Plant Genome Organisation

The Plant Journal (2011) 66, 18–33 doi: 10.1111/j.1365-313X.2011.04544.
THE PLANT GENOME: AN EVOLUTIONARY VIEW ON STRUCTURE AND FUNCTION
Organisation of the plant genome in chromosomes

J. S. (Pat) Heslop-Harrison* and Trude Schwarzacher*
Department of Biology, University of Leicester, Leicester LE1 7RH, UK
Received 31 January 2011; revised 11 February 2011; accepted 15 February 2011.

*
For correspondence (fax +44 116 252 3330; e-mail phh4@le.ac.uk or ts32@le.ac.uk).
SUMMARY
The plant genome is organized into chromosomes that provide the structure for the genetic linkage groups and
allow faithful replication, transcription and transmission of the hereditary information. Genome sizes in plants
are remarkably diverse, with a 2350-fold range from 63 to 149 000 Mb, divided into n = 2 to n = approximately
600 chromosomes. Despite this huge range, structural features of chromosomes like centromeres, telomeres
and chromatin packaging are well-conserved. The smallest genomes consist of mostly coding and regulatory
DNA sequences present in low copy, along with highly repeated rDNA (rRNA genes and intergenic spacers),
centromeric and telomeric repetitive DNA and some transposable elements. The larger genomes have similar
numbers of genes, with abundant tandemly repeated sequence motifs, and transposable elements alone
represent more than half the DNA present. Chromosomes evolve by fission, fusion, duplication and insertion
events, allowing evolution of chromosome size and chromosome number. A combination of sequence
analysis, genetic mapping and molecular cytogenetic methods with comparative analysis, all only becoming
widely available in the 21st century, is elucidating the exact nature of the chromosome evolution events at all
timescales, from the base of the plant kingdom, to intraspecific or hybridization events associated with recent
plant breeding. As well as being of fundamental interest, understanding and exploiting evolutionary
mechanisms in plant genomes is likely to be a key to crop development for food production.
Keywords: genome, nucleus, chromosomes, cytogenetics, genome size, evolution, polyploidy, centromeres,
plant breeding, heterochromatin.
THE ORGANIZATION OF THE PLANT GENOME The Arabidopsis genome sequencing initiative was estab-
lished partially on the basis that the genes and gene
Plant nuclear genomes
sequences found in Arabidopsis would be substantially
The plant nuclear genome, consisting of the DNA and similar to those in all other plants (Meyerowitz, 1989;
associated proteins, is organized into discrete chromo- Somerville, 1989). Rice, because of its nutritional importance
somes. Each unreplicated chromosome and metaphase as a crop, was the next target for genomic sequencing
chromatid consists of a single DNA molecule that is linear following an initiative to identify all genes by sequencing.
and unbroken from one end to the other (Figure 1). At The similarity of gene sequences across all plants has been
metaphase of mitosis, the DNA is condensed into mitotic found to be true, although an initial surprise was the low
chromosomes – short, rod like bodies – while at interphase, total number of genes (27 206 protein-coding genes
the chromosomes are decondensed within the interphase in Arabidopsis, The Arabidopsis Information Resource
nucleus (Figure 2). The study of the chromosome and its website, http://www.arabidopsis.org/portals/genAnnotation/
organization involves cytogenetics, and the field of molec- genome_snapshot.jsp, and rice with 37 544 genes; Interna-
ular cytogenetics has developed to understand DNA tional Rice Genome Sequencing Project, 2005), only half the
sequence and the molecular structure of the chromosome number estimated before gene sequences were analysed
and chromatin. Both the size of the plant genome and the directly (Heslop-Harrison, 1991). Arabidopsis and rice were
number of chromosomes vary widely between species. also selected for genome sequencing in part because of their
In this article we will discuss the nature and consequences of small genome size. Chromosome biologists have tended
these differences in an evolutionary context. to choose species with large chromosomes as their ‘model’
18 ª 2011 The Authors

The Plant Journal ª 2011 Blackwell Publishing Ltd
Organisation of the plant genome in chromosomes 19
Short arm Long arm
Chromatid
Chromatid
Telomere NOR Centromere Telomere

secondary primary
constriction constriction
Chromosome regions: Pericentric Intercalary Subtelomeric

(pericentromeric) interstitial terminal
paracentric
(paracentromeric)
Figure 1. The organization and features of a plant chromosome. Figure 2. Chromosomes at all stages of the cell cycle.
Top: A fluorescent light micrograph of a metaphase chromosome stained A spread of a root tip of a hybrid plant of Hordeum · Secale showing nuclei at
blue with the DNA-binding fluorochrome 4¢,6-diamidino-2-phenylindole all stages of the cell cycle (labelled). The condensation of chromosomes to
(DAPI). In situ hybridization shows the location of two tandemly repeated metaphase and decondensation at telophase is evident, and one or several
DNA sequences detected by red and green fluorescence. nucleoli are seen within the interphase nuclei. This hybrid line is unstable and
Centre: A diagram of the structure of a metaphase chromosome with two chromosomes are sometimes lost during division, forming micronuclei
chromatids. (arrows). Bar 10 lm.
Centromeres or primary constrictions are seen as gaps in cytological
chromosome preparations (see Figure 3b,d). They nucleate the proteinaceous
kinetochore plate to which the spindle microtubules attach and are charac-
terised by specific centromeric histones. DNA sequences at the centromeres amigo.geneontology.org). It defines ‘chromosome organi-
are not conserved between species (see text). zation’ as ‘a process that is carried out at the cellular level
The centromere and the regions surrounding it, called paracentromeric
that results in the assembly, arrangement of constituent
regions, contain large arrays of tandem repeats and are often enriched in
transposable elements. parts, or disassembly of chromosomes, structures com-
Euchromatin. Lightly stained in cytological preparations (Figure 3a); posed of a very long molecule of DNA and associated
generally gene rich, showing high transcriptional activity and higher levels
proteins that carries hereditary information’. Many of these
of recombination at meiosis. Transposable elements may be dispersed widely
through euchromatin. genes are related to chromatin (see Fransz and deJong,
Heterochromatin. Strongly stained in cytological preparations (Fig- 2011), or meiosis and recombination, rather than the struc-
ure 3a); rich in highly repeated tandemly organised DNA sequence families
tural and evolutionary aspects of chromosome organization
and sometimes transposable elements. Heterochromatin generally lacks
meiotic recombination and is relatively deficient in genes, and those present that are discussed here.
often have decreased transcriptional activity.
NOR. Nucleolus organising regions contain the long arrays of 45S rDNA Non-nuclear genomes and DNA sequences
repeat units, including the 18S–5.8S–26S rRNA genes and intergenic spacers.
Most genomes have several major and minor rDNA loci (Figure 4c,d). Along with the nuclear genome, genes are also carried in the
Expression of the rRNA genes generates the nucleolus at interphase organelles (chloroplasts or plastids, and mitochondria) and
(Figure 4b); at metaphase, NORs are often visible as secondary constrictions
the genomes of viruses, mycoplasmas, bacteria and fungi
as the arrays of genes active at the previous interphase remain decondensed.
Subtelomeric or telomere associated sequences (TAS) are long tandem may be present within or in close association with plant
repeats (Figure 3b) sometimes containing degenerate (TTTAGGG)n motifs, nuclei or cells. These genomes interact and impact on the
and are species specific and often chromosome specific.
organization and evolution of the associated plant nuclear
Telomeres, at the ends of chromosomes, are relatively short arrays usually of
the conserved simple repeat (TTTAGGG)n (Figure 4c). They maintain chro- genome. Furthermore, the possible presence and effects of
mosome integrity by stabilizing chromosome termini. non-nuclear genomes (which may be transmitted to the next
generation) must be considered in genomic and evolution-
ary studies. Increasing amounts of data obtained after the
species such as Secale, Triticum (Figures 3 and 4), Lilium or first plant genome sequences were completed have shown
Vicia faba. that transfer of genes into the plant nuclear genome, while
Chromosome organization is related to genome function not frequent, is a regular and evolutionarily important
within the cell nucleus (Spector, 2003), with physical orga- occurrence.
nization relating to regulation and gene expression, cell Transfer of genes from both mitochondria (see Goremy-
division, recombination and replication. There are genes kin et al., 2009) and chloroplasts or other plastids (see Cullis
involved in aspects of chromosome organization. The Gene et al., 2009) to the nucleus over evolutionary time has led to
Ontology (GO) project aims to generate descriptions of the loss of many genes from organelles (see Green, 2011).
gene products in their database consisting of a controlled There is also evidence for transfer of genes from mitochon-
vocabulary of terms covering biological concepts (http:// dria to chloroplast (grape: Goremykin et al., 2009). These
ª 2011 The Authors
The Plant Journal ª 2011 Blackwell Publishing Ltd, The Plant Journal, (2011), 66, 18–33
20 J. S. (Pat) Heslop-Harrison and Trude Schwarzacher
(a) (b)
(c) (d)
Figure 3. Metaphase chromosomes with centromeres and heterochromatin composed of tandemly repeated sequences.
(a, c) Metaphase and interphase chromosomes of rye, Secale cereale, 2n = 2x = 14 after fluorescent banding with 4¢,6-diamidino-2-phenylindole (DAPI) (a); and
fluorescence in situ hybridization (FISH) (c); with simple sequence repeats (red) and tandemly repeated satellite DNA sequences (green; Cuadrado and
Schwarzacher, 1998). Many homologous chromosomes show differences of signal strength indicating polymorphic repeat copy numbers in this heteromorphic
and outbreeding species. At interphase the subtelomeric heterochromatin consisting of tandemly repeated satellite DNA (Alkhimova et al., 2004) is strongly stained
with DAPI (a); and green FISH signals (c); are on opposite ends to the centromeres identified by the red FISH signals. (b) Chromosomes of Rumex acetosa
2n = 12 + XY1Y2. After FISH with the simple sequence repeat (AAC)5. The sequence is amplified on the two Y chromosomes. (d) Feulgen stained chromosomes of
Cephalanthera longifolium (2n = 36). Both large and small chromosomes show clear primary constrictions at the centromere. Bar = 10 lm in (a) and (c); 15 lm in (b)
and (d).
authors, and Bock and Timmis (2008), review the continuing Cavemoviruses and in some cases reach several thousand
nature of transfer of genes into the nucleus, with the integrants. Host genome invasion by pararetroviruses has
increased regulatory ability, and the variation in genes that occurred several times during the evolution of Solanaceae
have been transferred in different evolutionary groups of (Staginnus and Richert-Pöggeler, 2006) and repeatedly in
plants. These gene transfers have led to many incongruent banana (Gayral and Iskra-Caruana, 2009). Non-functional
evolutionary trees from analysis of nuclear copies of orga- sequences as well as complete and inducible integrants
nellar genes, where short PCR products have not distin- have been isolated indicating that integrated seq-
guished the origin of the gene. Large insert (e.g. BAC) uences decay and can be highly degenerated; they tend
sequences can identify DNA sequences flanking the orga- to be concentrated in pericentromeric heterochromatin
nelle-origin genes, or in situ hybridization can show their associated with retrotransposable elements (Metaviridae
location on chromosomes rather than in organelles (e.g. sequences; Gregor et al., 2004; Hansen et al., 2005;
Vaughan et al., 1999). Staginnus et al., 2007), and may play a role in host defence
Viral genomes, particularly from the pararetroviruses with against virus infection through RNAi silencing (Staginnus
a DNA genome, can transfer from the episomal virus into the and Richert-Pöggeler, 2006).
nucleus, and can be expressed as infective virus particles In the 1970s, Agrobacterium species were shown to be
that cause disease. The banana streak virus was the first able to transfer genes for hormone and opine synthesis
example to be characterized (Gayral and Iskra-Caruana, into the plant nuclear genome, and Schell and van Montagu
2009; Harper et al., 1998), and petunia and tobacco vein showed how this property could be used in plant transfor-
clearing virus was identified soon after (Lockhart et al., 2000; mation (see, for example, Zambryski et al., 1983). Subse-
Richert-Pöggeler et al., 2003). Solanaceous species are quently, technology to transfer genes from outside the
particularly rich in endogenous pararetroviruses (EPRVs; nucleus into the genome of the host plant has been
Hansen et al., 2005), where the majority show homology to developed using the Agrobacterium or other approaches.
ª 2011 The Authors

(a) (b)
(c) (d)
Figure 4. Large and small chromosomes share features of rDNA loci, centromeres and telomeres.
(a) 4¢,6-diamidino-2-phenylindole (DAPI)-stained metaphase and interphase chromosomes of Arabidopsis thaliana; enlarged inset after fluorescence in situ
hybridization (FISH) with the abundant centromeric 180-bp repeat (red). (b) Interphase of Medicago truncatula after FISH with 45S rDNA probe (red). Unexpressed
condensed sites of the rDNA are visible at the periphery of the nucleolus while decondensed, expressed strands run though the lighter volume of the nucleolus with
less DAPI-stained DNA (micrograph from Matheus Mondin). (c) A wheat/rye recombinant line carrying a 1DL.1RS translocation as identified by genomic rye DNA
(red) and the presence of major 45S rDNA sites (green) on the short arms of chromosome 1R, 1B and 6B and minor sites on 5D and 1A. (d) Oil palm, Elaeis guineensis
(2n = 32) metaphase chromosomes after FISH with the telomeric sequence (TTTAGGG)6 (green) located in variable copy numbers at the end of each chromatid, and
the 45S rDNA on one chromosome pair (red). Part of an interphase is visible lower right hand side (Castilho et al., 2000). Bar = 10 lm.
Molecular cytogenetic analysis including fluorescent in-situ chromosome centromeres and telomeres (see below; Fig-
hybridization is very appropriate to locate the transgene ures 1 and 4a,c), and the rDNA (rRNA genes and intergenic
in the genome), and even to determine copy numbers spacers) at the 45S and 5S loci (Figures 1 and 4b–d). Tan-
(Fransz et al., 1996; Leggett et al., 2000; Pedersen et al., demly repeated or satellite DNA consists of a motif (as short
1997; Salvo-Garrido et al., 2001; Schwarzacher, 2008; as two bases, a microsatellite or simple sequence repeat, but
Svitashev and Somers, 2002; Wolters et al., 1998). Consi- sometimes 10 000 bp long) that is repeated in many copies
derable efforts are required for analysis of low or single copy at one or more genomic locations (Figure 3b,c). Satellite
sequences, but these are justified as verification of nuclear DNA in plants typically consists of motifs of about 180 bp
integration may be difficult by Southern hybridization or (Kubis et al., 1998; Contento et al., 2005), and can be seen
PCR, particularly in slow-growing, sterile or non-intercros- either as deep-staining heterochromatin that does not
sable hybrids or polyploids where transmission and segre- decondense during interphase (blue condensed chromatin
gation analysis is impractical. Chromosomal analysis of in Figures 3a and 4b) or by in situ hybridization of the
transgenic lines can also establish whether the plants have sequence after labelling (Figure 3b,c); these satellite
maintained their chromosomal integrity or whether aneu- sequences are abundant but their function in the genome is
ploidy, polyploidy or rearrangements have occurred. not known. Transposable elements are the third class of
repetitive DNA sequences; both class I (retrotransposons)
Composition of nuclear DNA
and class II (DNA transposons) elements may amplify and
The nuclear DNA of plants consists of the single- or low-copy the elements and recognizable degraded remnants may
coding sequences, introns, promoters and regulatory DNA represent half or more of the entire DNA present in the
sequences, but also of various classes of repetitive DNA genome (Kubis et al., 1998; Pearce et al., 1997). Both classes
motifs that are present in hundreds or even thousands of of transposable elements include sequences that encode
copies in the genome (Heslop-Harrison and Schmidt, 1998). enzymes related to their own replication and integration into
Repetitive DNA motifs include characteristic sequences at the nuclear DNA.
ª 2011 The Authors

tae (2n = approximately 40), to the largest of Paris japonica

Genome size or nuclear DNA content
(2n = 8x = 40) at 149 000 Mb, a 2350-fold range among
Each plant species has a characteristic number of base pairs measurements of 6288 species. For a diploid rather than
in its nuclei, known as its genome size or nuclear DNA polyploid species, Fritillaria platyptera (2n = 2x = 24) has the
content. Work from Swift (1950) onwards has shown that highest value at 84 150 Mb. Species with the smallest
the nuclear DNA content is largely constant within a species. genomes of <200 Mb belong to one monocot and 13 diverse
Measuring and cataloguing the size of genomes, number eudicot families. Many species with very large genomes are
of chromosomes and range of chromosome sizes and in the order Liliales (Liliaceae, Melanthiaceae and Alstro-
morphology (karyotypes) has been carried out over many emeriaceae), with only nine eudicot families having species
decades. Karyotype data have proven useful for evolution- with genomes over 15 000 Mb. The average angiosperm
ary and phylogenetic studies at taxonomic levels between genome size is 5800 Mb, with the major groups (Angiosperm
the species and family. In contrast to DNA sequence data, Phylogeny Group III, 2009) of basal angiosperms (average
karyotype data often do not allow inference of higher levels 2300 Mb) and eudicots (2800 Mb) being smaller than the
of relationships. Indeed, the significance, any selective monocots (10 200 Mb, reduced to 8500 Mb if the order
constraints, or other ‘reasons’ for differences in genome Liliales is excluded). Interestingly, gymnosperm genomes
organization above the family level between species groups are larger with an average genome size of 18 200 Mb, and a
remain unknown. range from 2200 to 35 200 Mb. Figure 5 illustrates this wide
Genome sizes are now normally estimated by using flow range of nuclear DNA contents in angiosperms.
cytometry, replacing earlier methods of measuring absor- Among eukaryotic genomes which have been sequenced,
bance of stained nuclei (microdensitometry). Nuclear gen- the average length of the coding sequences (excluding
ome size has been widely measured and cited in pg introns) has been reported as 1346 bp (with little variation
(picograms) of DNA, but in the context of molecular biology between groups; Xu et al., 2006), while the number of genes
is now most frequently given in number of base pairs for the in diploid higher plants has been found to be about 30 000
1C DNA content. A nucleus immediately after meiosis but (see Ming et al., 2008), accounting for a total of 40 Mb of
before DNA replication will have the 1C DNA content, while a
replicated nucleus entering mitosis in the vegetative part of
an angiosperm would have four times this amount, the 4C (a)
DNA content. Bennett and Leitch (2011) have assembled the
diverse measurements of plant genome sizes into online
databases (http://data.kew.org/cvalues/cvalOrigReference.
html); the algae (see Bowler and Tirichine, 2011), pterido-
phyte and bryophyte data are not considered here. The
databases of plant and animal genome sizes have been
discussed in a broader context by Gregory et al. (2006; http://
www.genomesize.com).
(b)
Published measurements of genome sizes and chromo-
some numbers often need critical assessment as they can be
made for purposes where rigorous checking and replication
is not required, may be field-based, carried out on a large
scale, use techniques which are unproven or of limited
reliability, or have technical errors (Greilhuber, 2005; Suda
and Leitch, 2009). Hence individual reports should be
compared with measurements from multiple sources or
observation. Reports of extreme values are particularly
prone to error. Casual examination of stained chromosome
preparations by light microscopy – preferably of metaphase
spreads, but even of stained interphase nuclei – will avoid
mistakes in measurement of genome size by four-fold or
Figure 5. Frequency distribution histograms showing the nuclear DNA con-
more, and ensure that diploids are separated from polyp-
tent of angiosperms.
loids with 50% (3·) or more (4· and above) chromosomes. (a) Genome sizes up to 10 000 Mb in 250 Mb bins. (b) Genome sizes up to
Bennett and Leitch (2011) report angiosperm genome 150 000 Mb in 3750 Mb bins. Vertical axis: frequency; Horizontal axis:
alternate bin boundaries in Mb. red: monocots; green: eudicots; blue: basal
sizes as varying from the smallest reported higher plant
angiosperms; light: truncated columns. Data from http://data.kew.org/cva-
genome size of 63 Mb in two species of the carnivorous lues/cvalOrigReference.html, downloaded 1/2011 (see Bennett and Leitch,
Genlisea, G. aurea (2n = approximately 52) and G. margare- 2011; Leitch et al., 2010).
ª 2011 The Authors

DNA. With the requirement for structural regions of chro- and examples of both increases and decreases during evo-
mosomes (centromeres and telomeres), rRNA, regulatory lution and speciation are frequent. Within the eudicots, the
sequences and introns, this suggests 60 Mb is close to the lowest and highest chromosome numbers, 2n = 4 and
minimum genome size. Lysak et al. (2009) studied genome 2n = around 640 have both been reported in the single
size evolution in the Brassicaceae (showing a 16-fold range genus Sedum (Crassulaceae; in a flora by ‘t Hart and Bleij,
in 185 taxa studied) in the context of the phylogenetic 2003; source and reliability unknown), although few species
relationships within the family. They concluded that half have more than 200 chromosomes. Several other eudicots
the species had a decreased genome size compared with and monocots have 2n = 4, while 2n = circa 596 has been
the common ancestor, despite the occurrence of dynamic reported in the monocot palm Voanioala gerardii and
genomic processes (transposition of transposable elements 2n = around 1200 in the fern Ophioglossum reticulatum. In
and polyploidization) that can increase genome size; the genetic mapping and DNA sequencing projects, chromo-
mechanisms to eliminate amplified DNA remain to be some number is critical to know as it defines the number of
elucidated. Knowledge of genome size is important for independent linkage groups.
choice of strategies for genomic projects including library There are a few exceptions to the constancy of chromo-
construction, cloning, and genome sequencing. In general some number within a species where species include
terms the collection of this data has not revealed general several cytotypes, like members with different ploidy levels.
principles related to consequences of variation in genome For example, individuals of Hordeum murinum may be
size, nor suggested constraints, nor the mechanisms or diploid (2n = 2x = 14) or tetraploid (2n = 4x = 28) plants
selection pressures that modulate genome size over evolu- (Taketa et al., 1999); there are even a few tetraploid
tionary time. populations of Arabidopsis thaliana (2n = 4x = 20; Heslop-
Greilhuber (2005) remarked that the occurrence and Harrison and Maluszynska, 1994; Steinitz-Sears, 1963).
extent of genome size variation below the species level is Another source of variation in chromosome number (and
controversial, pointing out faults in a number of studies genome size) is the presence of supernumerary or B
reporting differences. Nevertheless, unless speciation is chromosomes (review: Jones et al., 2008) in addition to
driven by genome size changes, differences between spe- the normal chromosome complement. These usually small
cies show that intraspecific differences in DNA content are chromosomes are derived from the standard chromosomes
present and have consequences for chromosome behaviour in the complement, and apparently lack genes although
including meiotic pairing. Chromosomal polymorphisms there is a ‘drive’ process which ensures their survival and
caused by differences in repetitive DNA sequences can occur indeed amplification in number within some plants despite
rapidly. In maize, there are differences in the sizes of having detectable and often negative effects on the
terminal heterochromatic knobs, consisting of repetitive phenotype.
DNA sequences (Aguiar-Perecin and de Vosa, 1985; In contrast to the wide chromosome number range
Laurie and Bennett, 1985). The extensive variation in seen among the angiosperms, gymnosperms (character-
heterochromatin contents in rye – seen as chromosome ized by large genomes; Murray et al., 2002) have no
polymorphisms even within the two homologues (see species with extreme chromosome numbers (typically
Figure 1b) – also gives differences in nuclear DNA content 2n = 2x = 14–28), and there are very few polyploid species
(Alkhimova et al., 2004). Under some conditions, repetitive in the group. Chromosome number can be stable across
sequences at the terminal regions of chromosomes are lost families: of the 232 species in 11 genera in the Pinaceae,
during mitotic divisions. Özkan et al. (2010) have shown all those studied have 2n = 2x = 24 chromosomes except
limited variation in genome size in wheat, with substantial for Douglas fir (Pseudotsuga menziesii, 2n = 26; Krutovsky
interspecific variation, due to the activity of retroelements. et al., 2004). The 400–500 species of grasses (Poaceae) in
Copy number variations (CNV) have been demonstrated to the subtribe Triticeae, including barley, rye, wheat and a
arise in the rRNA arrays of flax given different treatments by number of forage grasses (Barkworth, 2010), all have a
Cullis (2005). CNVs involving chromosome segments more basic chromosome number of x = 7 (Figure 3a,c),
than 1 kb in size with insertions, deletions and duplications, although many are polyploids (Figure 4d; see below). In
have been found across all chromosome arms in maize (Beló contrast, the Brassica genus has a wide range in chro-
et al., 2010). Such polymorphisms in the genome, in plants mosome number, and the changes, discussed below, may
like animals, are likely to have important consequences for be driving speciation.
populations and their adaptation (Biemont, 2008), disease
Chromosome size
response and heterosis (Beló et al., 2010).
Average chromosome size for a species is derived from
Chromosome number
chromosome number and genome size. Based on Bennett
Every species has a characteristic number of chromosomes and Leitch (2011), taking unreplicated haploid genome sizes
in the nucleus. Numbers vary extensively between species, (1C) for angiosperms and dividing by haploid number (n) of
ª 2011 The Authors
chromosomes reveals that 18 of the 5163 species have may be accompanied by duplication and inversions of
chromosomal DNA molecules (as would, for example, be chromosome arms. As an example, the chromosomes of
analysed by pulse field gel electrophoresis, PFGE) <10 Mb in the native European orchid Cephalanthera (see Figure 3d)
average size, while 118 species have an average size of more with species having 2n = 32, 36 or 44, are thought to have
than 3000 Mb. The double-stranded DNA molecule in each evolved by palaeotetraploidy from x = 9 followed by cen-
chromatid of a metaphase chromosome of Genlisea aurea, tric (Robertsonian) fusions leaving interstitial telomeres
averaging 2.4 Mb, is only half the size of the 4.6 Mb genome (Moscone et al., 2007).
of the bacteria Escherichia coli. In species with small With genomic data involving both genetic mapping and
chromosomes, stained bacteria (where the genome may genome sequencing, it is now possible to identify the large
be replicated several times) can be confused with scale chromosomal rearrangements that have occurred
chromosomes in microscope preparations. Figure 4 shows during evolution. Chromosome numbers in the Brassicaceae
A. thaliana chromosomes averaging 30 Mb in size together vary from 2n = 8 to 2n = 256 (Lysak et al., 2005). A. thaliana,
with wheat chromosomes averaging 800 Mb and oil palm with 2n = 10 (Figure 4a), has one of the smallest chromo-
(Elaeis guineensis) chromosomes of 114 Mb. some numbers, an advanced character representing reduc-
Despite the stability of chromosome number in the tion from its ancestors in the clade including A. lyrata and
Pinaceae (2n = 24), genome size varies over a three-fold Capsella rubella (both 2n = 16). An impressive use of com-
range up to 35 000 Mb, and in the Triticeae, the haploid, x, parative chromosome painting to meiotic pachytene chro-
genome size varies from about 3300 to more than 8000 Mb. mosomes using groups of BAC probes to identify each
Like genome size and chromosome number, these differ- chromosome segment allowed Lysak et al. (2006) to show
ences in average chromosome size, and the nature of the the origin of each chromosome in A. thaliana relative to
differences involving amplification or DNA and RNA trans- the ancestral n = 8 karyotype, involving four chromosomal
posable elements, tandemly repeated DNA sequences, inversions, two translocations and three chromosome fusion
and perhaps segmental duplications of the genome, can events. In Brassica, Mandakova and Lysak (2008) used
be described accurately from several complementary multiple selected BACs as probes to reveal the monophyletic
methods. Detailed sequence analysis (e.g. International origin of the x = 7 tribes, some of which included a translo-
Brachypodium Initiative, 2010) indicates that footprints of cation where chromosomal segments are exchanged
centromeric repeats and peaks in retroelement frequency between two chromosomes. The results also suggest that
are seen at the junctions of ancestral chromosome inser- structure of the ancestral karyotype of the Brassica, with
tions. Both single-generation chromosomal changes and a reduction in chromosome number from n = 8 to n = 7 has
long-term accumulation of repetitive DNA have evolutionary happened more than once, with different fusion and intra-
roles in reproductive isolation and restriction of gene flow chromosomal inversion events. Xiong and Pires (2011) have
between newly evolving species, with consequences for developed an in situ chromosome painting method to
understanding genome and gene evolution, as well as for identify all chromosomes in Brassica napus and its diploid
the population biology, acquisition, loss or modification of progenitors, showing a chromosomal translocation in one
gene function, and allele diversity. B. napus cultivar. They suggest that this approach will be
As chromosomes within a species can be of different useful to understand chromosome reorganization, genome
sizes, they can be sorted using flow-cytometry based on evolution and recombination; sequence analysis would
their fluorescence. In bread wheat, the first DNA library was not be appropriate for the detection of single translocation
made by Wang et al. (1992) from wheat chromosome 4A. breakpoints.
A flow sorted BAC library of chromosome 1B was made While some of the chromosome number changes occur
by Janda et al. (2006), and many other chromosomes have through doubling of chromosome numbers or polyploidy
been sorted and characterized (Dolezel et al., 2007; Paux (see below), many involve fusion or fission of chromo-
et al., 2006; Šafář et al., 2004). The International Wheat somes, as shown in the Brassicaceae, grasses and many
Genome Sequence Consortium (IWGSC – http://www. other families. Through sequence comparisons, multiple
wheatgenome.org) is using these flow sorted chromosomes orthologous gene sequences are found to show a conserved
to partition the wheat genome before chromosome-by- order (synteny) along chromosomes over large taxonomic
chromosome sequencing of the 17 000 Mb genome. distances. Data of this nature are accumulating rapidly, and
syntenic comparisons are now an essential part of most
CHROMOSOMAL AND KARYOTYPE EVOLUTION genome sequence papers. For example, Jaillon et al.
(2007) compared Vitis (grape vine) genomic regions to their
Chromosome evolution and structural variation
orthologues in Populus trichocarpa, A. thaliana and Oryza
Chromosomes evolve by fission and fusion (leading to a sativa, a taxonomic range where direct comparisons were
change in chromosome number, or to inversions of seg- hardly conceivable before sequence-based comparisons
ments within one chromosome; Jones, 1998), events that became possible. In Vitis, their analysis showed that the
ª 2011 The Authors
genome has been triplicated during its early evolution,

Aneuploidy – chromosome loss or gain
before the split of the poplar/Arabidopsis/Vitis lineages,
but after the monocot/eudicot split as it was not shared with Aberrant cell division is relatively frequent, and chromo-
rice. The analysis identified an additional duplication in the somes are lost or gained during mitosis or meiosis leading
poplar lineage, and two whole genome duplication events in to aneuploidy. Figure 2, an intergeneric hybrid, shows nuclei
the Arabidopsis lineage, as well as global duplications in at all phases of the cell cycle, but includes some cells with
the rice lineage. In the grass Brachypodium distachyon micronuclei (arrows) from mis-divisions. In many cases,
(2n = 10), sequencing of the 272 Mb genome (International these cells will not divide further, but the mis-division
Brachypodium Initiative, 2010) revealed a complex evolu- can occur in gametes or cells which regenerate to a
tionary history with six major interchromosomal whole organism. In mammals, most such aneuploids do not
duplications within the genome, the five Brachypodium develop. Many plant aneuploids grow to generate adult
chromosomes originating from a five-chromosome ances- plants, not least because plant genomes are often polyploid
tral genome through a 12-chromosome intermediate involv- (see below) and have higher plasticity and mechanisms for
ing seven major chromosome fusions. Sets of collinear gene dosage compensation. Chromosome addition lines,
genes along all ten Brachypodium chromosome arms can with an extra copy of a chromosome, occur naturally (first
be identified easily in the other grasses where detailed found in Datura by Blakeslee and Avery, 1919). They are also
genetic maps are available (rice, barley, wheat, sorghum, made by crossing tetraploid and diploid plants, or crossing
and Aegilops tauschii). Twelve separate syntenic blocks different species, followed by backcrossing to derive lines
of orthologous genes from Brachypodium are present in with one or a few extra chromosomes. These hybrids have
rice, sorghum and barley, with nested insertions of some proved valuable to transfer alien chromosomes from wild
Brachypodium ancestral groups into centromeres of the relatives to crop species; recombination between the alien
other species. In the Triticeae, a detailed analysis of syntenic and crop chromosome can then reduce the chromosome
regions by Luo et al. (2009) has shown how the basic number while still transferring the required characters.
number of x = 7 has been derived from x = 12 in the Particularly in wheat, such lines (Figure 4d) have a long
ancestral species (represented by rice and sorghum) not history of use in breeding programmes (see, e.g. Heslop-
through end-to-end chromosome fusions, or translocations Harrison et al., 1991; Schwarzacher et al., 1992; Bardsley
and loss of microchromosomes, but by the insertion of four et al., 1999), and a number of programmes are exploiting the
whole chromosomes into breaks in the centromeric region transfer of important disease resistance genes into wheat
of four other chromosomes, with a further fifth fusion and (Ayala-Navarrete et al., 2007; Sepsi et al., 2008; Graybosch
translocation event. et al., 2009; Molnár et al., 2011).
Analysis of the nature of the rearrangements using whole Monosomic plants are regularly found in species with
genome sequence comparisons is enabling the history of a recognizable polyploid ancestry and are missing one
genome evolution to be reconstructed with unprecedented (of a pair) of chromosomes. These have proved extremely
accuracy. For plant breeders, knowledge of the nature of valuable for genetic analysis, as the phenotype of the plant
the changes shows the types of changes which might be reflects modified expression of the genes carried by that
introduced in the future, and suggests strategies and monosomic chromosome; substantial amounts of genetic
candidate accessions for crossing programmes. Parallel analysis in wheat (Sharp et al., 1989) and in maize have
work across the mammals (Nagarajan et al., 2008) is also involved monosomic analysis (Helentjaris et al., 1986).
showing the evolutionary chromosome rearrangements Trisomic lines, with an additional single chromosome, are
across diverse species. Similar chromosomal fusion, fission also valuable for genetic analysis of diploid species to assign
and elimination events to those discussed in Brassica have linkage groups to chromosomes (rice: McCouch et al., 1988).
been reported in cattle and the Artiodactyla (Chaves et al.,
Polyploidy
2003). In mammals, in situ hybridization and chromosome
painting is widely used (Froenicke et al., 2006). Despite some Whole genome duplication or polyploidy has probably
successes (Mandakova and Lysak, 2008), this technique has played a major role in the evolution of all angiosperms by
been less used in plants, presumably because of the more enabling fertile interspecific hybrids to be generated with
rapid homogenization of DNA sequences from retrotrans- multiple gene alleles at each locus, through freeing dupli-
posons, so probes from large amounts of DNA become cated genes to mutate, and through reproductive isolation of
genome-specific rather than chromosome- or linkage-group new polyploids leading to speciation with limited gene flow
specific. Recent advances in large-insert (BAC or fosmid) (see, for example, Soltis and Burleigh, 2009; Proost et al.,
hybridization suggest it will be increasingly used to address 2011). Polyploidy can arise by multiplication of the genome
chromosome evolution (Lysak et al., 2006) and physical in one plant – autopolyploidy – or through hybridization of
linkage mapping of sequences (Anhalt et al., 2008; Han two species with doubling of the chromosomes of one or
et al., 2011). more of the species involved – allopolyploidy. Autopolyp-
ª 2011 The Authors

loids may be recognized as a different species from their tionary advantage over their diploid ancestors (Proost et al.,
diploid progenitor, or may be placed in the same taxon, 2011). It will be interesting to see if more recent events are
despite usually having some morphological differences found, or whether polyploidy is ultimately an evolutionary
including size and pollen morphology, and being repro- dead-end except following catastrophic climate change.
ductively isolated. Interestingly, the K–T adaptation through polyploidy seems
Cytological evidence for polyploidy includes the occur- to be restricted to the angiosperms. The pteridophytes
rence of a regular series of chromosome numbers within a include polyploids and many high chromosome numbers
species group (e.g., Cephalanthera; Moscone et al., 2007), that potentially represent higher ploidies, but the K–T
the behaviour of hybrids with chromosome pairing at mei- extinction event marked the extinction of the fern forests;
osis, and the existence of monosomic plants. In the 1990s, in contrast, the gymnosperms survived and remain a very
this evidence suggested that perhaps 30% of plants were successful group although they include few polyploids
polyploid, although some questioned whether species (except in the genus Ephedra). There are not enough
such as maize were polyploids or palaeopolyploids. How- sequence data from these large genomes to identify older
ever, with DNA sequence and genetic map data showing polyploids, although the similar and low chromosome
the presence of copies of multiple genes in the same order number in most gymnosperms provides weak evidence
on two or more chromosomes, evidence for whole against whole genome duplication.
genome duplications or polyploidy in the ancestry of
Chromosome changes and speciation
species becomes unequivocal (Tang et al., 2010). Schnable
et al. (2009) show that every chromosome arm in maize Occasional chromosomal mutations can become fixed in
carries blocks of genes duplicated in order on another a population, thus establishing reproductive barriers and
chromosome, and the results clearly show chromosomes leading to the emergence of new species. The diverged
involved in translocations. It is now obvious that ‘diploid’ species may later form hybrids, often in a limited geographic
Brassica species including B. oleracea and B. rapa are area, a hybrid or tension zone, where otherwise selectively
ancient hexaploids (Lagercrantz and Lydiate, 1996), with disadvantaged hybrids with reduced fitness survive in an
three different genomes. The analysis of sequence data in environment not optimal for either of the parental species
combination with physical and genetic mapping shows the (Hewitt, 1988). Analysing the gene flow and differential
complex nature of the collinear genome segments, trans- introgression of genomes in such hybrid zones allows
locations and inversions (Trick et al., 2009) and the ampli- identifying genomic regions involved in speciation (Payseur,
fication of repetitive elements after separation of the 2010). Furthermore, the seemingly random changes found
ancestral species (Alix et al., 2008). in chromosomal sets of individuals are often of a similar
Many of the polyploid events, recent and ancient, have nature to those found between species. They can be seen as
involved autopolyploidy or hybridization of species which the first step in speciation through chromosome evolution.
are evolutionarily close. For these plants to be fertile, meiotic
chromosome pairing must lead to regular formation of THE STRUCTURE OF THE CHROMOSOME
bivalents, rather than multivalents involving more than one
Chromosome packaging
homologous pair of chromosomes where recombination
and segregation would lead to unbalanced gametes. In The packaging of the double-stranded DNA helix into the
wheat, Riley and Chapman (1958) described the effect of nucleosomes is similar in all organisms (Richmond et al.,
a single locus, Pairing homoeologous (Ph), which ensures 1984); coiling into the next level of fibre is discussed by
strict bivalent formation, showing that homology search Fransz and deJong (2011). Neither the detailed nature nor
mechanisms are under genetic control. We can speculate the consequences of packaging of the DNA fibres into the
that the widespread and early occurrence of polyploidy in chromosome at higher levels are clear. Many biology text-
the angiosperm lineage is due to the group’s unique ability books include diagrams with a hierarchy of coiled-coils, but
to achieve strict bivalent pairing at meiosis, which could evidence for this is weak and inconsistent. There are tech-
be a consequence of very sensitive homology matching nical reasons why investigation has been difficult, including
(Schwarzacher, 1997). Evidence suggests mediation by the fact that the DNA is in a hydrated matrix with salts and
cyclin-dependent kinase-like genes (reviewed in Yousafzai proteins which is rapidly disturbed by fixation protocols,
et al., 2010). while the structures are too polymorphic to be understood
Recent work by Fawcett et al. (2009) and associated by crystallography. However, study of higher levels chro-
commentary by Soltis and Burleigh (2009) has dated whole matin packaging, its genetic control and the access by rep-
genome duplication events across 13 diverse angiosperm lication, transcription and condensation proteins will lead
families to the Cretaceous–Tertiary (K–T) boundary when to better understanding of normal and abnormal nuclear
60% of plant species went extinct; Fawcett et al. (2009) development and the genetic and epigenetic regulation
speculate that the new polyploids had a substantial evolu- processes.
ª 2011 The Authors

analysis has shown the presence of actively transcribed

Morphological features of chromosomes
genes (Jiang et al., 2003; Yan et al., 2006; Mutti et al., 2010).
In most species, chromosomes have three structural fea- However, despite the conservation of the function, the
tures that have been identified since the earliest microscopy kinetochore proteins and the CenH3 histone that forms part
work: the telomeres at the ends of each chromosome, the of the nucleosomes core at centromeres of metaphase
centromere or primary constriction and, on some chromo- chromosomes, the DNA sequences at the centromere in
somes, a secondary constriction at the nucleolar organizing different species are highly diverged and show considerable
region (NOR) (Figure 1). Using conventional DNA stain size variation (Ma et al., 2007). It is now clear that epigenetic
Feulgen these features are particularly well distinguishable mechanisms establish and propagate active centromeres on
(Figure 3d). Chromosome shape is defined by the position of chromosomes, independent of their sequence (Jiang et al.,
the centromere along its length: it can be at one end of the 2003; Carroll and Straight, 2005; Morris and Moazed, 2007;
chromosome (a telocentric chromosome), close to the end Wang et al., 2009).
(acrocentric), near the middle (metacentric), or somewhere Because of the epigenetic nature of centromeres, it is
between the physical middle and the end (submetacentric). possible for a chromosome to have a ‘neo-centromere’ that
The description of the chromosome sizes, usually given as is not always functional (Carvalho et al., 2008). It is also
measurements of physical length made in a microscope, found that centromeres from one species may not nucleate
and the position of the centromeres, gives the karyotype of a microtubules strongly in another species background (e.g.
species. Karyotypes can include a set of very similar sized Ishi et al., 2010), and hence the chromosomes of one species
chromosomes such as seen in rye and wheat (Figures 3a,c do not segregate efficiently and are lost (Figure 2). In the
and 4d), but bimodal karyotypes with several large and a hybrid Hordeum vulgare · Hordeum bulbosum, the chro-
number of smaller chromosomes (Figure 3d) are frequently mosomes from many genotypes of H. bulbosum are lost
seen. during division (Bennett et al., 1976; mechanism investi-
gated by Gernand et al., 2006), giving a haploid H. vulgare
Telomeres
plant where the chromosome number can be doubled to
The Nobel prize-winning work of Blackburn and Szostak generate homozygous plants. A very exciting approach to
discovered that a unique DNA sequence in the telomeres generating haploids came from Ravi and Chan (2010): noting
protects the chromosomes from degradation in many spe- that the centromeres of the eliminated genome were less
cies, and confirmed that indeed each chromosome was able to interact with spindle microtubules, they made
a single, double-stranded DNA molecule. In work with transgenic Arabidopsis plants with a CenH3 protein modi-
A. thaliana, Richards and Ausubel (1988) showed that chro- fied to be less efficient. When crossed to wild-type plants,
mosomes ended with the repeated 7-bp long DNA motif chromosomes from the modified genome were eliminated,
(TTTAGGG)n, which is added by a telomerase enzyme, leading to the formation of haploids.
rather than through semi-conservative replication. This While the monocentric centromere as above is very
event solves the capping and replication problem of the widespread in the plant kingdom, two other types of
ends of a DNA double helix (reviews: Fajkus et al., 2005; centromere structure have been identified in eukaryotes.
Watson and Riha, 2010). Because of this mode of addition The localized point centromere from budding yeast Saccha-
to chromosomes, the copy number of the repeat unit has romyces cerevisiae, with a DNA sequence of about 125 bp
been found to vary both between different cells and diffe- that provides specific kinetochore protein binding sites
rent chromosomes (Figure 4c; Schwarzacher and Heslop- (Morris and Moazed, 2007), seems not to have any sequence
Harrison, 1991). The repetitive motif is not universal, but a similarity with the centromeres of plant and animal eukary-
6 bp motif, as found in many mammals, (TTAGGG)n is otes. The second centromere type is not localized on the
present in some groups of plants (Sykorova et al., 2003a,b). chromosome, but functions to allow microtubules to bind
along their complete length. The first animal to be fully
Centromeres
sequenced, Caenorhabditis elegans, had these diffuse or
The centromere of plant metaphase chromosomes is nor- holocentric centromeres, where the microtubules attach
mally visible as a sharp constriction along its length (Fig- along the whole chromosome. Six families of plants (three
ures 1 and 3a,d), if not present near the end on acrocentric monocots and three eudicots), have holocentric chromo-
chromosomes. It acts as the focus where the proteinaceous somes. Nagaki et al. (2005) showed that CenH3 was localized
kinetochore plate forms, to which the spindle microtubules along the length of the holocentric chromosomes in Luzula.
attach. The centromeres of most plant species include large The association of microtubules along the whole chromo-
arrays of tandemly repeated DNA (Figure 4a; Maluszynska some length was observed by Guerra et al. (2006) in
and Heslop-Harrison, 1991; Brandes et al., 1997; Heslop- Rhynchospora tenuis (2n = 4; Cyperaceae). In this family,
Harrison et al., 1999) and often retrotransposon sequences chromosome number varies up to 2n = circa 200, including
(Gindullis et al., 2001; Wolfgruber et al., 2009). Genomic many chromosomes <10 Mb in size, suggesting that
ª 2011 The Authors
chromosome fragmentation may have occurred during between independent molecules or parts of macromole-
evolution, but the chromosomes are still able to segregate cules. The degree to which this framework involves a
at division by binding microtubules. In contrast to these physical scaffold or is self-organizing remains uncertain. The
exceptionally small chromosomes, another genus with processes involved in ‘decondensation’ of the chromosome
holocentric chromosomes, Cuscuta, has a large average to the interphase nucleus are also, in general, poorly
chromosome size ranging up to 1000 Mb. understood, although likely to involve loops of chromatin
extending from more condensed axes that are visible by
The rRNA sites and the nucleolus
light or electron microscopy. During interphase there may
As well as the centromeres, another constriction or gap is be a gradient across the nucleus in the proportion that is
usually seen on some metaphase chromosomes in a com- filled with chromatin, and chromatin may be more dense
plement – the secondary constriction at the NOR (Figures 1 adjacent to the nuclear envelope, particularly in species with
and 3a, arrow). The NOR corresponds to major sites of the small genomes. The interphase nucleus itself is a dynamic
45S rDNA, consisting of a tandem repeat of a unit with the environment, and both structural components and the DNA
18S–5.8S–26S rRNA genes and their transcribed and move during the interphase. Most obviously, soon after
untranscribed spacer regions (Figure 4b–d). The repeat unit division, rRNA gene expression from multiple chromo-
is typically about 10 kb long, and in Arabidopsis it is present somes (the homologous pair if only one pair of sites is
about 360 times on two pairs of chromosomes, representing present, or sites on several different chromosomes) form
about 5% of the DNA (Copenhaver and Pikaard, 1996; individual nucleoli. At later stages of the cell cycle, these
Heslop-Harrison and Maluszynska, 1994). In other species have normally moved and fused to a smaller number of
with larger genomes, such as wheat, the rRNA genes are larger nucleoli. Interphase nucleus size varies within a single
present at a small number of discrete sites on the chromo- plant: the egg cell is often characterized by a large volume,
somes (Figure 4d), with a larger number of copies of the with the chromatin being much dispersed through the whole
repeat – 1200 at one locus in hexaploid wheat. volume, while the male sperm cell nucleus is highly con-
At interphase, the nucleolus, the most conspicuous densed (Cao and Russell, 1997; Russell et al., 1996).
structure within the nucleus, is the site of transcription of In 2003, Cremer and Cremer wrote ‘there is increasing
the rRNA repeat units and there is little stained DNA within agreement that the study of the functional architecture of
the volume of the nucleolus. Untranscribed copies of the the eukaryotic nucleus will be one of the most important
rDNA are often condensed and locate just outside the post-genomic research areas’. Since writing this, chromatin
nucleolus, while in situ hybridization shows the transcribed research, involving understanding of the interactions of
genes as a decondensed thread running through the DNA and proteins has expanded, and the epigenetic conse-
nucleolus (Figure 4b). quences of chromatin modification have become clear (see
The 18S, 5.8S and 26S rRNA products come together with Fransz and deJong, 2011). However, the relationship
the 5S rRNA and the ribosomal proteins to make the between nuclear organization, gene expression, higher-
ribosomes. The 5S rRNA genes, like the 18S–5.8S–26S rRNA order chromatin arrangements and their interactions with
genes, are present in the genome as a tandem repeat. Both other nuclear components, as considered by Cremer and
the 45S and the 5S rRNA loci are often found to have Cremer (2001) remains a challenge to understand. Shopland
‘rearranged’ as blocks during evolution. In A. thaliana, the and Bewersdorf (2008) discuss how recent advances in light
sites of the 5S rDNA are on different chromosomes in the microscopy are likely to reveal more information about
Landsberg and Columbia ecotypes (Murata et al., 1997). In chromosome structure and function, and point out that
cereals, both the sites of the rDNA and the order of the relatively little is known about the structural, dynamic, and
loci, varies extensively between related species (Castilho mechanical properties of these macromolecular assemblies.
and Heslop-Harrison, 1995). Where genetic maps are avai- Figure 6 illustrates the application of super-resolution
lable, the change in position of the loci is not accompanied microscopy to resolve the synaptonemal complex at
by transfer of regions of genes flanking the moved rRNA meiosis, where conventional light microscopy is unable to
genes. (Dubcovsky and Dvorak, 1995). resolve the two lateral elements that are closer than 300 nm.
Gustafsson et al. (2008) show that advanced systems have
THE CELL CYCLE AND THE INTERPHASE NUCLEUS
wide application to study chromosomal organization at high
The physical structure of the plant cell nucleus changes resolution, so in great detail.
through the cell cycle (Figure 2). The ‘framework’ within
SEX CHROMOSOMES AND SEX DETERMINATION
which these physical events happen can be regarded as the
IN PLANTS
architecture of the nucleus. It is this architecture, in combi-
nation with the linear order of genes along the chromo- More than 95% of angiosperm and gymnosperm species are
somes, that is responsible for the higher-level organization hermaphrodite, bearing flowers with both pollen and ovules
of the nucleus, and the processes related to interactions (as in Arabidopsis or wheat), or monoecious where both
ª 2011 The Authors

plants. Such non-heteromorphic sex-chromosome-like

regions have been described in several crop plants whose
genomes have been sequenced such as papaya, grape and
poplar (grape: Jaillon et al., 2007; papaya, Ming et al., 2008;
poplar, Yin et al., 2008), as well as asparagus, kiwi and
spinach.
Papaya is trioecious with XX female, XY male, and XYh
hermaphrodite (Liu et al., 2004; Zhang et al., 2008). The Y is
evolutionarily young and is estimated to have diverged from
the X 2–3 million years ago. Within its male specific region,
some 13% of the Y, including the centromere and highly
methylated heterochromatic knobs have been found (Zhang
et al., 2008) and numerous chromosomal rearrangements
have been detected (Yu et al., 2008). In poplar, Yin et al.
(2008) have identified a region of one chromosome showing
characteristics of a sex chromosome with a gender-associ-
ated locus. Reduced recombination, distorted segregation
and haplotype divergence was only observed in the female
and consequently sex determination in Populus is an
incipient ZW chromosome system where males are ZZ and
females are the ZW heterogametic sex.
Plant sex chromosome evolution occurred recently, and is
still ongoing, so provides an excellent model to study DNA
sequence and chromosome evolution. It is believed that the
process started with the emergence of sex determining
genes (X has male sterility and female fertility; Y has
maleness factor and female suppressor) followed by sup-
pression of recombination in their surrounding region (for
Figure 6. Super resolution microscopy resolves the lateral elements of the review see Bergero and Charlesworth, 2009; Kejnovsky and
synaptonemal complex. Vyskot, 2010; Navajas-Pérez et al., 2005, 2006). Thus cyto-
Two synaptonemal complexes of meiotic prophase in the domestic pig logical homomorphic sex chromosomes with their hetero-
(Sus scrofa domestica) after immuno-staining with rabbit anti-SCP3 (detected
with goat anti-rabbit Alexa 488; green fluorescence) specific for the lateral morphic DNA regions could represent this first step and are
elements. In imaging with the Leica TCS STED CW in conventional confocal indeed often found to be younger than dimorphic sex
scanning mode (TCS SP5), the two parallel lateral elements that form a gap of chromosomes. The expansion of suppression of recombi-
100–300 nm cannot be distinguished (a). Using the same microscope with the
super-resolution mode enables imaging below the diffraction limit of light nation to the majority of the chromosome is postulated to
by purely optical methods; the two lateral elements can be seen (b). lead to accumulation of deleterious mutations, erosion of
(Micrographs from Kees Straatman and Trude Schwarzacher who thank genes caused by insertion of retroelements or DNA trans-
Leica Microsystems Milton Keynes UK for use of the microscope).
posons and finally degeneration. As a result heteromorphic
sex chromosomes emerge that are often larger than the
autosomes in plants (Figure 3b) due to accumulation of
male and female flowers are carried on the same plant (as in repetitive DNA elements (see below) and are in contrast to
maize) (Dellaporta and Calderon-Urrea, 1993). Some 4% of the small mammalian Ys that are much older and have been
plants are dioecious, where male and female flowers are allowed to lose genes by rearrangements (Bergero and
carried on different plants and, in most of these, sex is Charlesworth, 2009).
determined genetically. Dioecy is thought to have evolved Molecular investigations have shown that the Y chromo-
relatively recently and independently in a number of plant some of Silene latifolia estimated to be about 10 million
families. In a few cases, dimorphic sex chromosomes were years old shows all of the above signs of sex chromosome
found such as in the ‘classic’ examples of Rumex species evolution including genetic degeneration, reduction of DNA
and Silene latifolia, as well as Humulus, Cannabis and Coc- polymorphism, accumulation of mutations at important
cinia (see Figure 3b; Kejnovsky and Vyskot, 2010; Navajas- functional sites coding for proteins, and gene expression
Pérez et al., 2005, 2009; Vyskot and Hobza, 2004). When changes (see Armstrong and Filatov, 2008; Filatov et al.,
cytologically homomorphic sex chromosomes are present, 2009). Analysis of the repetitive DNA distribution and
gene differences and sex-determining genes, including a comparing female and male DNA sequences on S. latifolia
MSY (male specific Y) region are found in male and female sex chromosomes, has revealed that parts of the Y
ª 2011 The Authors

chromosome have diverged from the X at different times physical reorganization. Following completion of the Ara-
and can be divided into ‘strata’ similar to the human Y. bidopsis and other genome sequences, the widespread
Different amounts of various DNA sequence families, from presence of segmental and whole genome duplications
almost all classes of repeats known in plants, are present on across angiosperms is much more frequent than was sus-
the Y in large numbers. Cermak et al. (2008) undertook a pected from earlier studies. Comparative genomics using
survey of all repeats on the Y of S. latifolia and found in whole genome sequencing complemented by molecular
decreasing abundance, subtelomeric tandem repeats, gypsy cytogenetics has provided new insights into the nature of
and copia like retroelements, followed by LINEs and SINEs chromosomal rearrangements including fusions, fissions,
and DNA transposons including hATs and MITES. Interest- inversions, deletions and duplications, across a much wider
ingly, they and Filatov et al. (2009) found a transposable groups of plants than has been possible with cytogenetic
element (TE) abundant on autosomes that is excluded on the approaches alone. These episodic events combine with
Y indicating a divergent evolution of DNA sequences on sex continuous processes including sequence mutation, trans-
and autosomal chromosomes. posable element accumulation, tandem repeat amplification
Accumulation of repetitive DNA sequences has also been and sequence homogenization. Improved methods of
seen in the genus Rumex, which contains several species chromosomal analysis with in-situ hybridization and use of
with dimorphic sex chromosomes and a derived com- antibodies are assisting characterization of genome-wide
plex XX/XY1Y2 system in R. acetosa, R. papilaris and and chromosome-level changes in the genome. The
R. hastatulus (Navajas-Pérez et al., 2006, 2009; see also fundamental insights gained from these studies are now
Figure 3b). The Y degeneration in XX/XY1Y2 system was showing how genomes evolve and how diversity can be
accompanied by massive accumulation of repetitive DNA generated.
followed by chromosomal rearrangements giving rise to the So far, the controls on many features of chromosome
multiple Y chromosomes (Mariotti et al., 2009; Navajas- organization and their variability remain to be elucidated.
Pérez et al., 2009). The loss of recombination between X and Why should different species have genomes varying in size
Y chromosomes would reduce the evolutionary rate of by more than 2000-fold, and both chromosome number and
Y-specific satDNAs, but also hinders intra-specific homo- chromosome sizes vary by 300-fold? The behaviour of these
genization processes. As a consequence, different rates of genomes seems to be similar in terms of replication, gene
evolution have been found for autosomal and sex chromo- expression, control and evolution, or at least differences do
some variants of repeats, and differential patterns of Y-het- not reflect the huge variation in genome organization.
erochromatin as well as the presence of different Indeed, it is remarkable that the same genetic, segregation,
subfamilies and related satDNAs in different regions of the expression, replication and evolutionary mechanisms seem
Y chromosomes (Mariotti et al., 2009; Navajas-Pérez et al., to be applicable over this large range. Crop plants represent
2006, 2009). Further the Y chromosome experienced many an intensively selected subset of <0.1% of the 400 000
inversions of various extents. angiosperm species, and fewer than 30 species provide
Additional evidence of repeat accumulation at different more than 97% of the world’s food (FAOstat, 2010). Even
times during the evolution of the Y chromosomes, comes among the top crops, the variation in nature of genomes is
from the studies of simple sequence repeats that have evident with diploids, recent polyploids, and hybrid species,
accumulated in the Y chromosome of Silene especially in the and genome sizes between 465 Mb in rice to 17 000 Mb
longer arm which has stopped recombining relatively in wheat. Exploiting the diversity and evolutionary mecha-
recently and harbours no other repeats yet (Kejnovsky et al., nisms in plant genomes is likely to be a key to crop
2009). In Rumex acetosa several simple sequence repeats development for food production.
including (ACC) (see Figure 3b; Karwur, 2001) are found
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The Plant Journal (2011) 66, 18–33 doi: 10.1111/j.1365-313X.2011.04544.

THE PLANT GENOME: AN EVOLUTIONARY VIEW ON STRUCTURE AND FUNCTION

Organisation of the plant genome in chromosomes

Received 31 January 2011; revised 11 February 2011; accepted 15 February 2011.

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Short arm Long arm

Telomere NOR Centromere Telomere

Chromosome regions: Pericentric Intercalary Subtelomeric

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tae (2n = approximately 40), to the largest of Paris japonica

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genome has been triplicated during its early evolution,

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analysis has shown the presence of actively transcribed

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plants. Such non-heteromorphic sex-chromosome-like

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ª 2011 The Authors

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