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Whole Genome Duplications (Polyploidy)

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  1. Whole Genome Duplications (Polyploidy) Made famous by S. Ohno, who suggested WGD can be a route to evolutionary innovation (focusing on neofunctionalization) Ohno proposed in the 1970s that vertebrate lineage underwent two WGDs … later confirmed with whole-genome sequence data. WGDs are most common in plants but observed in vertebrates, fishes, yeast, and Paramecium, among other species

  2. Major mechanisms of polyploidy • Gameticnonreduction- production of unreduced gametes caused by an error in meiosis • Somatic doubling - production of a cell with twice the normal chromosome number caused by an error in mitosis • Polyspermy – fertilization of multiple gametes Errors in meiosis/mitosis can be caused by genetic or environmental factors

  3. Production of 2n gametes Spindle error or failure Abnormal chromosome pairing Abnormal or absent cytokinesis Pre-meiotic doubling Produced at an average rate of 0.5% per gamete Bretagnolle and Thompson New Phytol. (1995)129: 1-22

  4. Types of Polyploidy Autopolyploidy– chromosomal duplications derived from the same species … produce ohnologs Allopolyploidy– chromosomal duplications derived from different species … produce homeologs

  5. Timeline after WGD • Initial duplication of entire genome • autopolyploid = identical genome • Gene loss is likely frequent immediately after (although some papers • find no evidence of this) • which copy is lost is initially random • As sequences diverge, loss may not be random • sub/neofunctionalization may favor retention of specific ohnologs • Chromosomal rearrangements reduces 2X chromosome number • Reciprocal Gene Loss (RGL) in different individuals • can promote speciation

  6. From Kellis & Lander. Nature 2004

  7. Reciprocal Gene Loss (RGL): differential loss of ohnologs can lead to speciation (due to problems pairing chromosomes) Ancient WGD’s correlate with increased species diversity and even radiations WGD-driven speciation (via RGL) may be more likely to occur soon after WGD: rate of gene loss is highest soon after WGD and the copy lost is more likely to be random Mating RGL in individuals WGD event Difficulties during subsequent meiosis (F2s)

  8. The costs & benefits of WGD Costs: Doubles the DNA content and chromosome number More DNA = larger cells, larger volume, more proteins required Benefits: Doubles whole pathways of functionally related genes Maintains balanced expression across the genome

  9. The Balance Hypothesis Single-gene duplication can = stoichiometric imbalance WGD maintains stoichiometry (at least initially) The Balance Hypothesis predicts that proteins in multi-subunit complexes and proteins that require precise stoichiometry are more likely to be influenced by WGD vs single-gene duplications

  10. The fate of duplicate genes after WGD ‘Classical’ sub- or neo-functionalization (“6 – 36% of ohno. pairs have one with higher rate of divergence note this evolution can occur at the level of function OR expression

  11. The fate of duplicate genes after WGD ‘Classical’ sub- or neo-functionalization note this evolution can occur at the level of function OR expression 2. Buffering (?) Observation: yeast genes with retained ohnologs have less phenotypic consequence of deletion … probably due to redundancy ? But is the driving force for their retention? ( seems weird that buffering could drive their retention )

  12. The fate of duplicate genes after WGD ‘Classical’ sub- or neo-functionalization note this evolution can occur at the level of function OR expression 2. Buffering (?) 3. Benefit of copy number increase (maintaining stoichiometry across pathways) e.g. Most glycolytic enzymes & most ribosomal proteins in S. cerevisiae are retained Ohnologs

  13. The fate of duplicate genes after WGD ‘Classical’ sub- or neo-functionalization note this evolution can occur at the level of function OR expression 2. Buffering (?) 3. Benefit of copy number increase (maintaining stoichiometry across pathways)

  14. The fate of duplicate genes after WGD ‘Classical’ sub- or neo-functionalization note this evolution can occur at the level of function OR expression 2. Buffering (?) 3. Benefit of copy number increase (maintaining stoichiometry across pathways) 4. Need to maintain stoichiometry across pathways

  15. The fate of duplicate genes after WGD ‘Classical’ sub- or neo-functionalization note this evolution can occur at the level of function OR expression 2. Buffering (?) 3. Benefit of copy number increase (maintaining stoichiometry across pathways) 4. Need to maintain stoichiometry across pathways 5. Evolution of new regulatory circuits (‘rewiring’)

  16. Veronet al. MolBiolEvol2007

  17. unicellular ciliate (eukaryote): evidence of three ancient and successive WGDs • find no evidence for rapid gene loss shortly after WGD • the latest WGD correlates with expansion of sister species • 10-16% of ohnologs show asymetric evolutionary rates (i.e. one copy faster) • Gene retention driven by stiochiometric requirements (complexes) and expression • abundance (higher expression = more likely to be retained)