alice ecker february 27th 2007 n.
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Alice Ecker February 27th, 2007. Ancient Polyploidy. Ancient Polyploidy. Definition (ancient vs. neopolyploidy) Importance of ancient polyploidy Known ancient genome doublings: Saccharomyces Arabidopsis. Ancient vs. Neopolyploidy. Neopolyploidy is characterized by...

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ancient polyploidy
Ancient Polyploidy
  • Definition (ancient vs. neopolyploidy)
  • Importance of ancient polyploidy
  • Known ancient genome doublings:
    • Saccharomyces
    • Arabidopsis
ancient vs neopolyploidy
Ancient vs. Neopolyploidy
  • Neopolyploidy is characterized by...
    • Multivalent chromosome pairing
    • Multisomic inheritance
    • Unbalanced gamete production

*Ramsey & Schemske, 2002.

ancient vs neopolyploidy1
Ancient vs. Neopolyploidy
  • Ancient polyploidy can be difficult to detect because...
    • Disomic segregation is reestablished
    • Chromosomal synteny becomes scrambled by rearrangements
    • Changes in or loss of duplicate genes

*Otto & Whitton, 2000

what is interesting about ancient polyploidy

...polyploidy has contributed little to progressive evolution.

Stebbins, 1971

...polyploidy, far from playing a secondary role in evolution, has provided the additional, uncommitted gene loci necessary for major steps in the evolution of animals.

Schultz, 1980

*Selection of quotes by Otto & Whitton, 2000.

What is interesting about ancient polyploidy?
what is interesting about ancient polyploidy1
What is interesting about ancient polyploidy?

Clearly, scientists feel differently about the role that polyploidy plays in shaping the eukaryotic tree of life!

By recognizing and studying paleopolyploidy, we can come closer to understanding the impact polyploidy has on the tempo and mode of evolution

specific ancient polyploidizations
Specific ancient polyploidizations
  • Detection made relatively easy by availability of sequenced genomes
  • Dating (or at least relative dating) made possible by availability of sequences from many taxa
  • Mode of polyploid formation often unclear (allo- or autopolyploidy)
  • Genome doublings have been detected in the human genome, but how many or when they occurred remains contentious
saccharomyces cerevisiae
Saccharomyces cerevisiae
  • Wolfe and Shields (1997) and Seoighe and Wolfe (1999) presented evidence that Saccharomyces cerevisiae is a degenerate tetraploid
ancient tetraploidy in s cerevisiae
Ancient tetraploidy in S. cerevisiae
  • One duplication is proposed, but the method of polyploid formation is unclear
  • This hypothesis is supported by two lines of evidence:
    • Large, duplicated chromosomal regions (Wolfe & Shields, 1997)
    • Gene order and comparisons to closely related species (Seoighe & Wolfe, 1997)
evidence for ancient tetraploidy in s cerevisiae
Evidence for ancient tetraploidy in S. cerevisiae
  • Duplicated chromosomal regions were detected by BLASTPing all yeast protein sequences against one another
  • Results were plotted; duplicate regions are visible as diagonal series

*Wolfe & Shields, 1997

evidence for ancient tetraploidy in s cerevisiae1
Evidence for ancient tetraploidy in S. cerevisiae
  • A total of 55 duplicated regions, containing 376 pairs of homologous genes were identified
  • These regions are argued to have arisen by polyploidy because...
    • In a significantly non-random number of duplicated regions, both duplicates are oriented the same way relative to the centromere
    • 55 independent duplications would statistically be expected to result in 7 triplicate regions; however, none were observed
slide12
Gene order as evidence for ancient tetraploidy in S. cerevisiae
  • Kluyveromyces is demonstrated to have diverged from the Saccharomyces lineage before the duplication event

*Seoighe & Wolfe, 1997

slide13
The date of tetraploid formation was estimated from the molecular clock date for the Kluyveromyces / Saccharomyces divergence (1.5x10^8 years)
aftermath of the s cerivisiae genome duplication
Aftermath of the S. cerivisiae genome duplication
  • Roughly 12.9% of S. cerivisiae's genes are polyploidy derived duplicates

*Wolfe & Shields, 1997

slide15
Gene duplicates do not appear to have diverged greatly in function
  • Genes retained in duplicate are non-randomly partitioned between functional categories
  • This suggests that duplicates were retained to increase the efficiency of the processes they already controlled

*Wolfe & Shields, 1997

aftermath of the s cerivisiae genome duplication1
Aftermath of the S. cerivisiae genome duplication
  • High expression genes were preferentially retained in duplicate

*Seoighe & Wolfe, 1997

f a c and the s cerivisiae genome duplication
F.A.C. and the S. cerivisiae genome duplication
  • Saccharomyces is able to “vigorously” ferment sugars under anaerobic conditions, setting it apart physiologically from other yeasts
  • Several sets of duplicate genes encode sugar transporters or pairs of genes that are regulated differently in aerobic vs. anaerobic conditions
f a c and the s cerivisiae genome duplication1
F.A.C. and the S. cerivisiae genome duplication
  • The proposed genome doubling event may have been crucial to Saccharomyces' ability to ferment rapidly in anaerobic conditions
  • It may also be significant that the doubling occurred around the time that angiosperms became abundant
arabidopsis
Arabidopsis
  • Bowers, Chapman, Rong, and Peterson searched the Arabidopsis genome for duplicated regions
  • Three ancient duplications were identified
arabidopsis genome analysis
Arabidopsis genome analysis
  • A database of 26,028 protein sequences was searched for matches
  • 34 nonoverlapping chromosomal segment pairs were identified, encompassing 89% of the genes searched (23,117 genes)
  • The doubling event that formed these duplicate regions was dubbed α
arabidopsis genome analysis1
Arabidopsis genome analysis
  • Using the duplicated regions, researchers next reconstructed the gene order of the diploid that gave rise to the α polyploid
  • Nested within 26 α regions were another 29 duplications
  • These duplications fell into two groups based on degree of similarity between gene copies, termed β and gamma, which represent another two ancient polyploidizations
the and duplications
The β and γ duplications
  • The β population consists of 22 non-overlapping duplicate regions and 13,449 genes (51.6% of the transcriptome)
  • The γ population conists of 7 duplicate regions, some of which overlap with β duplicates, and 5,287 genes (20.3% of the transcriptome)
dating the arabidopsis genome duplications
Dating the Arabidopsis genome duplications
  • To date the α, β, and γ duplications, Arabidopsis gene pairs were compared to genes from both distantly and closely related plants
  • If the two Arabidopsis gene copies had more in common with each other than with the heterologous genes, then the polyploidy that generated those copies post-dated divergence from the source of the heterologous sequence
  • Both rooted trees and PAM comparisons were used
estimated duplication dates
Estimated duplication dates

α Sometime between the divergences from Brassica (14.5-20.4 mya) and Malvaceae (83-86 mya)

β After divergence from monocots (170-235mya) but before divergence from other dicots in the study

γ Possibly after divergence from gymnosperms (300mya), definitely before divergence from angiosperms included in the study

implications of the arabidopsis duplications
Implications of the Arabidopsis duplications:
  • Most or all angiosperms are paleopolyploid
  • Synteny between Arabidopsis and other plants which diverged before the α polyploidization may have been underestimated
  • Inference of ancestral gene orders in model organisms has the potential to greatly aid mapping of large genomes in other organisms that may not be fully sequenced soon
slide27
Synteny in diploid

relatives of ancient

polyploids

*Seoighe, 2003

literature cited
Literature Cited:
  • Bowers, John E., Brad A. Chapman, Junkang Rong, & Andrew H. Peterson. 2003. Unraveling angiosperm evolution by phylogenetic analysis of chromsomal duplication events. Nature, 422:433-438.
  • Otto, Sarah P. and Jeannette Whitton. 2000. Polyploid Incidence and Evolution. Annu. Rev. Genet, 34:401-37.
  • Ramsey, Justin and Douglas W. Schemske. 2002. Neopolyploidy in Flowering Plants. Annu. Rev. Ecol. Syst., 33: 589-639.
  • Seoighe, Cathal. 2003. Turning the clock back on ancient genome duplication. Current Opinion in Genetics and Development, 13:636-643.
  • Seoighe, Cathal and Kenneth H Wolfe. 1999. Yeast genome evolution in the post-genome era. Current Opinion in Microbiololgy, 2:548-554.
  • Wolfe, Kenneth H. and Denis C. Shields. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature, 387:708-713.