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

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Presentation on theme: "Réarrangements chromosomiques Evolution des génomes de levures 2ème réunion GTGC Nantes 12 et 13 octobre 2006 Gilles Fischer."— Presentation transcript:

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 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 Hemiascomycetes Archiascomycetes Basidiomycetes Euascomycetes Neurospora, Magnaporthe, Aspergillus, etc… Mus musculus Takifugu rubripes Tetraodon negroviridis Homo sapiens Ciona intestinalis 100 * * Data from O. Jaillon et al., Nature,

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., 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: S. cariocanus S. paradoxus S. mikatae S. kudriavzevii S. cerevisiae S. bayanus var. uvarum 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 Archiascomycetes Basidiomycetes Euascomycetes Neurospora, Magnaporthe, Aspergillus, etc… monophyletic group of species closely related to S. cerevisiae viable hybrids

7 Electrophoretic Karyotypes: sensu stricto species S. cerevisiae S1S2S3 S4 S5 S6 S1S2S6 S4 S5 S3 Chromosomal Translocations: mechanism of post-zygotic isolation?

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

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

10 S.bayanus gene 1 gene 2 0.4X about 2000 neighboring gene couples : => 35 synteny breakpoints(80 predicted in total) 3 corresponded to translocations = > 32 breakpoints left ??? 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 Hemiascomycetes Archiascomycetes Basidiomycetes Euascomycetes Neurospora, Magnaporthe, Aspergillus, etc… S.cerevisiae gene 1’ gene 2’ Synteny conservation S.cerevisiae gene 1’ gene 2’ Synteny breakpoint

11 X YJR052wYJR053wYJR054wYJR055wYJR057w YJR056cYJR058c YML051w K. thermotolerans : YJR052w YML046w YJR055w YML051w YML049w K. lactis : YJR052w YML046w YJR053w YML048w YJR052w YJR053w YJR054wYJR055wYJR057w YJR056cYJR058c YML051w YML046w YML048w YML049w (i) Gene transposition:

12 YJR052w YJR053w YJR054wYJR055wYJR057w YJR056cYJR058c YML051w YML046w YML048w YML049w DUPLICATION YJR052w YJR053w YJR054wYJR055wYJR057w YJR056cYJR058c YML051w YML046w YML048w YML049w (i) Gene transposition:

13 YJR052w YJR053w YJR054wYJR055wYJR057w YJR056cYJR058c YML051w YML046w YML048w YML049w YJR052w YJR053w YJR054wYJR055wYJR057w YJR056cYJR058c YML051w YML046w YML048w YML049w RECIPROCAL GENE LOSS (i) Gene transposition:

14 YML051w YML046w YML048w YML049w (i) Gene transposition: YJR052w YJR053w YJR054wYJR055wYJR057w YJR056cYJR058c YML047c X XIII S. cerevisiae

15 YML046w YML048w YML049w (i) Gene transposition: YJR052w YJR053w YJR054wYJR055wYJR057w YJR056cYJR058c YML047c X XIII S. bayanus YML051w Fischer et al., Genome Research 2001

16 IVtII SuYBR60cSuYBR061c SuYDR037w IItIV SuYDR038c SuYDR037w S. uvarum YBR60c II YBR061c YDR036c IV YDR038c YDR037w (KRS1) S. cerevisiae Relic of YDR037w paralog (ii) Species specific gene duplication: 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 Hybrid 2n meiosis 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 Liti et al., Genetics in press S. cariocanus 0,3% 0,15% 0,1% 0,6% 1% 5% 15%

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

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

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

23 2> Level of chromosome reorganisation: Genolevures 2 Dujon et al., Nature, 2004 Human pathogen Model organism Cryotolerant, halotolerant marine yeast Alkane-using yeast S. cerevisiae C. glabrata K. lactis D. hansenii Y. lipolytica ADHoRe sofware ( Vandepoele et al., Genome Res, 2002) Genome 1 Genome 2Genome 2 gap r2r2 Synteny blocks 10 pairwise comparisons Duplication blocks 5 intra comparisons

24 S. cerevisiae C. glabrata Blocks of ancestral duplications S. cerevisiaeC. glabrata Total nb of duplicated blocks internal to chromosomes 5620 sutelomeric 21 0 Block size (kb)mean 4227 max Nb of gene pairs /blockmean max.156 Dujon et al., Nature 2004

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

26 K. lactisD. hanseniiY. lipolytica Total nb of duplicated blocks internal to chromosomes sutelomeric Block size (kb)mean max Nb of gene pairs /blockmean max K. lactisD. hanseniiY. lipolytica Sporadic segmental duplications ? Blocks of ancestral duplications

27 Example of a tandem repeat array in D. hansenii D. hansenii_ CONTIG=DEHAOK Similar to S. cerevisiae YHR179w OYE2 NADPH dehydrogenase (old yellow enzyme), isoform 1 pseudogenes Amino-acid sequence identity between copies: from 82 % to 95 % total nb of directtotal nb of tandem pairs orientationarrays S. cerevisiae 6179% 50 C. glabrata 4783% 32 K. lactis 3672 % 33 D. hansenii32992 %247 Y. lipolytica 5472 % 48

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

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

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

31 S.cerevisiaeC. glabrataK. lactisD. hansenii C. glabrata K. lactis D. hansenii Y. lipolytica

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

33

34 S.paradoxus S.mikatae S.bayanus S.cerevisiae C. glabrata K. lactis D. hansenii Y. lipolytica Low genome reorganization massive reorganization 4 translocations 2 translocations 4 translocations reference 0 0 S. paradoxus S. kudriavzevii S. cariocanus S. mikatae S. bayanus S. cerevisiae 0 Variable rates of rearrangements?

35 S.paradoxus S.mikatae S.bayanus C. albicans K. waltii S.cerevisiae C. glabrata A. gossypii K. lactis D. hansenii Y. lipolytica  Gene order conservation: GOC  =5 Species 1 gene 1 gene 2 Species 2 gene 1’ gene X ? Rates of genome rearrangements among Hemiascomycetes:

36 K. waltii A. gossypi K. lactis D. hansenii Y. lipolytica S.cerevisiae S.paradoxus S.mikatae S.bayanus C. glabrata C. albicans i GOC 0.88 GOL 0.12 GOL est X12+X13 +X15+X17 +X19 X1 X2 X4 X3 X5 X7 X8 X9 X10 X11 X12 X13 X15 X16 X17 X18 X19 X14 X6 Rates of genome rearrangements among Hemiascomycetes:

37 Fischer et al., PLoS Genetics, < < WGD K. waltii A. gossyp K. lactis D. hansenii Y. lipolytica S.cerevisiae S.paradoxus S.mikatae S.bayanus C. glabrat C. albicans GOC 0.88 GOL 0.12 GOL est X12+X13 +X15+X17 +X19 Rates of genome rearrangements among Hemiascomycetes:

38 Fischer et al., PLoS Genetics, < < WGD K. waltii A. gossyp K. lactis D. hansenii Y. lipolytica S.cerevisiae S.paradoxus S.mikatae S.bayanus C. glabrat C. albican C. albicans C. glabrata D. hansenii S. cerevisiae S. mikatae S. paradoxus K. lactis Y. lipolytica S. bayanus K. waltii A. gossypii 0.9 Genome instability scale:

39 Synteny conservation among Hemiascomycetes: Genome reorganization

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

41 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 Conclusions :

42 - Unité de Génétique Moléculaire des Levures Romain Koszul, Celia Payen, Ingrid Lafontaine, Bernard Dujon Génolevures - The Génolevures Sequencing Consortium GDR 2354 CNRS Plateforme séquençage, Genopole Institut Pasteur Genoscope Cécile Neuvéglise Pascal Durrens Jean-Luc Souciet - 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 - Genome Stability Group (Nottinhgam, UK) Edward J. Louis


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