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Wide-spread polyploidizations during plant evolution

Telomere-centric genome repatterning <0.5 sugarcane determines recurring chromosome number 11-15 sorghum ~70 ~50 12-15 maize reductions during the evolution of eukaryotes monocot 1 0.01rice wheat barley Brachypodium 170-235 18- tomato 23 potato euasterids I asterids sunflower euasterids II lettuce

~60 3-5 castor bean poplar Xiyin Wang ? melon eurosids I eudicot 15-23 8-10 soybean Medicago Plant Genome Mapping Laboratory, University of Georgia, USA cotton rosids 13-15 1-2 Center for Genomics and Biocomputation, Hebei United University, China papaya 112- 15-20 eurosids II 156 8-15 Arabidopsis Brassica grape

Dicot polyploidizations number reduction

Starting from dotplot Rice 2, 4, and 6 •For ancestral chromosome A, after WGD, you have 2 A speciation •A fission model: A => R2 P1 Q1 P2 Q2 A => R4, R6

•Example: Dotplot of rice and •A fusion model: sorghum A1 => R4 A2 => R6 •All non-shared changes are in A1+A2 => R2 sorghum, e.g. two chro. fusion •Likely chromosome fusion •All other changes are shared by Repeats accumulation at rice and sorghum colinearity boundaries, which would not be like that for fission •Rice preserves grass ancestral genome structure

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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 •Fission model: A => R7, R10 One ancestral chromosome split to produce R4 and R6 •A fusion model: Another duplicate – R2 A1 => R7 A2 => R10 • Fusion model: A1+A2 => R3 Two ancestral chromosomes merged to produce R2 •Likely chromosome fusion Two other duplicates-R4 and Repeats accumulation at R6 colinearity boundaries, which would not be like that for fission • Similar to R3, R7 and R10

Grasses had 7 ancestral chromosomes before WGD (n=7) A model of genome repatterning

•A1 => R1 •A6 => R8 •A nested fusion model •A1 => R5; •A6 => R9

•A2 => R4 •A7 => R11 •A3 => R6 •A7 => R12 •A2+A3 => R2

•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

• clustering (bouquet structure)

•Nucleus oscillation

•DNA recombination

Susan et al. 2001. Journal of Cell Research

A theory of telomere rearrangement Why extra (s) lost?

+ + lost

+

lost •Satellite chromosome (SC): two and a little extra DNA •SC formation and loss result in chromosome number reduction

Reconstruct genomic repatterning Reconstruct genomic repatterning dynamics-Grass genomes dynamics-Arabidopsis genomes

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Lysak’s model Human and chimp

•Human is a end-end merge between chimp 2A and 2B

Chimpanzee* Chro*2B* Chro*2A*

Human*chro*2* •Inversion to produce telo- or acro- centric 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.

Mechanisms of Chromosome Number Evolution in Yeast Yeast – different model?Mechanisms of Chromosome Number Evolution in Yeast Yeast – different model? • For yeast -- Gondon et al. 2011. Plos : Gordon’s model: The major mechanism of • Chromosome number centromere loss was associated reduction occurs by the with the telomere-to-telomere simultaneous removal of a fusion of two chromosomes with centromere from a the loss of one of the 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. Cartoon showing the rearrangements indicated by lowercase letters 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 Figure 3. Progression of rearrangements and chromosome fusions leading to the loss of a centromere in Z. rouxii. Two non-reciprocal 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 telomeric translocations and a telomere-to-telomere fusion gave rise to the extant chromosome structures in Z. rouxii. Chromosomes in green boxes essentially swaps the telomeres of Anc3 and Anc8 at the ends of Lklu3 and Lklu4. are those that underwent rearrangements, while those in gray boxes are finished translocation products (i.e., extant regions in Z. rouxii). The edges of doi:10.1371/journal.pgen.1002190.g002 the breakpoints 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 rearrangementsled 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

CDEIII consensus is 26 bp. Within a given species there are intervening CDEII regions are alwayshighly AT-rich (76–98%). PLoS Genetics | www.plosgenetics.org 4 July 2011 | Volume 7 | Issue 7 | e1002190 often further invariant sites in their CDEI or CDEIII regions, The length of CDEII varies twofold among species, but there is for example G at positions 2 and 8 in S. cerevisiae CDEIII. The remarkably little CDEII length variation within each species,

PLoS Genetics | www.plosgenetics.org 7 July 2011 | Volume 7 | Issue 7 | e1002190

A model for linear chromosomes -----supporting evidence Conclusions Fu et al. 2013. PNAS: • Chromosome number reduction is accompanied by The centromere is the part of the chromosome that organizes the kinetochore, the production of satellite chromosomes. which mediates chromosome movement • Grass common ancestor had 7 chromosomes during mitosis and . A small fragment from , named Duplication 3a rather than 5 raised previously. (Dp3a), was described from UV-irradiated • The ‘invading’ and ‘invaded’ chromosomes are materials by Stadler and Roman in the 1940s [Stadler LJ, Roman H (1948) Genetics frequently homoeologs, originating from duplication 33(3):273–303]. The genetic behavior of Dp3a of a common ancestral chromosome. is reminiscent of a ring chromosome, but • Novel chromosomes were often constructed by fluoresecent in situ hybridization detected telomeres at both ends, suggesting a linear using the existing telomeres of ‘invaded’ and structure. This small chromosome has no centromeres of ‘invading’ chromosomes, the detectable canonical centromeric sequences, alternative ones were lost. but contains a site with protein features of functional centromeres such as CENH3, the • A general mechanism of restoring small linear centromere specific H3 variant, and chromosome numbers in higher eukaryotes. CENP-C, a foundational kinetochore protein, suggesting the de novo formation of a centromere on the fragment.

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References Acknowledgements

 Wang X, Wang Z, Guo H, Zhang L, Wang L, Li J, Jin D, • Thanks to Paterson AH. Telomere-centric genome repatterning determines recurring chromosome number Andrew Paterson reductions during the evolution of eukaryotes. New Zhenyi Wang Phytologist. 2015. Dianchuan Jin

Hui Guo  Movies are available at New Phytologist website. Lan Zhang

• NSF, CNSF, Hebei-NSF, 100-talents projects.  [email protected]

Thanks for your patience

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