Ancient Polyploidy
Alice Ecker
February 27th, 2007
Ancient Polyploidy

Definition (ancient vs. neopolyploidy)

Importance of ancient polyploidy

Known ancient genome doublings:

Saccharomyces

Arabidopsis
Ancient vs. Neopolyploidy

Neopolyploidy is
characterized by...

Multivalent
chromosome pairing

Multisomic inheritance

Unbalanced gamete
production
*Ramsey & Schemske, 2002.
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?
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




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 (alloor autopolyploidy)
Genome doublings have been detected in the
human genome, but how many or when they
occurred remains contentious
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


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


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. 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


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

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

Roughly 12.9% of S. cerivisiae's genes are
polyploidy derived duplicates
*Wolfe & Shields, 1997



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
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


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
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


Bowers, Chapman,
Rong, and Peterson
searched the
Arabidopsis genome
for duplicated regions
Three ancient
duplications were
identified
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 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 β and γ duplications


The β population consists of 22 nonoverlapping 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



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
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:



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
Synteny in diploid
relatives of ancient
polyploids
*Seoighe, 2003
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.