one plus one is better than two: genome doubling in ... · one plus one is better than two: genome...

One Plus One Is Better Than Two: Genome Doubling in Flowering Plants

Prof. Doug Soltis

1The screen versions of these slides have full details of copyright and acknowledgements

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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?


Prof. Doug Soltis


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Lets get started

Are you ready?

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Overview

• Definitions


– 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


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

0

2

4

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8

10

12

14

16

18

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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


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


Prof. Doug Soltis


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Ophioglossum

Ophioglossum2n = 1262

World record!

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Overview

• Definitions


– Autopolyploids vs. Allopolyploids

• Importance

– In nature

– Economically

– Examples

• Formation

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Formation—simplistic view: hybridization and then chromosome doubling


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


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


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


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


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


Prof. Doug Soltis


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– A driver of diversification

• Autopolyploids common

• Polyploid species ‐‐more than one origin



– 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


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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• Autopolyploids are common ‐ have we grossly

underestimated the number of species?

• Polyploid species ‐more than one origin



– Changes in gene expression,

subfunctionalization and more


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


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!


Prof. Doug Soltis


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• Autopolyploids are common‐‐have we grossly underestimated the number of species?

• Polyploid species often have more than one origin



– Changes in gene expression, subfunctionalization and more


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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.


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


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?


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


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


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


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


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?


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


Prof. Doug Soltis


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Tragopogon

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