Download Wide-spread polyploidizations during plant evolution Dicot

2/3/2015
Telomere-centric genome repatterning
determines recurring chromosome number
reductions during the evolution of eukaryotes
Wide-spread polyploidizations during
plant evolution
<0.5
~70
~50
12-15
~60
Xiyin Wang
Dicot polyploidizations
maize
monocot
1 0.01rice
170-235
Plant Genome Mapping Laboratory, University of Georgia, USA
Center for Genomics and Biocomputation, Hebei United University, China
sugarcane
11-15 sorghum
?
112156
wheat
barley
Brachypodium
18tomato
euasterids I
23
potato
sunflower
euasterids II
lettuce
castor bean
3-5
poplar
eurosids I
melon
15-23
soybean
8-10
Medicago
cotton
13-15 1-2
papaya
15-20
eurosids II
Arabidopsis
8-15
Brassica
grape
asterids
eudicot
rosids
Chromosome number reduction
Starting from dotplot
Rice chromosomes 2, 4, and 6
polyploidy
speciation
P1
Q1
P2
Q2
•Example: Dotplot of rice and
sorghum
•All non-shared changes are in
sorghum, e.g. two chro. fusion
•All other changes are shared by
rice and sorghum
•Rice preserves grass ancestral
genome structure
•For ancestral chromosome A,
after WGD, you have 2 A
•A fission model:
A => R2
A => R4, R6
•A fusion model:
A1 => R4
A2 => R6
A1+A2 => R2
•Likely chromosome fusion
Repeats accumulation at
colinearity boundaries, which
would not be like that for fission
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Rice chromosomes 3, 7, and 10
Banana can answer the question
•For ancestral chromosome A,
after WGD, you have 2 A
•A fission model:
A => R3
A => R7, R10
•Fission model:
One ancestral chromosome
split to produce R4 and R6
Another duplicate – R2
•A fusion model:
A1 => R7
A2 => R10
A1+A2 => R3
• Fusion model:
Two ancestral chromosomes
merged to produce R2
Two other duplicates-R4 and
R6
•Likely chromosome fusion
Repeats accumulation at
colinearity boundaries, which
would not be like that for fission
Grasses had 7 ancestral chromosomes
before WGD (n=7)
•A1 => R1
•A1 => R5;
•A6 => R8
•A6 => R9
•A2 => R4
•A3 => R6
•A2+A3 => R2
•A7 => R11
•A7 => R12
• Similar to R3, R7 and R10
A model of genome repatterning
•A nested fusion model
•A4 = R7
•A5 = R10
•A4+A5 => R3
Murat et al. 2010.
Genome research.
Key rearrangement patterns
How genomic repatterning occurred?
•NCF: nested chromosome fusion
•Repeat may mediate.
•Is that enough?
•Simulation test: 1000 repeats
•Exchange of chromosome arms
•IV: inversion
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Homologous chromosome pairing
Circular and free-end chromosomes
•Is it physically possible?
•Biology depends on physics: space, distance, interaction, time, force
•Chromosomes: interact, mingled, pull apart, break, merge
+
lost
•Telomere clustering
(bouquet structure)
•Nucleus oscillation
•DNA recombination
Susan et al. 2001. Journal of Cell Research
A theory of telomere rearrangement
Why extra centromere(s) lost?
+
+
lost
+
lost
•Satellite chromosome (SC): two telomeres and a little extra DNA
•SC formation and loss result in chromosome number reduction
Reconstruct genomic repatterning
dynamics-Grass genomes
Reconstruct genomic repatterning
dynamics-Arabidopsis genomes
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Lysak’s model
Human and chimp
•Human chromosome 2 is a end-end
merge between chimp 2A and 2B
Chimpanzee*
Human*chro*2*
•Inversion to produce telo- or acrocentric chromosomes
•This would break gene colinearity
•But not observed in some cases,
which was attributed to a second
inversion recovering colinearity
•Inversion occurred often, and was
not necessarily related to
chromosome fusion.
Yeast – different model?
•
For yeast -- Gondon et al.
2011. Plos genetics:
•
Chromosome number
reduction occurs by the
simultaneous removal of a
centromere from a
chromosome and fusion of
the rest of the chromosome
to another that contains a
working centromere. This
process also results in
telomere removal and the
movement of genes from the
ends of chromosomes to
new locations in the middle
of chromosomes.
Figure 2. Cart oon showing t he rearrangem ent s ind icat ed b y lowercase let t ers in Figure 1. Monocolored chromosomes belong to the
WGD Ancestor. Chromosomes in gray boxes are extant L. kluyveri chromosomes. Events encircled by a color correspond to events on branches of the
same color in Figure 1. Black crossed lines between chromosomes represent points of interchromosomal translocations, and square brackets along
chromosomes (events c, f and h) represent inversions. Arrows point to the products resulting from each rearrangement. The rearrangement for event
o (marked with two asterisks) is not shown as it involves a reciprocal translocation located one gene from the edge of the Ancestral inference, which
essentially swaps the telomeres of Anc3 and Anc8 at the ends of Lklu3 and Lklu4.
doi:10.1371/journal.pgen.1002190.g002
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Yeast – different model?
Mechanisms of Chromosome Number Evolution in Yeast
Mechanisms of Chromosome Number Evolution in Yeast
PLoS Genetics | www.plosgenetics.org
Chro*2B*
Chro*2A*
July 2011 | Volume 7 | Issue 7 | e1002190
Gordon’s model:
The major mechanism of
centromere loss was associated
with the telomere-to-telomere
fusion of two chromosomes with
the loss of one of the
centromeres.
Figure 3. Progression of rearrangem ent s and chromoso me fusions leading t o t he loss of a cent romere in Z. rouxii. Two non-reciprocal
telomeric translocations and a telomere-to-telomere fusion gave rise to the extant chromosome structures in Z. rouxii. Chromosomes in green boxes
are those that underwent rearrangements, while those in gray boxes are finished translocation products (i.e., extant regions in Z. rouxii). The edges of
the breakpoint s are labelled with both the Ancestral and current Z. rouxii gene names. In the bottom step, the loss of a centromere occured
contemporaneously with the two chromosomes fusing at their telomeres. All three rearrangements led to the internalisation of previously telomeric
genes. The panels on the right show details of the gene orders and internalized telomeric genes at the junctions.
doi:10.1371/journal.pgen.1002190.g003
CDEI I I consensus is 26 bp. Within a given species there are
often further invariant sites in their CDEI or CDEI I I regions,
for example G at positions 2 and 8 in S. cerevisiae CDEI I I . T he
PLoS Genetics | www.plosgenetics.org
A model for linear chromosomes
-----supporting evidence
Fu et al. 2013. PNAS:
The centromere is the part of the
chromosome that organizes the kinetochore,
which mediates chromosome movement
during mitosis and meiosis. A small fragment
from chromosome 3, named Duplication 3a
(Dp3a), was described from UV-irradiated
materials by Stadler and Roman in the 1940s
[Stadler LJ, Roman H (1948) Genetics
33(3):273–303]. The genetic behavior of Dp3a
is reminiscent of a ring chromosome, but
fluoresecent in situ hybridization detected
telomeres at both ends, suggesting a linear
structure. This small chromosome has no
detectable canonical centromeric sequences,
but contains a site with protein features of
functional centromeres such as CENH3, the
centromere specific H3 histone variant, and
CENP-C, a foundational kinetochore protein,
suggesting the de novo formation of a
centromere on the chromatin fragment.
intervening CDEI I regions are always highly AT -rich (76–98%).
T he length of CDEI I varies twofold among species, but there is
remarkably little CDEI I length variation within each species,
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July 2011 | Volume 7 | Issue 7 | e1002190
Conclusions
•
•
•
•
•
Chromosome number reduction is accompanied by
the production of satellite chromosomes.
Grass common ancestor had 7 chromosomes
rather than 5 raised previously.
The ‘invading’ and ‘invaded’ chromosomes are
frequently homoeologs, originating from duplication
of a common ancestral chromosome.
Novel chromosomes were often constructed by
using the existing telomeres of ‘invaded’ and
centromeres of ‘invading’ chromosomes, the
alternative ones were lost.
A general mechanism of restoring small linear
chromosome numbers in higher eukaryotes.
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References

Wang X, Wang Z, Guo H, Zhang L, Wang L, Li J, Jin D,
Paterson AH. Telomere-centric genome repatterning
determines recurring chromosome number
reductions during the evolution of eukaryotes. New
Phytologist. 2015.

Movies are available at New Phytologist website.

[email protected]
Acknowledgements
• Thanks to
Andrew Paterson
Zhenyi Wang
Dianchuan Jin
Hui Guo
Lan Zhang
• NSF, CNSF, Hebei-NSF, 100-talents projects.
Thanks for your patience
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