gap r2 2> Level of chromosome reorganisation: Genolevures 2 Dujon et al., Nature, 2004 S. cerevisiae C. glabrata Human pathogen K. lactis Model organism D. hansenii Cryotolerant, halotolerant marine yeast Y. lipolytica Alkane-using yeast Duplication blocks 5 intra comparisons Synteny blocks 10 pairwise comparisons ADHoRe sofware ( Vandepoele et al., Genome Res, 2002)

  24. C. glabrata S. cerevisiae C. glabrata Total nb of duplicated blocks internal to chromosomes 56 20 sutelomeric 21 0 Block size (kb) mean 42 27 max. 243 89 Nb of gene pairs /block mean 5.8 3.8 max. 15 6 Dujon et al., Nature 2004 Blocks of ancestral duplications S. cerevisiae

  25. Extensive loss of duplicated genes More extensive loss of duplicated genes and reductive evolution Other mechanisms of duplication GENOME DUPLICATION AND GENOME REDUNDANCY Overall genome redundancy (nb of genes in families over total nb of genes) 44.2 % 35.1 % 31.8 % 51.5 % 41.8 % S. cerevisiae Whole Genome Duplication 4 C. glabrata 3 2 K. lactis 1 D. hansenii Y. lipolytica

  26. Blocks of ancestral duplications K. lactis D. hansenii Y. lipolytica K. lactis D. hansenii Y. lipolytica Total nb of duplicated blocks internal to chromosomes 8 5 2 sutelomeric 1 10 0 Block size (kb) mean 9 19 90 max. 25 59 148 Nb of gene pairs /block mean 4.3 3.7 4.0 max. 11 6 4 ? Sporadic segmental duplications

  27. pseudogenes pseudogenes total nb of direct total nb of tandem pairs orientation arrays S. cerevisiae 61 79% 50 C. glabrata 47 83% 32 K. lactis 36 72 % 33 D. hansenii329 92 % 247 Y. lipolytica 54 72 % 48 Similar to S. cerevisiae YHR179w OYE2 NADPH dehydrogenase (old yellow enzyme), isoform 1 Example of a tandem repeat array in D. hansenii D. hansenii_ CONTIG=DEHAOK Amino-acid sequence identity between copies: from 82 % to 95 %

  28. Extensive loss of duplicated genes More extensive loss of duplicated genes and reductive evolution Segmental duplication Segmental duplication Tandem repeat formation Segmental duplication GENOME DUPLICATION AND GENOME REDUNDANCY S. cerevisiae Whole Genome Duplication 4 C. glabrata 3 2 K. lactis 1 D. hansenii Y. lipolytica

  29. WGD segmental duplications gene tandem duplications <-DUPLICATION LOSS -> sequence degeneration deletion New functions Gene dosage Gene order changes and translocations Pseudogenes and gene relics Speciation

  30. Low genome reorganization: • 10 translocations in total => High synteny conservation Synteny conservation among Hemiascomycetes: S. cerevisiae S. paradoxus S. cariocanus S. bayanus C. glabrata K. lactis D. hansenii Y. lipolytica

  31. S.cerevisiae C. glabrata K. lactis D. hansenii C. glabrata K. lactis D. hansenii Y. lipolytica

  32. S.cerevisiae C. glabrata 88% of the genomes are conserved within synteny blocks

  33. S. cerevisiae S. paradoxus 0 reference S. cerevisiae S. mikatae 4 translocations S. cariocanus S. bayanus C . g l a b r a t a Variable rates of rearrangements? 0 S. paradoxus 2 translocations S. mikatae K . l a c t i s 0 S. kudriavzevii 4 translocations S. bayanus Y . l i p o l y t i c a D . h a n s e n i i massive reorganization Low genome reorganization 1000 1000 1000 1000 1000 1000 0.1

  34. =5 S. cerevisiae 1000 S. paradoxus 1000 S. mikatae S. bayanus 1000 C . g l a b r a t a =5 1000 K . l a c t i s 1000 ? Y . l i p o l y t i c a 923 1000 987 A . g o s s y p i i 1000 K . w a l t i i C . a l b i c a n s D . h a n s e n i i 0.1 Rates of genome rearrangements among Hemiascomycetes: • Gene order conservation: GOC gene 2 gene 1 Species 1 gene X gene 1’ Species 2

  35. GOL GOLest X19 X17 X18 X12+X13 +X15+X17 +X19 X15 0.12 X16 X13 X11 X14 X12 X5 X10 X8 X9 X6 X7 X4 X2 X3 X1 Rates of genome rearrangements among Hemiascomycetes: GOC S. cerevisiae 9 S. paradoxus 8 0.88 S. mikatae 7 S. bayanus 6 C . g l a b r a t a 3 A . g o s s y p i i 5 K . l a c t i s 4 1 K . w a l t i i C . a l b i c a n s 2 D . h a n s e n i i Y . l i p o l y t i c a

  36. GOC GOL GOLest 0.51 0.08 X12+X13 +X15+X17 +X19 9 0.54 WGD 0.88 0.12 1.00 8 0.29 0.81 7 2.18 -2 < 10 6 1.13 1.63 0.43 3 4.09 5 0.75 -2 < 10 4 1 0.23 1.43 1.89 2 0.98 1.20 Rates of genome rearrangements among Hemiascomycetes: S. cerevisiae S. paradoxus S. mikatae S. bayanus C . g l a b r a t A . g o s s y p K . l a c t i s K . w a l t i i C . a l b i c a n s D . h a n s e n i i Y . l i p o l y t i c a Fischer et al., PLoS Genetics, 2006

  37. Genome instability scale: 0.51 1 0.08 9 0.54 WGD 1.00 C . a l b i c a n s 8 0.29 0.81 0.9 7 2.18 -2 < 10 6 C . g l a b r a t a 1.13 D . h a n s e n i i 0.8 1.63 S . p a r a d o x u s 0.43 S . m i k a t a e 3 S . c e r e v i s i a e 4.09 5 S . b a y a n u s 0.75 -2 < 10 K . l a c t i s 4 0.7 1 0.23 Y . l i p o l y t i c a 1.43 1.89 0.6 2 A . g o s s y p i i 0.98 K . w a l t i i 1.20 0.5 Rates of genome rearrangements among Hemiascomycetes: S. cerevisiae S. paradoxus S. mikatae S. bayanus C . g l a b r a t A . g o s s y p K . l a c t i s K . w a l t i i C . a l b i c a n D . h a n s e n i i Y . l i p o l y t i c a Fischer et al., PLoS Genetics, 2006

  38. 3 0 0 2 5 0 2 0 0 S. cerevisiae vs C. glabrata K. lactis vs A. gossypii Number of synteny blocks 1 5 0 1 0 0 5 0 0 5 1 0 1 5 2 0 2 5 3 0 3 5 4 0 4 5 5 0 > 5 0 number of genes in synteny blocks Synteny conservation among Hemiascomycetes: Genome reorganization

  39. Synteny conservation among Hemiascomycetes: Constraints onto gene order changes Proportion of genes in synteny that are essentials (1176/5807) (914/4268) (886/3814) (101/340) (58/157) (625/2481) (40/113) (10/23)

  40. Conclusions : • Moderate genome reorganization between closely related species • Few translocations • 90% of the synteny breakpoints are due to alternative loss of duplicated genes • Major role of duplications onto chromosomal dynamics • WGD • Segmental duplications • tandem gene duplications • Massive genome reorganization at larger evolutionary distances: • hundreds of interchromosomal rearrangements • Important reshuffling of gene order • Variable rates of genome rearrangements between lineages but also at different times within a lineage: • pathogenic yeasts having the most unstable genomes

  41. - Unité de Genetique des Génomes Bactériens Eduardo Rocha - Unité Génomique des Microorganismes Pathogènes Massimo Vergassola - Laboratoire de Biologie Moléculaire de la Cellule (ENS Lyon) Frédéric Brunet - The Génolevures Sequencing Consortium GDR 2354 CNRS Plateforme séquençage, Genopole Institut Pasteur Genoscope Cécile Neuvéglise Pascal Durrens Jean-Luc Souciet - Unité de Génétique Moléculaire des Levures Romain Koszul, Celia Payen, Ingrid Lafontaine, Bernard Dujon - Genome Stability Group (Nottinhgam, UK) Edward J. Louis

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