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One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Prof. Doug SoltisDepartment of Biology
College of Liberal Arts & SciencesUniversity of Florida
One Plus One Is Better Than Two:Genome Doubling in Flowering Plants
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Overview: background
• Definitions
– What is genome doubling (or polyploidy)?
– Autopolyploids vs. allopolyploids
• Importance
– In nature
– Economically
– Examples
• Formation
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Overview: recent discoveries
• Reconsider the traditional tenets: major questions
– Frequency of polyploidy
– Polyploidy and diversification
– Importance of autopolyploidy
– Multiple origins of polyploids (origins of species)
– Polyploids as genomically dynamic
Genomic and expression changes that accompany polyploidy
Chromosomal changes in polyploids
Caught in the act ‐what can we learn from the study of recently formed polyploid species?
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
2The screen versions of these slides have full details of copyright and acknowledgements
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Lets get started
Are you ready?
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Overview
• Definitions
– What is genome doubling (or polyploidy)?
– Autopolyploids vs. allopolyploids
• Importance
– In nature
– Economically
– Examples
• Formation
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Polyploidy
• Diploid ‐ nucleus contains two copies of each chromosome
• Polyploid ‐ nucleus contains three or more copies of each chromosome
– Autopolyploid ‐ formed from a single species
– Allopolyploid ‐ combines the genomes of more than one species
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Significance of polyploidy
• Flowering plants are of ancient polyploid origin
• Seed plants are of polyploid origin
• 95% of all ferns may be polyploid
• Most of the world’s worst weeds are polyploid
• Many major crops are polyploid
– Wheat, corn, sugar cane, cotton, potato, coffee
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Success of the tetraploids: size matters
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T. dubPullman
T. dubRosalia
T. porrPullman
T. pratMoscow
T. miscPullman
T. miscMoscow
T. miscSpangle
T. mirPullman
T. mirRosalia
T. mirPalouse
Dry Weight (g)
Species and Population
Field Aboveground Biomass
Tetraploids
Diploids
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Broader systematic importance of polyploidy (genome doubling)
Two episodes of polyploidy for vertebrates
Salmonids are tetraploids
Genome of yeast
was anciently duplicated
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Broader systematic importance of polyploidy (genome doubling)
Odotophrynus americanus
Shrimp
Flatworms
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Extent of polyploidy: examples
Taxon Diploid Chromosome Numbers
• Sedum 16, 24, 32, 38, 56, 64, 128 ‐ 640
• Saxifraga 10 ‐ 200
• Claytonia virginica 12 ‐ 192
• Ophioglossum 200 – 1262
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Ophioglossum
Ophioglossum2n = 1262
World record!
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Overview
• Definitions
– What is genome doubling (or polyploidy)?
– Autopolyploids vs. Allopolyploids
• Importance
– In nature
– Economically
– Examples
• Formation
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Formation—simplistic view: hybridization and then chromosome doubling
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Unreduced gametes
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Formation: polyploidy as instant speciation
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Polyploidy: traditional views
• Polyploidization events rare; a “plant thing”
• Little long term evolutionary impact
• Autopolyploids considered extremely rare
• Each polyploid species had a single origin
– Genetic uniformity
– “Buffering effect” of multiple genomes
• Polyploids as “evolutionary dead ends”
– W. H. Wagner
– G. L. Stebbins
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Polyploidy: traditional views replaced by new paradigm
• Polyploidy prevalent; a major force in eukaryotes
– A driver of speciation/diversification
• Autopolyploids common
• Polyploid species ‐more than one origin
• Polyploids as evolutionarily dynamic
– Rapid genomic changes
– Changes in chromosomes, gene expression,
subfunctionalization and more
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Genome sequence of Arabidopsis
• Small genome (157 Mbp), but….
• Two or three rounds of ancient genome duplication(Vision et al., 2001; Bowers et al., 2003)
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Polyploidy in all sequenced angiosperm genomes
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Amborella trichopoda evolutionary reference genome
• Shrub, New Caledonia
• Spiral arrangement of floral parts
• Undifferentiated perianth
Eudicots (e.g. Arabidopsis, Populus, Vitis, Carica)
Ceratophyllum
Monocots (e.g. Oryza, Zea)
Magnoliids
ChloranthaceaeAustrobaileyalesNymphaealesAmborellaGymnosperms
Angiosperms
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Ancient polyploidy
Jiao et al., 2011
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Pre‐angiosperm WGD confirmed
High resolution analysis of intragenomic syntenic regions from Amborella that are putatively derived from a pre‐angiosperm whole genome duplication event; Note the series of collinear genes between the two regions
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Ancient “hexaploidy” in eudicots
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Ancient polyploidy in angiosperms: it’s everywhere
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• Revised estimate – 100%
• Real question – How many rounds of genome
duplication have occurred in various lineages of angiosperms?
Polyploidy in the flowering plants
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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(1) Is there a perfect correspondence between ancient
polyploidization and increased net diversification?
(2) Is there a 'delay' in elevated net diversification rates
following polyploidization?
Questions
Tank, DC, JM Eastman, MW Pennell, DE Soltis, PS Soltis, and LJ Harmon, Progressive radiations, polyploidy, and the pulse of angiosperm diversification
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Nine successful whole genome duplications
Tank, DC, JM Eastman, MW Pennell, DE Soltis, PS Soltis, and LJ Harmon, Progressive radiations, polyploidy, and the pulse of angiosperm diversification
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Polyploidization
Random
• Is there a 'delay' in elevated net
diversification rates following polyploidization?
‒ 5/9 nodes (p=0.0003)
Internode distance
Density
‐20 ‐10 0 10 20
0.00
0.05
0.10
0.15
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Polyploidy: traditional views replaced by new paradigm
• Polyploidy prevalent; a major force in eukaryotes
– A driver of diversification
• Autopolyploids common
• Polyploid species ‐‐more than one origin
• Polyploids as evolutionarily dynamic
– Rapid genomic changes
– Changes in gene expression, subfunctionalization and more
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Autopolyploidy in the angiosperms
• Traditional view ‐ fewer than 5 good examples
• Galax urceolata
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Autopolyploidy in Tolmiea menziesii
Diploids and tetraploids have:
• Distinct ranges
• Reproductively isolated
• Cryptic morphological differences2n = 28
2n = 14
T. menziesii
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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What would Darwin do?
T. diplomenziesii
2 species?
2n = 28
2n = 14
T. menziesii
Diploids and tetraploids have:
• Distinct ranges
• Reproductively isolated
• Cryptic morphological differences
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Autopolyploidy and cryptic species:insights from the California flora
• Of 2647 species, 334 species (13%) have clear 3x, 4x, or higher multiples of the base chromosome number
• Most are presumed autopolyploids, all require study
• If each cytotype represented a distinct species, the total number of unrecognized species in CA is actually 483
J. J. Ramsey and B. C. Husband, unpublished; Soltis et al. 2007
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Polyploidy: traditional views replaced by new paradigm
• Polyploidy prevalent; a major force in eukaryotes
• Autopolyploids are common ‐ have we grossly
underestimated the number of species?
• Polyploid species ‐more than one origin
• Polyploids as evolutionarily dynamic
– Rapid genomic changes
– Changes in gene expression,
subfunctionalization and more
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Tragopogon: a North American success story
• Diploids introduced from Europe 1900s:
– T. dubius, T. porrifolius, T. pratensis
• Allotetraploids T. mirus and T. miscellus named in 1950
• Ancestry of tetraploids is well‐documented
• Polyploids
– Native to western N.A.; have not formed in Europe
– Less than 80 years old
– Formed repeatedly
– Have been very successful
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Quotations from Marion Ownbey (1950)
• Described populations of the newly formed allotetraploids as “small and precarious”
• Had “attained a degree of success”; were “competing successfully” with diploid parents
• Would be “important to follow the ecological development of the newly formed polyploids”
through time
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The Tragopogon triangle
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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A text book example of polyploidy
Novak, Soltis, Soltis (1991)
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Molecular markers: origins of species
• T. mirus 11+ origins
• T. miscellus 15+ origins
• Frequent origins, within a short time period (<80 years)
• In a small geographic area (eastern WA and adjacent ID)
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The Arctic: multiple origins on a broad scale
The rule:many polyploids
are of multiple origin
Originsof species!
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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• Polyploidy prevalent; a major force in eukaryotes
• Autopolyploids are common‐‐have we grossly underestimated the number of species?
• Polyploid species often have more than one origin
• Polyploids as evolutionarily dynamic
– Rapid genomic changes
– Changes in gene expression, subfunctionalization and more
Polyploidy: traditional views replaced by new paradigm
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Cotton
Wendel, J.
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Brassica napus
• Transcriptome shock
• Frequent expression change
• Chromosomal change
• Fragment losses
• Changes occurred independently among lines
Pires, C.
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Well known polyploid models are “old”
Taxon Age
• Gossypium 1‐2 mya
• Triticum 10,000 ya
• Nicotiana 200,000 years to 4.5 mya
• Arabidopsis suecica 12,000‐300,000 ya
• Brassica napus 4,000 ya
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Polyploidy in compositae: ancient to recent
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Compositae: ancient polyploidy
• Parallel retention of duplicate genes across tribes
• Consistent patterns of gene retention and gene loss
at deep levels
Barker et al. 2008
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Convergent gene fates at deep levels
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The Tragopogon triangle
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Multiple origins of the same polyploid species pose the questions:
• Does evolution repeat itself?
• When you merge diploid genomes:
Are there genomic “rules” or “principles”?
• How much of evolution is stochastic?
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Is evolution predictable?
No!
“Chains of historical events are so intricate,
so imbued with random and chaotic elements,
so unrepeatable in encompassing such a multitude
of unique objects, that standard models of simple
prediction and replication do not apply”
S. J. Gould
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Genetic & genomic consequences of polyploidy in Tragopogon: repeated evolution
• Concerted evolution of duplicated genes
• Loss and silencing of duplicated genes
• Tissue specific changes in expression
• Chromosomal changes
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Define homeolog
Tragopogon mirus
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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One at a time gene approach
Loss of T. pratensis homoeolog
Loss of T. dubius homoeolog
Buggs et al. 2009
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Genomics approach
• Data ~ 400 homeolog‐specific SNPs
– ~20% of loci missing one or both alleles of a homeolog
– Repeated patterns of homeolog loss
– Gene ontology categories of missing genes correspond
with those lost after ancient WGD in Compositae
• Outcomes of WGD are predictable <40 generations
• In other words it like the movie “Groundhog Day”
Buggs et al. 2012, American Journal of Botany 99: 372‐382Buggs et al. 2012, Current Biology 22: 1‐5
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Homeolog loss: natural populations of separate origin
0%
10%
20%
30%
40%
50%
60%
% con
tig
gDNA pratensis loss
gDNA equal
gDNA dubius loss
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Homeolog loss: natural vs. synthetic T. miscellus
0%
10%
20%
30%
40%
50%
60%
70%
natural gDNA synthetic gDNA
% co
ntig
pratensis loss
equal
dubius loss
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119211631157
Lf Co Pp Ov St Sl Ph Lf Co Pp Ov St Sl PhLf Co Pp Ov St Sl Ph
But wait, there’s more:tissue‐specific expression of homeologs
Suggests repeated subfunctionalization in T. miscellus
R. Buggs
Co = Corolla; St = Stigma; Sl = Style; Pa = Pappus; Ph = Phyllary; Ov = Ovary
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Genome in situ hybridization (GISH): Tragopogon miscellus
Lim et al. 2008; Chester et al. 2012
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Compensated aneuploids
Tetrasomy Nullisomy
A B C D E F A B C D E F
Trisomy Monosomy
TrisomyMonosomy
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• Substantial chromosomal instability following allopolyploidy
• A common process following polyploidy
• A driver of allopolyploid speciation with unexplored
implications for gene loss, gains, and changes in expression
Chromosomal big picture summary
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Summary: does evolution repeat itself?
• Concerted evolution in the same direction (T. dubius)
• Chromosomal instability
• Same genes undergo loss/silencing
• Same genes show no evidence of loss/silencing
• Loss/silencing often in the same direction (T. dubius)
• Evidence for repeated subfunctionalization
• But, within populations loss/silencing is stochastic
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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There is stochasticity, but many facets of evolution are repeated…
there may be some rules to polyploidy
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What drives these patterns?
• Gene dosage balance?
– Preservation of stoichiometric relationships may be responsible for maintaining duplicate copies of genes whose
protein products interact
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The dynamic nature of polyploidy
• Polyploidy a major force in eukaryotes
• Associated with major diversification events
• Amborella‐ useful evolutionary reference genome
• Autopolyploidy ‐ common
• Multiple origins common – source of novelty
• Polyploid genome evolution—dynamic
• Outcomes of WGD are predictable <40 generations
• Some rules to polyploidy
• No single polyploidy paradigm – clade‐specific?
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Thanks
• Numerous collaborators
• Brad Barbazuk, Pat Schnable
• Amborella Genome Project
• The Soltis lab
• Our Sponsors…
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Traglodytes
Jennifer Tate
Pam Soltis Jin Koh
Vaughan Symonds
Doug Soltis
Evgeny Mavrodiev David
Lefkowitz
Richard Buggs
AndrewDoust
Pat Schnable
Joe Gallagher
Lyderson Viccini
Mike Chester
Chris Pires
Ingrid Jordon‐Thaden
Andrew Leitch
Yoong Lim
Roman Matyasek Ales
Kovarik
Mike Chester
Joe Combs
Brad Barbazuk
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Tragopogon ski team
Andrew Leitch
Ales Kovarik
Yoong Lim
RomanMatyasek
One Plus One Is Better Than Two: Genome Doubling in Flowering Plants
Prof. Doug Soltis
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Tragopogon
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