Evolutionary trends and mechanisms
of chromosome number variation
Basic or base chromosome number (x)
• a relative concept [x has to be related to a certain taxonomic unit, e.g. genus or
(sub)family]
• monobasic taxa (single x number), dibasic taxa (two x nos.) and polybasic taxa (>2 x
nos.)
• are there any evolutionary trends in chromosome number changes?
• are the same chromosome number and similar karyotype structure indicative of close
phylogenetic relationship?
• can polybasic taxa be regarded as monophyletic?
• is the most common basic chromosome number automatically the ancestral one?
Asteraceae – example of a polybasic family
Chromosome numbers of plants vary enormously over
a 360-fold range.
n = 2 in five angiosperm species
n = 630 in the fern Ophioglossum reticulatum
Chromosome number variation
Haplopappus gracilis
Chromosome number variation
• Stasis
• Decrease (descending dysploidy)
• Increase (polyploidy and ascending dysploidy)
Chromosome Number Diversity Across Land Plants
9,000 species 200 - 250 1,290 10,560
Rice et al. (2014) New Phytol; Christenhusz and Byng (2016) Phytotaxa
1,079
12,700 295,383
Fern „Polyploidy Paradox“: high chromosome nos., but no clear
evidence. Multiple WGDs and Dysploidies ?
Clark et al. (2016) New Phytologist
64
68
46
40
48
72
44
78
90
104
216
44
48
46
44
56 1,080
18 120
92 276
22 576
40 232
22 256
44
78 160
104
1,440
416
216
88
Vanneste et al. (2015) Plant Cell
13
21
7 - 28 (69% species polyploid)
12
8-14
11, 22
12, 13
12 12
11
12
12
12
12
x = 22
x = 9 - 19
Li et al. (2015) Sci Adv
Murray (2013) in Plant Genome Diversity
Ickert-Bond and Renner (2016) JSE
Reduced Chromosome Number Diversity and
Rare Neopolyploids in Gymnosperms
M
T T
Ancient Whole-Genome Duplications in Gymnosperms
13
21
7 - 28 (69% species polyploid)
12
8-14
11, 22
12, 13
12 12
11
12
12
12
12
x = 22
Li et al. (2015) Sci Adv
Murray (2013) in Plant Genome Diversity
Ickert-Bond and Renner (2016) JSE
Post-Polyploidy Chromosomal Schuffling in Coniferales ?
de Miguel et al. (2015) GBE; Li et al. (2015) Sci Adv
2 independent WGDs ?
Li et al. (2015)
de Miguel et al. (2015)
Kotseruba et al. (2003) Genome
Jackson et al. (2002) Am J Bot
A 160-Fold Variation of Chromosome Numbers in Angiosperms
Haplopappus gracilis
n = 2
Zingeria biebersteiniana
n = 2
Voanioala gerardii
n = 303
Röser et al. (2015) CGR
Oginuma et al. (2006) PSE
Strasburgeria robusta
n = 250
diploidspolyploids
diploidization
(dysploidy, aneuploidy,...)
genome duplication
Otto and Whitton (2000) Annu Rev Genet; Rice et al. (2014) New Phytol
Distribution of Haploid Chromosome Numbers in Angiosperms
Was Shaped by Polyploidy and Subsequent Dysploidy
even = duplication
dysploidy
odd =dysploidy
allopolyploidy
2 320
Chromosome number variation
• Stasis
• Decrease (descending dysploidy)
• Increase (polyploidy and ascending dysploidy)
Allopolyploidy (and of course autopolyploidy)
• misdivision resulting in a tetrasomic plant (2n+2)
(or first trisomy: 2n+1 followed by tetrasomy, 2n+2)
or monosomic plant (2n-1, this is descending dysploidy)
• the extra chromosome can diverge from their
homologues through a translocation with nonhomologous
chromosomes
Ascending dysploidy
1. Centric fission (1 metacentric chromosome  2 telocentrics)
2. Meiotic misdivision (non-disjunction)
probably in orchids,
cycads...
Centric fissions  telocentric chromosomes in cycads (Zamia)
Centric Fissions Increase Chromosome Number in Seed Plants
18  30
26
 32
26
 42
20
20
Guo et al. (2012) Plos ONE; Karasawa and Tanaka (1980) Cytologia
Cox et al. (1998) Am J Bot; Leitch et al. (2009) Ann Bot
Centric Fissions Are Rare in Seed Plants Despite Evidence
of Efficient Chromosome Healing
Luzula elegans
Jankowska et al. (2015) Chromosoma
McClintock (1941), Marks (1957), Brighton (1978), Schubert et al. (1992), Slijepcevic
and Bryant (1998), Tsujimoto et al. (1999), Jankowska et al. (2015), Koo et al. (2015),
Wanner et al. (2015), Rocha et al. (2016)
bread wheat, ditelosomic Dt 3AS
courtesy of B. Friebe (Koo et al. 2015, PLoS ONE)
„Sticky“ chromosome ends can be stabilized by de novo
telomere formation or „chromosome healing.“
Telocentrics can be „unstable“…
Wanner et al. (2015) Chromosoma
Bst7
Bst3
Bst6
Bst1
Bst4
Bst2
Bst5
Boechera genomes originated from
eight ancestral chromosomes
descending dysploidy
n = 8  n = 7
Boechera stricta
(n = 7)
A1
C1
D
BS2
C2
A2 F
X
W
G
I
J
V
K
H
L
M
N
O
P
Q
R
S
T
U
BS3 BS4 BS5 BS6 BS7BS1
E
B
Mandáková et al. (2016) Plant J
20
A1
C1
D
2
C2
A2 F
X
W
G
I
J
V
K
H
L
M
N
O
P
Q
R
S
T
U
3 4 5 6 7BS1
E
B
2n = 15
apomict
BS 1
Het
Del
2n = 15
Ascending dysploidy by centric fission fixed due to apomixis
A1
C1
D
BS1
A1
C1
Het
centric
fission Del
D
pericentric
inversion
A1
C1
2n = 14
sexual
A1
C1
D
BS1
Del
D
A1
C1
Het
Mandáková et al. (2016) Plant J
Chromosome number variation
• Stasis
• Decrease (descending dysploidy)
• Increase (polyploidy and ascending dysploidy)
Descending Dysploidy via Terminal Chromosome Translocations
Roberstonian(-like)
translocations /
centric „fusions“
End-to-end
translocations / „fusions“
Robertsonian (unequal reciprocal)
translocation and meiotic seqregation
gametes
lost
2n = 8
2n = 8 or 7 or 6
chromosome
number
reduction
End-to-End Translocations in Plants Are Probably More
Common Than Previously Thought
Mandáková et al. (2016) Am J Bot Wang and Bennetzen (2012) PNAS
Chromosome „fusion“ – the origin of the human (dicentric) chromosome 2
Chiatante et al. (2017), MBE
Two optionss how the „fusion“ chromosome 2 was stabilized
• the ancestral centromere (AC) was either epigenetically inactivated or centromeredetermining
sequences were excised
• the excision is more probable – what mechanism?
• recombination-based excision, most likely in one step (similar human clinical cases...)
Ancestral Crucifer Karyotype (ACK)
(24 ancestral genomic blocks)
n = 4 – 8?
n = 8
 - WGD
diploidization
WGD = whole-genome duplication (polyploidization)
Crucifers (Brassicaceae): the origin of
the common ancestral genome
27
Arabidopsis thaliana - extensive chromosome reshuffling
linked with chromosome number reduction from n=8 to n=5
Lysak et al. 2006, PNAS; Hu et al. 2011, Nat Genet
Ancestral
Karyotype
Ancestral Crucifer Karyotype (n=8)
Ancestral
Karyotype
Lysak et al. (2006) PNAS
Reductions of Chromosome Numbers Were Independent and
Used Different Chromosome Breakpoints
Descending Dysploidy in Grasses is Mediated by
Nested Chromosome Insertions (NCIs)
Wang et al. (2014) New Phytol
Nested Chromosome Insertions Repeatedly Mediated
Descending Dysploidy in Grasses
Wang et al. (2014) New Phytol
n = 12
n = 7
n = 9
n = 10
n = 12
n = 5
n = 10
AK5/8/6
Fonsêca, Ferraz and PedrosaHarand
(2016) Chromosoma
Mandáková, Heenan and
Lysak (2010) BMC Evol Biol
Lysak et al. (2006) PNAS
Mandáková et al. (2013) Plant Cell
Did Nested Chromosome Insertions Occur Only in Grasses ?
Phaseolus
22  20
Hornungia alpina
8  6
Cardamine pratensis
32  30
Hou et al. (2016) GBE
Populus / Salix
19  19
Pachycladon exilis
15 (16)  10
Chromosome number change due to aneuploidy
the diploid apple tree - Malus (Considine et al.)
• all tetraploid seedlings were derived from 2n ova fertilized with 2n spermatozoa
• all triploids from 2n ova fertilized with n spermatozoa
• all aneuploids from n ova fertilized with aneuploid spermatozoa
Thus ova only contributed euploidy while spermatozoa contributed a range of
cytotypes, including aneuploidy, to non-diploid seedlings in the diploid Malus.
Odd basic chromosome numbers in Rosaceae (x=7, 8 and 7;
x=17 in the tribe Pyreae)
the Pyreae have long been considered an example of
allopolyploidization between species related to extant Spiraeoideae
(x = 9) and Amygdaleoideae (x = 8) taxa
Considine MJ et al. (2012) Molecular Genetic Features of Polyploidization and Aneuploidization Reveal Unique Patterns
for Genome Duplication in Diploid Malus. PLoS ONE 7(1): e29449.
Schematic Summary of the Features of Gametic Combinations for
Apple Polyploidization in Diploid Malus
Three-step scenario to the odd basic chromosome number in Malus:
(aneuploidization - eupolyploidization - dip​loidization)
 aneuploidization of two sister taxa (x = 9, 2n = 18) to 2n = 17 (x = 9)
 whole-genome duplication in both ova and spermatozoa  tetraploids (x = 9,
4n = 34)
 diploidization  the extant diploid state (x = 17, 2n = 34) (diploid-like meiosis)
Odd basic chromosome numbers in the Pyreae (x=17)
Aneuploidization can result in speciation with both odd and even basic
chromosome numbers, while eupolyploidization can ONLY contribute to even
basic chromosome numbers.
Chromosome number evolution in phylogenetic contexts
Descending dysploidy in Hypochaeris (Asteraceae)
n=4
n=6
n=3
n=5
n=4, 5
Descending dysploidy in Podolepis (Asteraceae)
• the extraordinary series of chromosome numbers, n = 12, 11, 10, 9, 8, 7
and 3 (dysploidy)
• chromosome number of n = 10 is the most common in the genus, and
thus, x = 10 was regarded as the ancestral chromosome base number for
the genus
Descending dysploidy in Podolepis (Asteraceae)
Podolepis
• the haploid chromosome number of n = 12 is the most common in the related
genera (Chrysocephalum, Waitzia, Leptorhynchos, Pterochaeta)
• according to the phylogenetic analysis, the ancestral chromosome base
number in the genus Podolepis may be x = 12
• chromosome number reduction has occurred in three
lineages:
‐ from n = 12 to n = 10 and 9 in the subclade A
‐ from n = 12 to n = 8 and 7 in the subclade B1
‐ from n = 12 to n = 11 and 3 in the subclade B2
• the low chromosome numbers of n = 8, 7 and 3 were
found only in annual species which were distributed in
semi-arid regions
• comparing the karyotypes between the taxa with n =
12 (in Waitzia and Chrysocephalum) and n = 10 (perennial
Podolepis), the increase in the number of large
chromosomes accompanies the decrease in the
number of medium-sized chromosomes in Podolepis 
the reduction in chromosome number has been
achieved by the unequal reciprocal translocations,
followed by the loss of the short translocation product
Chromosome number pattern congruent with phylogenetic
relationships: Ranunculaceae
• the Thalictrum group (T-chromosome group)
has short and small chromosomes with a basic
number of 7 or 9
• Langlet (1927, 1932) recognized two subfamilies of Ranunculaceae (Ranunculoideae and Thalictroideae)
on the basis of cytological characters, including chromosome size and basic number
• Ro et al. (1997): chromosome type and base
number are congruent with the inferred molecular
(rDNA) phylogeny
• fruit type (often used for the higher classification)
was not congruent with karyological data and
phylogenetic patterns
• the Ranunculus group of genera (R-chromosome group) has large and long chromosomes with a basic
number of 8
• c. 67 spp.
• chromosome numbers n = 6, 7, 8, 9, and 10
• molecular phylogenetic study carried out to test the
monophyly of the three sections and 12 subsections
erected by Ownbey (1940) based on morphology and
chromosome number
Descending and ascending (?)
dysploidy in Calochortus (Liliaceae)
• the ancestral chromosome number of Calochortus is x = 9
• descending aneuploidy (9  8, 7, 6)
• ascending aneuploidy (9  10) BUT is this true or the
phylogeny is wrong?
Descending and ascending (?)
dysploidy in Calochortus (Liliaceae)
Patterson and Givnish (2003)
end
Crucifers (Brassicaceae): evolution of
an ancestral genome
eight but rearranged
Evolution of the Ancestral Crucifer Genome – DIPLOIDS
unchanged
descending dysploidy
n = 8  n = 7, 6 & 5
Cardamine hirsuta
(n = 8)
Boechera stricta
(n = 7)
A1
C1
D
BS2
C2
A2 F
X
W
G
I
J
V
K
H
L
M
N
O
P
Q
R
S
T
U
BS3 BS4 BS5 BS6 BS7BS1
E
B
Capsella rubella
(n = 8)
46
Lysak et al. 2006, PNAS; Schranz, Lysak & Mitchell-Olds 2006, TiPS
Ancestral Crucifer Karyotype (ACK)
(24 ancestral genomic blocks)
Different fates of the Ancestral Crucifer Karyotype
in „diploids“ and polyploids
n = 4
n = 8
 - WGD
WGD
WGD

WGD = whole-genome duplication (polyploidization)
47
Ancestral Crucifer Karyotype remained
conserved in some taxa of Lineage I
Slotte et al. 2013, Nat Genet
Capsella rubella
(n = 8)
Capsella rubella vs. Arabidopsis lyrata
(both have ACK-like genome)
48
Diversification without large-scale chromosome
rearrangements: karyotype stasis in the Cardamineae
ACK
(n = 8)
ancestral karyotype of
Cardamineae (n = 8)
Cardamineae:
12 genera (337 spp.) worldwide
Mandáková and Lysak, in prep.
49
Descending dysploidy and genome stasis across Lineage II
Mandáková and Lysak 2008, Plant Cell; Cheng et al. 2013, Plant Cell
ACK (n = 8)
Ancestral Crucifer
Karyotype
t(AK2, AK5/6/8)
tPCK (n = 7)PCK (n = 7)
Proto-Calepineae Karyotype
n = 8
n = 7
Soltis et al. 2005
Reconstructing the ancestral base number for angiosperms
• the reconstructed ancestral base
chromosome number is x=6
• x=6 is a theoretical reconstructed
base number, it can be said that the
ancestral number was low - between
x=6 nad 9
x=6
Salse 2012
Reconstructing the ancestral chromosome number and paleogenomes
Reconstructing the ancestral chromosome number and paleogenomes
Salse 2012
whole-genome duplication
Reconstructing the ancestral chromosome number and paleogenomes
whole-genome duplication
Reconstructed genome evolution in grasses
CF = „chromosome fusion“
= whole-genome duplication (polyploidy)
Murat et al. (2014) GBE
Descending and ascending aneuploidy in Sideritis
(Lamiaceae)
• bimodal pattern of chromosomal
change
• Clade 1 shows decreasing aneuploid
series, with 2n=44 being the ancestral
number
• Clade 2 (with some ambiguity): 2n=36
is the ancestral number and ascending
aneuploidy has occurred